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Left Versus Right
Asymmetries of
Brain and Behaviour
Edited by
Lesley J. Rogers
Printed Edition of the Special Issue Published in Symmetry

www.mdpi.com/journal/symmetry
Left Versus Right Asymmetries of
Brain and Behaviour
Left Versus Right Asymmetries of
Brain and Behaviour

Special Issue Editor

Lesley J. Rogers

MDPI • Basel • Beijing • Wuhan • Barcelona • Belgrade

Special Issue Editor
Lesley J. Rogers
University of New England
Australia

Editorial Office
MDPI
St. Alban-Anlage 66
4052 Basel, Switzerland

This is a reprint of articles from the Special Issue published online in the open access journal Symmetry
(ISSN 2073-8994) from 2018 to 2019 (available at: https://www.mdpi.com/journal/symmetry/
special issues/Left Versus Right Asymmetries of Brain and Behaviour)

For citation purposes, cite each article independently as indicated on the article page online and as
indicated below:

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Page Range.

ISBN 978-3-03921-692-5 (Pbk)

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Cover image courtesy of Gisela Kaplan.


c 2019 by the authors. Articles in this book are Open Access and distributed under the Creative
Commons Attribution (CC BY) license, which allows users to download, copy and build upon
published articles, as long as the author and publisher are properly credited, which ensures maximum
dissemination and a wider impact of our publications.
The book as a whole is distributed by MDPI under the terms and conditions of the Creative Commons
license CC BY-NC-ND.
Contents

About the Special Issue Editor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii

Preface to ”Left Versus Right Asymmetries of Brain and Behaviour” . . . . . . . . . . . . . . . ix

Elisa Frasnelli and Giorgio Vallortigara

Individual-Level and Population-Level Lateralization: Two Sides of the Same Coin
Reprinted from: Symmetry 2018, 10, 739, doi:10.3390/sym10120739 . . . . . . . . . . . . . . . . . 1

Emily R. Boeving and Eliza L. Nelson

Social Risk Dissociates Social Network Structure across Lateralized Behaviors in
Spider Monkeys
Reprinted from: Symmetry 2018, 10, 390, doi:10.3390/sym10090390 . . . . . . . . . . . . . . . . . 11

Emre Ünver, Qian Xiao and Onur Güntürkün

Meta-Control in Pigeons (Columba livia) and the Role of the Commissura Anterior
Reprinted from: Symmetry 2019, 11, 124, doi:10.3390/sym11020124 . . . . . . . . . . . . . . . . . 20

Lesley J. Rogers, Adam Koboroff and Gisela Kaplan

Lateral Asymmetry of Brain and Behaviour in the Zebra Finch, Taeniopygia guttata
Reprinted from: Symmetry 2018, 10, 679, doi:10.3390/sym10120679 . . . . . . . . . . . . . . . . . 31

Martine Hausberger, Hugo Cousillas, Anaı̈ke Meter, Genta Karino, Isabelle George, Alban
Lemasson and Catherine Blois-Heulin
A Crucial Role of Attention in Lateralisation of Sound Processing?
Reprinted from: Symmetry 2019, 11, 48, doi:10.3390/sym11010048 . . . . . . . . . . . . . . . . . . 47

Michio Hori, Masanori Kohda, Satoshi Awata and Satoshi Takahashi

Dynamics of Laterality in Lake Tanganyika Scale-Eaters Driven by Cross-Predation
Reprinted from: Symmetry 2019, 11, 119, doi:10.3390/sym11010119 . . . . . . . . . . . . . . . . . 64

Catarina Vila Pouca, Connor Gervais, Joshua Reed and Culum Brown
Incubation under Climate Warming Affects Behavioral Lateralisation in Port Jackson Sharks
Reprinted from: Symmetry 2018, 10, 184, doi:10.3390/sym10060184 . . . . . . . . . . . . . . . . . 73

Marcello Siniscalchi, Daniele Bertino, Serenella d’Ingeo and Angelo Quaranta

Relationship between Motor Laterality and Aggressive Behavior in Sheepdogs
Reprinted from: Symmetry 2019, 11, 233, doi:10.3390/sym11020233 . . . . . . . . . . . . . . . . . 82

Shanis Barnard, Deborah L. Wells and Peter G. Hepper

Laterality as a Predictor of Coping Strategies in Dogs Entering a Rescue Shelter
Reprinted from: Symmetry 2018, 10, 538, doi:10.3390/sym10110538 . . . . . . . . . . . . . . . . . 90

v
About the Special Issue Editor
Lesley J. Rogers is a Fellow of the Australian Academy of Science and Emeritus Professor at the
University of New England, Australia. After being awarded a First-Class Honours degree by the
University of Adelaide, she studied at Harvard University in USA and then the University of Sussex,
UK. She was awarded a Doctor of Philosophy and, later, a Doctor of Science from the University of
Sussex, UK. After returning to Australia, she held academic positions at Monash University and the
University of New England. Her publications, numbering over 500, include 18 books and over 280
scientific papers and book chapters, mainly on brain and behaviour. In the 1970s, her discovery of
lateralized behaviour in chicks was one of three initial findings that established the field of brain
lateralization in non-human animals, now a very active field of research. Initially, her research
was concerned with the development of lateralization in the chick as a model species, and the
importance of light stimulation before hatching, which she investigated at the neural and behavioural
levels. She then compared lateralized behaviour in different species spanning from bees to primates
and, more recently, has focused on the advantages of brain asymmetry and the link between social
behaviour and population-level asymmetry. Her other roles include Editor of the journal Laterality
and Academic Editor of numerous other scientific journals.

vii
Preface to ”Left Versus Right Asymmetries of Brain
and Behaviour”
Asymmetry of the brain and of behaviour is a characteristic of a wide range of vertebrate species,
as shown by an increasing number of studies testing animals in the laboratory and in the natural
environment. Some asymmetries of behaviour have also been found in invertebrate species. Given
its ubiquity, lateralization must confer an advantage for survival, despite the apparent disadvantages
of side biases in perception and response. A disadvantage of lateralized responding is evidenced
by the fact that many species are more likely to respond to a predator when it is seen on their left
side and to their prey when it is seen on their right side. How do different species deal with these
asymmetries? The topics covered in this book address this question and report further evidence
of lateralized brain and behaviour in non-human species. In addition, the brain function involved
in lateralized processing and control of response is discussed, and also the relationship between
lateralized behaviour and animal welfare.
The paper by Frasnelli and Vallortigara addresses the question of why the majority of individuals
in a population are lateralized in the same direction (population-level lateralization). They show
that, although the cognitive advantage of having a lateralized brain places no constraints on the
direction of lateralization, population-level lateralization develops as an evolutionary stable strategy
when lateralized organisms must co-ordinate their behaviour with other lateralized organisms. This
explains why population-level lateralization is a characteristic of social species. In this paper, the
authors affirm that population-level asymmetry is also an advantage in so-called “solitary” species
when individuals have to interact, as in aggressive and mating behaviour. They clarify an important
point about inter-individual interaction and the evolution of lateralization as an evolutionary stable
strategy.
The paper by Boeving and Nelson considers the link between social and affiliative behaviour
from another perspective; by relating research showing that lateralization influences social structure
in spider monkeys. Previous research had shown that social affiliative behaviour—embrace and
face-embrace—in spider monkeys is left-side biased. In this paper, the authors apply social network
analysis and find that laterality of affiliative behaviour influences social structure. Network patterns
that are left-lateralized for affiliative behaviour are more cohesive than those that are right lateralized.
The paper by Üver, Xiao and Güntürkün reports research on the mechanism by which the brain
deals with the conflicting responses elicited by each hemisphere’s differing reaction to the same
stimulus. In short, they reveal how one hemisphere achieves dominance (meta-control) over the
other. Experiments addressing this issue involved sectioning the anterior commissure of pigeons,
the largest commissure connecting the left and right sides of the avian brain. The results showed
that meta-control is modified by interhemispheric transmission via this commissure, although it does
not seem to depend entirely on it. The results suggest that the two hemispheres compete to take
control of a particular behaviour and they do so on the basis of their processing speed. Since the
hemisphere specialised to respond to a particular stimulus processes information faster than the other
hemisphere, it takes control of the response.
From early research on lateralization of song production in the zebra finch, there has been
speculation about the possibility that lateralization in this species differs from the general pattern
found in other avian species and generally in vertebrates. The chapter by Rogers, Koboroff and
Kaplan discusses more recent evidence refuting this idea and reports experimental evidence showing

ix
that population-level lateralization is present in preferred-eye use by zebra finches when they view
a predator. Since zebra finches often alternate looking with the monocular field of one eye and then
the other eye, a new method had to be developed in order to score eye preferences. The experiments
showed that the birds have a significant preference to view a monitor lizard with their left-eye (using
their right hemisphere). This result is discussed together with evidence of other asymmetries in zebra
finches, for visual searching and courtship behaviour and for processing, producing and learning of
song. The authors conclude that, contrary to earlier suggestions, the zebra finch brain is lateralized
with the same pattern as that of that found in other vertebrate species.
Hausberger and colleagues consider lateralization of auditory processing. Auditory stimuli of
differing salience (e.g., familiar versus novel sounds) were presented to Campbell’s monkeys and
only novel sounds elicited laterality. The monkeys had a significant right-hemisphere preference
to attend to novel sounds but no preference to attend to familiar sounds. The authors also
considered auditory lateralization in starlings. In starlings, the right hemisphere was found to process
sounds of individual identity, whereas the left hemisphere was more involved in processing socially
meaningless stimuli. The authors suggest an attention-based explanation to reconcile the different
hypotheses about right-hemisphere specialisation.
Although many behavioural responses have a directional bias within the population, some types
of laterality occur with equal numbers of left and right biased individuals in the population. Laterality
in scale-eating cichlid fishes is such an example, discussed in the chapter by Hori and colleagues.
These fish have asymmetry of the body, in the direction of the mouth opening either to the left or right
side. The distribution of laterality within a population is bimodal (anti-symmetry). The authors have
investigated the relationship between behavioural laterality and morphological asymmetry in two
species studied over three decades. They found that the dimorphism is maintained dynamically with
a cycle of four years oscillating between more left and more right individuals. This cycling is caused
by frequency-dependent selection (the minority type having an advantage) between predator and
prey species. Since both predator and prey fish are lateralized, the authors examine cross-predation
versus parallel-predation in terms of the physical and sensory abilities of fishes.
The development of lateralization in Port Jackson sharks is dependent on temperature of the
sea, as Pouca et al. report. They found that, under water temperatures predicted for the end of
the century, development of sharks is affected, as seen by measuring preferences of direction taken
during a detour test. Sharks incubated at the higher temperature had stronger lateralization (biased
to detour to the right) than did sharks incubated at current sea temperature. The authors suggest that
this change in lateralization might be a way by which the species could cope with deleterious effects
of climate change.
Two papers deal with different aspects of laterality in dogs and its relationship to behaviour and
welfare. The paper by Siniscalchi and colleagues reports on turning behaviour in sheepdogs. The
dogs showed significantly more aggressive behaviour toward the sheep when they were circling
the herd in an anticlockwise direction and so could see the sheep in their left visual field and
process the information in their right hemisphere. Dominance of the right hemisphere in aggressive
behaviour has been found also in a number of other vertebrate species. As the authors say, this
relationship between motor lateralization and aggressive behaviour has practical implications for
training sheepdogs.
The paper by Wells and colleagues relates laterality to the welfare of dogs. The subjects were
rescued dogs and they were tested during the first week after they had been placed in a rescue shelter.

x
Paw preference measured in a food-retrieval task was linked to stress-related behaviour. The results
showed that stronger left-paw preference was associated with higher stress-related behaviour, such
as frequent change of state, vocalisations and lower body posture. This finding is in keeping with
other findings of the association between left-limb preference and vulnerability to stress. The authors
suggest that testing paw preference may be a useful tool for detecting different coping strategies in
dogs entering a kennel environment and for targeting individuals at risk of experiencing reduced
welfare.

Lesley J. Rogers
Special Issue Editor

xi
SS symmetry
Concept Paper
Individual-Level and Population-Level Lateralization:
Two Sides of the Same Coin
Elisa Frasnelli 1, * and Giorgio Vallortigara 2
1 School of Life Sciences, University of Lincoln, Lincoln LN6 7DL, UK
2 Center for Mind/Brain Sciences, University of Trento, Piazza della Manifattura 1, I-38068 Rovereto, Italy;
giorgio.vallortigara@unitn.it
* Correspondence: efrasnelli@lincoln.ac.uk

Received: 21 November 2018; Accepted: 7 December 2018; Published: 11 December 2018

Abstract: Lateralization, i.e., the different functional roles played by the left and right sides of
the brain, is expressed in two main ways: (1) in single individuals, regardless of a common
direction (bias) in the population (also known as individual-level lateralization); or (2) in single
individuals and in the same direction in most of them, so that the population is biased (also known
as population-level lateralization). Indeed, lateralization often occurs at the population-level, with
60–90% of individuals showing the same direction (right or left) of bias, depending on species and
tasks. It is usually maintained that lateralization can increase the brain’s efficiency. However, this may
explain individual-level lateralization, but not population-level lateralization, because individual
brain efficiency is unrelated to the direction of the asymmetry in other individuals. From a theoretical
point of view, a possible explanation for population-level lateralization is that it may reflect an
evolutionarily stable strategy (ESS) that can develop when individually asymmetrical organisms
are under specific selective pressures to coordinate their behavior with that of other asymmetrical
organisms. This prediction has sometimes been misunderstood as it is equated with the idea that
population-level lateralization should only be present in social species. However, population-level
asymmetries have been observed in aggressive and mating displays in so-called “solitary” insects,
suggesting that engagement in specific inter-individual interactions rather than “sociality” per se may
promote population-level lateralization. Here, we clarify that the nature of inter-individual interaction
can generate evolutionarily stable strategies of lateralization at the individual- or population-level,
depending on ecological contexts, showing that individual-level and population-level lateralization
should be considered as two aspects of the same continuum.

Keywords: lateralization; individual-level; population-level; evolution; ESS; social interactions

1. Introduction
Lateralization, defined as the different specialization of function of the left and right sides of the
nervous system, is a widespread phenomenon in the animal kingdom. In the last three decades, many
studies have provided evidence that many animal species, from the evolutionarily closest to the most
evolutionarily distant from humans, show asymmetrical biases in behavior [1]. Examples range from
the asymmetrical use of limbs to handle objects or perform motor activities (for a review, see [2]) to
the asymmetrical use of sensory pair organs, such as eyes, nostrils, ears, and antennae to detect a
specific stimulus, such as a potential predator; from motor biases in escape directions or navigation
to the asymmetrical processes involving learning and memory and the processing of emotions [3,4].
All this evidence of brain and behavioral asymmetries in vertebrates [1], together with some in
invertebrates [5,6], suggests that having an asymmetrical brain must confer advantages to complex
brains, as well as to “simpler” ones.

Symmetry 2018, 10, 739; doi:10.3390/sym10120739 1 www.mdpi.com/journal/symmetry

Symmetry 2018, 10, 739

Lateralization varies in strength (an individual may be less or more strongly lateralized) and
direction (left or right) among individuals of the same species, of different species, and also depending
on the task considered. Moreover, it can be present at the individual- or population-level (when most
individuals within the population show the same direction of bias). Population-level lateralization
has been explained as a consequence of selective social pressures that have pushed individuals to
coordinate with each other and align their biases in the same direction [7]. In this paper, we discuss the
advantages and disadvantages connected with having a (less or more) strong lateralized brain and the
complexity of this fascinating phenomenon, while claiming that individual-level and population-level
lateralization should be interpreted as two aspects of the same continuum.

2. Advantages of Having an Asymmetrical Brain (at the Individual Level)

Having an asymmetrical brain provides several advantages (see, for an extensive discussion, [7–9]).
If the left and right sides of the brain perform different functions, it is possible to save energetic
resources in cognitive tasks. Indeed, lateralization avoids the duplication of functions in the two
hemispheres (otherwise, animals should probably have a brain double the size). Another big advantage
related to lateralization consists of the possibility to separately and simultaneously process external
stimuli, increasing the efficiency of the cerebral capacity. This is particularly easy to observe in animals
with laterally placed eyes, such as birds, which mainly have monocular vision when using their lateral
visual fields, i.e., they use their right and their left eye separately. More precisely, in birds, the lateral
part of the right retina only communicates with the left hemisphere and vice versa. Because of this
peculiarity, species such as the domestic chick Gallus gallus have been widely studied to assess the
preferential use of the left and right side of the brain in specific tasks [10,11]. Chicks are better at
discriminating grains of food from pebbles randomly mixed on the ground when they use their right
eye (and thus their left hemisphere as, in vertebrates, the left hemisphere controls the right part of the
body and vice versa; [12] see also for quails [13]). At the same time, chicks are better at detecting the
presence of a potential predator when this appears in their left visual hemi-field (and it is perceived by
their left eye and thus by the right hemisphere; [12]). Because of this functional specialization, chicks
can feed from the ground using their right eye and, simultaneously, they can keep their left eye ready
to respond to and protect themselves from potential predators [14].
Furthermore, when one hemisphere controls a specific behavior (for example, detecting potential
predators), it is not competing with the other hemisphere to take control of that specific behavior.
This leads to a more rapid and efficient response. Cerebral lateralization is indeed linked to better
cognitive performances. Some studies have shown that more strongly lateralized individuals are more
successful in some cognitive tasks compared to weakly lateralized conspecifics. In fact, behavioral
asymmetries may vary not only in direction, but also in strength, among different individuals of the
same species: some individuals can be more or less left-biased, others right-biased, and yet others
unbiased. This is the case, for example, for chimpanzees, when fishing for termites using a stick:
individuals with a strong preference to consistently use one hand (regardless of whether it is the left
or the right one) are more efficient than individuals that do not have any preference to use one or
the other hand [15]. Children with consistent early hand preferences exhibit advanced patterns of
cognitive development compared to children who develop a hand preference later, although this could
be a matter of synchronized development [16]. Strongly lateralized parrots showing a significant foot
and eye preference are better at solving novel problems, such as a pebble-seed discrimination test and
a string-pull problem, than less strongly lateralized parrots [17]. In domestic chicks (Gallus gallus), a
right-eye superiority has been documented in inhibiting pecks at pebbles while searching for grain
and this ability is impaired when lateralization is not present [14,18]. Similarly, pigeons (Columba livia
domestica) with the strongest eye lateralization in discriminating grains from pebbles are the most
successful in selecting grains when tested binocularly, suggesting that stronger lateralization increases
the efficiency of a performance [19].

2
Symmetry 2018, 10, 739

Surprisingly, insects also seem to have a preference for using one limb. Locusts crossing a gap
have been shown to preferentially use the left or the right leg in this task [20]. Different individuals
showed different biases not only in the direction (left or right), but also in the strength of the bias.
However, as in chimpanzees [15], the individuals with a strong preference were those that made fewer
mistakes in the task and thus were most successful [21]. This suggests that in this specific context,
stronger lateralization confers a benefit in terms of improved motor control. Strong lateralization also
seems to influence learning ability, as shown in larval antlions (Myrmeleon bore), with strong lateralized
righting behavior being better at associating a vibrational cue with prey removal [22].
Not only behavioral asymmetries may vary in direction and strength among different individuals
of the same species; biases can also change, depending on the task that an animal is performing
(e.g., handedness in marmosets, [23]). This indicates that lateralization is a complex phenomenon that
varies at the species, group, and individual level, bringing us to the question of what are the advantages
of having individuals with different biases in the population. Individuals with a strong lateralization
seem to have an advantage in terms of improved motor control [15,21] or problem solving [14,17–19].
However, in strongly lateralized fish, a consistent lateral bias to turn in one direction reduces their
ability to orient in a maze [24]. This makes the scenario more complex and opens further questions
about the optimal degree (and direction) of bias that an individual should have, depending on the task
and functional context.
In sage grouse (Centrocercus urophasianus), successfully mating males are in general more strongly
lateralized in courtship behavior than non-mating males, but this depends on the behavior of the
male and the social environment in which he is acting [25]. Larger male fallow deer (Dama dama)
display a greater tendency to show a right-sided bias when terminating the parallel walk during
fights and they terminate parallel walks sooner than smaller individuals, suggesting that lateralization
provides a mechanism by which contestants can resolve contests at a low cost [26]. Accordingly, in
dyadic contests, domestic pigs (Sus scrofa) with strong lateralization in the orientation towards their
opponent (regardless of the direction) have a shorter contest duration than conspecifics with a weak
bias. However, although lateralization seems to play a role in conflict resolution, it does not influence
fighting success, as winners and losers showed a similar strength and direction of bias [27]. Less
lateralized wild elk (Cervus canadensis) for front-limb biases (i.e., handedness) respond more intensely
to aversive stimuli (predator-resembling chases by humans), but the same animals are also more
inclined to reduce their flight responses (i.e., habituate) to human approaches when the latter are
benign [28]. On the other hand, more lateralized elks are bolder and more likely to move around,
whereas less lateralized animals tend to remain near humans year-round [28].
Substantial individual variation in the strength of cerebral lateralization may be associated with
individual variation in behaviour. For example, non-lateralized domestic chicks emitted more distress
calls and took longer to resume pecking at food after exposure to a simulated predator than lateralized
chicks [29]. Strongly lateralized convict cichlids (Amatitlania nigrofasciata) are quicker to emerge from a
refuge indicative of boldness [30]. The degree of laterality seems to be positively correlated with stress
reactivity in Port Jackson sharks (Heterodontus portusjacksoni) [31].
Recently, Whiteside and colleagues [32] showed that pheasants with a strong foot preference in
motor tasks were more likely to die earlier in natural conditions than conspecifics with a mild foot
preference. This study is the first trying to link lateralization with fitness in terms of survival and seems
to suggest that the degree of lateralization does not linearly associate with benefits and that there is an
optimum degree of laterality for pheasants in order to get the highest fitness (i.e., survival). Indeed, as
stated by Rogers, Vallortigara and Andrew [1], arguing for computational advantages associated with
the possession of an asymmetrical brain is not the same as arguing that the more asymmetric a brain,
the more computationally-efficient it will be. In humans, there is a clear inverted U-shape curve in
the relationship between degree of laterality and performance in word matching and face decision
tasks [33], suggesting that a moderately asymmetrical brain would provide the greatest advantage.
Finally, the relationship between lateralization and performance is task dependent [34]; therefore, a

3
Symmetry 2018, 10, 739

degree of laterality that may benefit one task may not benefit another. Survival requires an individual
to detect predators, discriminate and handle food, cope with disease, navigate a complex environment,
and learn strategies and much research on proxy measures of fitness looks at single factors, often in
highly controlled environments.

3. Population-Level Lateralization as an Evolutionarily Stable Strategy (ESS)

Lateralization presents an intriguing aspect: it is often present at the population-level
(i.e., directional asymmetry, where more than 50% of individuals within a population show the same
direction of bias, such as handedness in humans, where about 90% of people are right-handed; [35]).
If lateralization confers several advantages to the single individual in terms of brain efficiency, this
cannot explain the alignment of the bias in the population.
The first evidence for a role of social behavior in population-level lateralization was provided by
Rogers and Workman [36], who showed that more strongly lateralized chicks acquire a higher position
in the social hierarchy than less lateralized chicks. Subsequently, Vallortigara and Rogers [7] reviewed
the overall evidence and argued for a role of social interaction in the evolution of population-level
brain asymmetry. The hypothesis was supported by a theoretical model developed by Ghirlanda
and Vallortigara ([37]; see also [38]) showing that, in the context of prey-predator interactions,
population–level lateralization can develop as an evolutionarily stable strategy (ESS) when individually
asymmetrical organisms must coordinate their right-left behavioral patterns with those of other
asymmetrical organisms. As a lateralized brain leads to behavioral biases when escaping from
predators (e.g., [39]), the model considered the fitness consequences that the lateralization of one prey
has when it interacts with other group-living prey subject to predation. The model assumed that the
fitness was influenced by two contrasting selection pressures: (1) the benefit of being lateralized in
the direction of the majority as a consequence of the “dilution effect” (i.e., prey in large groups have a
lesser risk of being targeted by predators; [40]); and (2) the cost of being lateralized in the direction of
the majority as a consequence of predators learning to anticipate prey escape strategies. In this second
case, individuals who escape in a different direction from the majority have a benefit as they can
surprise predators and survive more often. By varying the contribution of these costs and benefits, the
model showed that population-level lateralization emerges as an ESS when neither of the two selection
pressures is much stronger than the other. Thus, the successful strategy of group-living prey is to
have a majority of individuals gaining protection from the group and escaping in the same direction
when facing a predator and a minority of them being able to surprise the predator by escaping in
the opposite direction. Empirical support for this hypothesis comes from fish schools, where animals
showing the same turning bias as the majority of the group have an improved escape performance
than fish at odds with the group [41].
A few years later, the mathematical model by Ghirlanda and Vallortigara [37] was extended
by considering intraspecific interactions instead of interspecific prey-predator interactions [42].
Specifically, the new model considered the selective pressures of synergistic (cooperative) and
antagonistic (competitive) interactions on individuals being lateralized in the same or opposite
direction within the same species. It assumed that individuals lateralized in the same direction
have a benefit in engaging in synergistic interactions as they can, for example, efficiently use the same
tools or coordinate better. On the other side, individuals lateralized in the direction different from that
of the majority have an advantage when engaging in antagonistic interactions for the same reason as
in the previous model: they can surprise the opponent by adopting a strategy to which opponents
are less accustomed. Empirical support for this assumption comes from the success of left-handers
(i.e., lateralized in the opposite direction compared to the majority) in competitive sports such as
fencing, boxing, and tennis (e.g., [43]; see also [44]). The ESS model for intraspecific interactions [42]
showed that when the pressure of synergistic interactions becomes more and more important compared
to that of antagonistic interactions, individually asymmetric organisms must interact with conspecifics

4
Symmetry 2018, 10, 739

and coordinate their activities and, consequently, asymmetry aligns in the majority of individuals in a
population (i.e., directional or population-level asymmetry).
In order to provide empirical evidence for this prediction, the relationship between the level
of lateralization and the presence of social behaviors was investigated using different species of
bees as a model system (summarized in [45]; see also [46]). A series of experiments provided
striking evidence that the alignment of lateralization within the population may be a consequence
of social interactions frequently encountered during the course of evolution [47–49]. In fact, eusocial
honeybees Apis mellifera [47], three species of primitively social Australian stingless bees [48], and
annual social bumblebees Bombus terrestris [49], but not the solitary bees Osmia rufa [47], were found to
be asymmetrical at the population-level for the use of the left and right antennae in recalling olfactory
memories. However, all these studies investigated the use of a preferred antenna in recalling a learnt
memory of an association between an odor and a food reward, and not really social interactions.
The first evidence of the role of antennal asymmetries in social interactions was shown in highly
social ants Formica rufa [50]. By looking at “feeding” contacts where a “donor” ant exchanges food with
a “receiver” ant through trophallaxis, the researchers [50] observed population-level asymmetry, with
the “receiver” ant using the right antenna more frequently than the left antenna. The role of antennal
asymmetries has also been investigated by observing the behavior of different dyads of honeybees
with only the left, only the right, or both antennae in use, and belonging to the same or different
hives [51]. In bees belonging to the same hive, dyads having only the right antenna in use took less
time to get in contact and interacted more positively then dyads with only the left antennae, which
instead interacted more aggressively than the other two groups. Interestingly, for bees belonging to
different hives, dyads with only the right antenna in use displayed more aggressive interactions than
bees with only the left or both antennae [51]. This suggests that the right antenna seems to control
the correct behavioral response, depending on the social context, i.e., positive interactions between
individuals of the same colony and negative interactions between individuals belonging to different
colonies. A similar pattern of behavior between individuals of the same colony has been found in
primitively social stingless bees Trigona carbonaria, where the right antenna stimulates positive contact
and the left stimulates avoidance or attack [52].
Advantages of the population-level lateral bias have also been documented in the preference for
keeping the mother on the left side in several terrestrial and aquatic mammal infants, supporting the
idea of the role that lateralization plays in social interaction [53].

4. Individual- or Population-Level Lateralization as an ESS

Only recently, however, our research provided surprising findings: not only social species, but
also so-called “non-social” species, of insects show asymmetries at the population-level when their
limited interactions with others individuals are considered. This is the case for Osmia rufa, a species
that does not show behavioral asymmetry in the recall of short-term olfactory memory [47], but shows
population-level lateralization in aggressive displays [54], similarly to eusocial honeybees [51] and
social stingless bees T. carbonaria [52]. Clearly, being engaged in interactions with other individuals,
rather than the way in which the species nests (socially or not), may affect lateralization.
In honeybees, so far, all the identified biases occur at the population-level: in the use of the right
visual pathway to learn visual stimuli [55], in the different use of the antennae in learning and recall
of olfactory memories [56–58], and in context-dependent social interactions with conspecifics [51].
A recent study, however, suggests that honeybees tested in a tunnel with gaps of different apertures to
the right and left sides, do not show population-level lateralization [59]. In this task, some individuals
showed a bias to the right, some others a bias to the left, and yet others no bias. This may indicate
that behavioral biases in bees vary in strength and direction, depending on whether the task requires
coordination among individuals. Note, however, that very few bees showed individual bias in this
task, and thus it is not clear whether individual lateralization was observed. Another example may be
provided by foragers of F. pratensis ants, a species which does not use trail pheromones, moves more

5
Symmetry 2018, 10, 739

often to the left side than to the right whilst walking towards the nest, and does not show any bias
when leaving the nest [60]. Moreover, it is still not clear to what extent the alignment occurs. Red wood
ants Formica rufa belonging to different colonies show population-level biases in different directions
when tested for forelimb preference during a gap crossing task, suggesting that social pressures act to
coordinate individuals within the same colony and not necessarily at the species-level [61].
The different types of social interaction can generate evolutionarily stable strategies of
lateralization at the individual- or population-level, depending on ecological contexts. Indeed, as
we showed, population-level asymmetries have been observed in aggressive and mating displays in
so-called “solitary” insects (e.g., tephrid flies, [62]; mason bees, [54]), suggesting that engagement in
specific inter-individual interactions rather than “sociality” in general may generate population-level
lateralization. This implies that lateralization is not necessarily a static feature of the neural
organization, but is modulated by the functional context. For example, the nematode C. elegans exhibits
a pronounced motor bias: males show a right-turning population-bias during mating. Interestingly,
this motor bias is also observed in nematodes with mirror–reversed anatomical asymmetry, perhaps
driven by epigenetic factors rather than by genetic variation [63].
The hypothesis that lateralization arises as an ESS is general and thus can predict either
population- or individual-level lateralization, depending on the type of interactive behavior considered
(e.g., cooperative or competitive) and ecological context. Although the advantage of being aligned
in the same direction is clear in cooperative behavior, it is not in aggressive interactions. Indeed, it
may be more advantageous for an aggressive display to not be directional, since population-level bias
would also mean predictability [7]. For example, if an individual attacks another individual, it would
be more convenient for it to be unpredictable. As a consequence, although each individual would have
an (individual-level) bias, there will be 50:50 right:left-biased individuals in the population. This is
the case for some predators, such as sailfish, which are lateralized at the individual-level in attacking
schooling sardines on one side (and the stronger they are lateralized, the more successful they are at
capturing their prey), but that overall, do not show a population-level bias [64]. However, if we think
specifically about aggressive displays (and not the interactions), the alignment within the population
may be linked to the need of an individual to position itself in a congruent way from a postural/motor
point of view, as happens in mating (for a review, see [65]).
If being aligned in the same direction may help individuals to better coordinate with each other
in specific tasks that require coordination between two or more individuals, being more or less biased
in opposite directions may also have a potential benefit in other tasks where it is important to make
best use of the available resources. This is something that future studies should address.

5. Conclusions
The ESS remains the single most powerful and widespread evolutionary hypothesis to explain
lateralization. The ESS theoretical models [37,42] are well-supported by the new data showing
population-level lateralization in interactions in the so-called “solitary” insects [54] and individual-level
lateralization in social insects for tasks not requiring coordination [59], as the models predict that when
social pressures become higher, population-level lateralization arises.
It is important, however, in order to avoid misunderstanding of the theory, to distinguish the
claims of the ESS theory as an evolutionary hypothesis (i.e., in terms of natural history) and the claims
concerning current living organisms. In terms of natural history, the ESS model hypothesizes that
individual-level lateralization emerged first (because of the computational advantages associated with
the individual possession of a slight asymmetry between the two halves of the brain) and that an
alignment in the direction of the asymmetries evolved subsequently as a result of the interactions
between individually-asymmetric organisms. For current-living organisms, any neat distinction
between social and non-social species is obviously meaningless because definitions attain to the formal
convention of specific disciplines. In entomology, honeybees are social and mason bees are solitary.
But of course, this does not mean that mason bees do not interact with conspecifics. Thus, for the

6
Symmetry 2018, 10, 739

EES theory, the crucial issue is not the abstract definition of a species as social or not social, but
rather whether a specific lateralized behavior entails constraints associated with the presence of other
individuals performing the same lateralized behavior.
Importantly, the theory does not predict in a simplistic way that all living species that are
not “social” should be lateralized at the individual level and that those that are “social” should be
lateralized at the population level. What is important is the presence of inter-individual interactions in
which the asymmetry of the individuals influences that of others (e.g., aggressive interactions in mason
bees, [54]). In other words, a major prediction of ESS theory is that alignment in lateralization should be
expected whenever asymmetric individuals exhibit a benefit from coordination with other asymmetric
individuals which is higher than the cost associated with the predictability of their individual behavior.
Vice versa, the lack of alignment in lateralization should be expected whenever costs associated with
the predictability of individual behavior overcome the benefit of coordinating the behavior among
different asymmetric individuals. This is a testable hypothesis that holds true, irrespective of whether
individuals of a species are conventionally defined as “social” or “solitary”.
For the ESS theory, individual-level and population-level lateralization are the two sides of the
same coin or, even better, of the same continuum: the stability (i.e., an ESS) can be obtained with
an individual-level or population-level asymmetry, depending on the context. In other words, the
theory does not predict that social species need to be lateralized at the population-level, but rather
that individual-level or population-level lateralization emerges as an ESS. Indeed, as discussed above,
there may be cases in which, within the group, it is stable to be asymmetrical at the individual level
(e.g., [64]).

Author Contributions: E.F. and G.V. conceived the paper, E.F. wrote the paper with inputs and additions from G.V.
Funding: This research received no external funding.
Acknowledgments: We thank Lesley Rogers for inviting us to contribute this paper in this special issue
of Symmetry.
Conflicts of Interest: The authors declare no conflicts of interest.

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© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

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SS symmetry
Article
Social Risk Dissociates Social Network Structure
across Lateralized Behaviors in Spider Monkeys
Emily R. Boeving * and Eliza L. Nelson
Department of Psychology, Florida International University, Miami, FL, 33199, USA; elnelson@fiu.edu
* Correspondence: eboev001@fiu.edu; Tel.: +1-305-348-4032

Received: 1 August 2018; Accepted: 6 September 2018; Published: 9 September 2018

Abstract: Reports of lateralized behavior are widespread, although the majority of findings have
focused on the visual or motor domains. Less is known about laterality with regards to the social
domain. We previously observed a left-side bias in two social affiliative behaviors—embrace and
face-embrace—in captive Colombian spider monkeys (Ateles fusciceps rufiventris). Here we applied
social network analysis to laterality for the first time. Our findings suggest that laterality influences
social structure in spider monkeys with structural differences between networks based on direction
of behavioral bias and social interaction type. We attribute these network differences to a graded
spectrum of social risk comprised of three dimensions.

Keywords: social networks; laterality; social behavior; spider monkey; risk; social interaction

1. Introduction
Reports of lateralized behavior are widespread, particularly in the visual and motor domains [1,2].
Decades of research have led to the general consensus that behavioral lateralization is subserved by
asymmetric brain function. These brain-behavior asymmetries may serve to streamline neurobiological
processes, thereby increasing behavioral efficiency in unpredictable or arousing situations, such as
social interactions [3,4]. Thus, laterality may be particularly advantageous in gregarious species such
as primates.
In a recent synthesis of prior research, Rogers and Vallortigara [1] linked left biases in social
behavior to the right hemisphere as a general pattern of lateralization in vertebrates. However, we later
showed that not all social behaviors are associated with this pattern of laterality [5]. Specifically,
we found that two variations of embracing, but not grooming, were lateralized in Colombian spider
monkeys. We argued that the differences in lateralization in social affiliative behaviors were due to the
social dynamic in which these behaviors occurred, with grooming considered a low-stakes routine state
while embraces were high-stakes risky events. In this study, we focused on assessing the behavioral
patterns among individuals within a group, and did not take into account the relational patterns of
the group as a whole (e.g., interaction history). While consistent with other laterality investigators,
this reductionist approach does not capture the true dynamics of a social system, begging the question:
does laterality influence social structure?
Spider monkeys are one of a handful of primates living in fission-fusion [6], a social dynamic
defined by separations and reunions. Embraces are a contact greeting gesture that occur at the
time of reunions in spider monkeys [7]. In the standard embrace, the hands are wrapped around
the body and the face is placed along the trunk [7,8]. A variation is the face-embrace, in which
faces touch [5]. Fission-fusion is characterized by marked unpredictability and low social cohesion
compared with species that have a known stable hierarchy, cohesive social groups, and low variability
in interactive exchanges [9,10]. With these differences in mind, social interactions within species
living in fission-fusion may consist of a level of risk unlike that experienced in other social dynamics,

Symmetry 2018, 10, 390; doi:10.3390/sym10090390 11 www.mdpi.com/journal/symmetry

Symmetry 2018, 10, 390

and laterality may play a role in negotiating this risk [2]. In general, social behavior in fission-fusion
species is remarkably multi-dimensional, and can be difficult to tease apart.
One method for teasing apart complex social systems is social network analysis [11], a concept
with roots in the mathematical field of graph theory. Social network analysis is a tool used to compute
and visualize structural relationships in relational data. There is a long history of applying network
analysis in the study of sociality in primates (for a review, see [12]) and other species [13]. Yet social
network analysis has never been applied in the area of behavioral laterality. Network analysis alone has
the unique ability to characterize and mathematically represent global inter-connected elements [14].
Within behavioral laterality, network level information may provide a more sophisticated method
to examine topological patterns that represent potential advantages of laterality for behavior, and to
accurately depict the multi-dimensional nature of social interaction.
As our primary objective, we leveraged social network analysis in the dataset reported by
Boeving, Belnap and Nelson [5] to examine whether similarly lateralized behaviors (i.e., embrace and
face-embrace) also have similar network structures, and we predicted that these networks would
not differ. In our secondary objective, we examined social networks based on direction of laterality
(i.e., left or right) regardless of behavior type by pooling embrace and face-embrace into an affiliative
category. We hypothesized that laterality would influence network structure, and we predicted that
global left and right affiliative networks would diverge. Finally, we examined the influence of both
direction of laterality and behavior type on social network structure by creating four sub-networks of
left embrace, left face-embrace, right embrace, and right face-embrace. We hypothesized that laterality,
but not behavior type, would alter network structure. We predicted that the left sub-networks
would differ from the right sub-networks, but that sub-networks within a behavior (i.e., embrace or
face-embrace) would not differ.

2. Materials and Methods

2.1. Social Network Construction from Live Coded Behavior

We constructed social networks from live coded behavioral observations of 15 captive Colombian
spider monkeys (Ateles fusciceps rufiventris). Portions of these data were previously reported in Boeving,
Belnap and Nelson [5]. To briefly summarize, 186 h of data were captured between May and August
2015 using the Animal Behaviour Pro mobile iOS application on apple iPod 5th generation [15].
The application was programmed with information about the individual monkeys to capture initiators
and receivers of embrace and face-embrace with the modifier set as side (i.e., left or right positioning).
Left or right was recorded with reference to the positioning of the faces regardless of whether there
was contact or not. Directionality was not determined by any positioning of the limbs. Data were
collected using the continuous sampling method, and ad libitum recording method [16,17] so that all
occurrences of the target behaviors could be captured across three equally distributed time periods
throughout the day to avoid disruptions due to husbandry procedures. The DuMond Conservancy
Institutional Animal Care and Use Committee approved the research, and the study was conducted
in accordance with the laws of the United States. The research adhered to the American Society of
Primatologists (ASP) Principles for the Ethical Treatment of Non-Human Primates.

2.2. Social Network Analysis

We utilized social network analysis as the computational method to investigate potential
structural differences within all networks. Networks were computed and visualized in Cytoscape
(http://www.cytoscape.com) (Version 3.4.0; [18]), an open source software project for modeling
interaction networks. The network metric of degree centrality, which provides a composite score from
the in-degree value (i.e., interactions directed towards a monkey) and out-degree value (i.e., interactions
directed by a monkey to others), was examined because this metric quantifies the number of edges

12
Symmetry 2018, 10, 390

(i.e., social interactions) shared between nodes (i.e., monkeys). The degree centrality of node (v) for a
given graph (G) = (V , E) with |V | nodes and |E| edges defined as:

CD (ν) = deg (ν)

Using the metric degree centrality, the total number of interactions for each individual was
computed where monkeys with the most connected interactions (initiated or received) were
positioned in the center of the graph and monkeys with fewer connected interactions were positioned
along the perimeter. Within Cytoscape, we used a variant of the “Kamada-Kawai Algorithm,”
a spring-embedded algorithm that forces connected nodes together while also forcing disconnected
nodes away from the center [19]. We constructed weighted networks because this method is best suited
for graphically representing the variation in social bonds [20,21]. All edges were weighted based on
frequency of interaction with thicker edges denoting more interactions and thinner edges denoting
fewer interactions. Node size denotes variation in rank of degree centrality where larger nodes indicate
higher values of degree centrality and smaller nodes indicate lower values of degree centrality.

2.3. Statistical Analysis

To examine whether similarly lateralized behaviors (i.e., embrace and face-embrace) have similar
network structures, we first pooled frequency data from each behavior separately regardless of side
to create global embrace and global face-embrace networks. To investigate the potential effect of
laterality on social network structure, we then pooled affiliative frequency data according to side of
positioning to create global left affiliative and global right affiliative networks. Finally, we examined
the effect of laterality within each type of embrace by constructing four direction x behavior networks:
left embrace, right embrace, left face-embrace, and right face-embrace. t-Tests and ANOVA with post
hoc comparisons were used to compare the resulting networks.

3. Results
A total of 1623 social interactions were examined. Of these, 1270 were embraces and 353 were
face-embraces, corresponding to 1227 left affiliative and 396 right affiliative interactions. Individual
raw frequency scores for each behavior are reported in Table A1. Four juveniles were excluded from
further analysis due to multiple zero values for out-degree, which we suggest is age-related and would
not accurately portray degree centrality in the spider monkey group. Network degree centrality values
for the global comparisons can be found in Table 1. Unpaired t-tests found a significant difference
in degree centrality between the global embrace and face-embrace networks (t(28) = 3.43, p < 0.01,
d = 1.296; Figure A1), and a significant difference in degree centrality between the global left and right
affiliative networks (t(20) = 3.92, p < 0.001, d = 1.753; Figure A2). There was no sex difference in the
global left affiliative, global right affiliative, or global embrace networks (all p > 0.05). However, there
was a sex difference in the face-embrace network such that females initiated the face-embrace behavior
more than males, and males received more of these interactions compared to females (F(1,13) = 4.82,
p < 0.05, η 2 = 0.270). To further examine structural differences between embrace and face-embrace
within the context of laterality, we examined the four sub-networks (left embrace, right embrace,
left face-embrace, right face-embrace). ANOVA revealed a significant difference in degree centrality
among the sub-networks (F(3,40) = 20.72, p < 0.001, η2 = 0.608; Figure 1). Post hoc analyses found that
each sub-network was different from the others (all p < 0.05).

13
Symmetry 2018, 10, 390

Table 1. Individual degree centrality values.

Monkey Sex Left Affiliative Right Affiliative Embrace Face-Embrace

Bon Jovi (Bon) M 202 57 214 62
Butch (Bu) M 294 82 263 128
Carmelita (Carm) F 76 25 82 24
Cleo F 208 62 208 73
CJ F 108 32 123 19
Dusky (Dusk) F 164 46 191 31
Mason (Mas) M 372 104 342 141
Mints (Min) F 79 38 136 4
Molly (Mol) F 94 25 110 15
Sunday (Sun) M 261 101 296 83
Uva M 386 144 445 121
M = Male, F = Female. The higher the degree centrality value, the more highly connected a monkey is to others.

(A) (B)

(C) (D)

Figure 1. Clockwise from top left: (A) Left embrace; (B) Right embrace; (C) Left face-embrace; and (D)
Right face-embrace. Networks are ordered on social risk index (see text for details). Red denotes
females, and blue denotes males. Nodes are weighted such that the larger the node, the higher the
degree centrality. Edges are weighted such that thickness denotes frequency of interactions.

14
Symmetry 2018, 10, 390

4. Discussion
The primary objective of this study was to examine if behaviors with similar patterns of behavioral
laterality would also have similar social network structures. We examined the social affiliative
behaviors, embrace and face-embrace, which we previously have shown to be left lateralized in
spider monkey behavior [5]. Contrary to our predictions, we found that the network for embrace was
structurally different from that of face-embrace. We then explored our secondary objective examining
whether the side with which the social affiliative behaviors were performed had an effect on network
structure. Here our results confirmed our prediction that the global left affiliative network was
structurally different from the global right affiliative network. Finally, our analysis of sub-networks
parsing direction within each behavior partially supported our prediction. All four sub-networks were
different from each other, suggesting an interaction between laterality and behavior type. We discuss
these differences in social network structure in the context of three dimensions of social risk.
The concept of risk is often described in the non-human primate literature in the context of risk of
aggression from neighboring groups [22], predation [23], and loss of resources [24], all of which are
typical challenges for species living in the wild. Rebecchini et al. [25] first identified embracing as a
component of risk in spider monkeys, and Boeving, Belnap and Nelson [5] suggested that embrace
risk may be graded according to the type of physical contact with face-embrace having higher risk
given the close placement of the faces. By comparison, embrace is lower risk because the faces do not
touch. Here, we label this type of risk contact risk. Although embrace and face-embrace have a similar
left behavioral lateralization pattern, the finding that they do not have similar network structures
supports the conclusion that these behaviors are related but distinct. The graphical representation of the
embrace network conveys the robustness of this behavior (Figure A1A). Specifically, most individuals
engaged in embracing, and with high frequencies, yielding a network graph with most monkeys
having high values for degree centrality. Overall, this pattern indicates strong cohesion in the embrace
network. In contrast, the face-embrace network depicts interactive patterns in which only a few males
were strongly bonded (Figure A1B). When in-degree and out-degree were examined, both males and
females initiated and received within the embrace network, but there was a significant difference in
the face-embrace network where females initiated more face-embrace and males received more of this
behavior. This sex difference is notable because aggression towards females from male spider monkeys
is a known pattern [26], making the social lives of female spider monkeys especially risky. In captivity,
intra-group aggression is an important consideration given that wild female spider monkeys emigrate
from their natal group [26,27]. We envisioned the face-embrace to be the riskier of the two embraces
given the close face contact. Yet, with the known pattern of aggression towards females in mind,
our social network analysis points to a second aspect of social risk within the face-embrace: partner risk.
Social risk in relation to sex roles has been widely discussed in the human literature. For example,
female sexual risk taking within certain communities is associated with greater risk of male aggression
towards them [28,29]. Contact and partner variables have also been examined in the literature on
social touch laterality in human kissing [30–34] and embracing [35,36], although these studies have
not framed their findings in the context of risk, which may be an avenue in the future to connect these
two streams of research.
A third type of risk identified by our network analyses is laterality risk. This dimension of
risk was informed by our analyses that identified a structural difference between the global left
affiliative and global right affiliative networks. In the left affiliative network, several monkeys were
central. In contrast, the right affiliative network had a significantly different architecture in which
fewer monkeys were central to the network, and in which the behavior occurred less frequently.
Previous work has suggested that the right hemisphere plays an important role in the monitoring
and detection of uncertain events in the environment, while the left hemisphere is more involved
in routine behavior [2]. This role differentiation between hemispheres is particularly relevant when
considering the positioning of the body for embrace and face-embrace. Specifically, if the functional
split between hemispheres is correct, then positioning others on the right side for either behavior would

15
Symmetry 2018, 10, 390

be risky. Moreover, face-embrace would be especially risky given the close contact of the face coupled
with the hypothesized decrease in ability for social monitoring when engaging others on the right
side. It would thus be advantageous to position conspecifics on the left side given the hypothesized
neural processing benefit. In line with this hypothesis, the structure of the left lateralized affiliative
network pattern can be characterized as a highly cohesive network where all monkeys engaged in
the behavior, and engaged frequently (Figure A2A). In contrast, the right lateralized network was
lower in cohesion; engagement occurred less frequently, with only a few monkeys reaching high
values of degree centrality (Figure A2B). Although not recorded in this study, capturing the sequence
of behaviors that follow these risky interactions would further test this theory, and is a goal for
future work.
Although we collected data over a four-month period, one limitation of this study is that we were
not able to assess the stability of these networks over time. Juvenile data were excluded from analyses
due to the low frequency of engagement in the behaviors we examined. However, we would expect
this pattern to change as individuals mature and develop social bonds. The novel application of social
network analysis could quantify this process, not only in primates, but other highly social species.
Moreover, here we have utilized a between-networks approach based on our research question, but a
within-networks approach across two or more timepoints could provide information about how an
individual’s position in a network changes as a function of development. A developmental network
approach would also broaden our knowledge of the factors that contribute to the emergence of social
laterality and its function.
Taken together, the structural differences between the four sub-networks confirmed a
graded spectrum of social risk in spider monkeys along the three dimensions of risk: contact,
partner, and laterality (Table 2). The sub-network with the lowest risk (i.e., left embrace) had
the most participation and strongest cohesion, whereas the sub-network with the highest risk
(i.e., right face-embrace) had the least participation and was the most disjointed of the networks
indicating low cohesion (Figure 1). To answer our original question posed in the introduction,
these findings suggest that laterality influences social structure. However, we acknowledge that
social structure may also influence laterality, or that the relationship is bidirectional. Future work
using longitudinal designs may address this point. Additional studies should also aim to include
network analyses of other behavioral domains that could be related to laterality, such as cognition
and motor skill. In conclusion, social network analysis is an exciting new avenue for characterizing
brain-behavior relationships. In using this unique computational method to elucidate factors that
drive global differences in social network topology, we advance our understanding of laterality within
a social framework.

Table 2. Dimensions of social risk.

Behavior Laterality Contact Partner Risk Index

Left Embrace Low Low Low Lowest
Right Embrace High Low Low Mild
Left Face-Embrace Low High High Moderate
Right
High High High Highest
Face-Embrace
See text for details.

Author Contributions: Conceptualization, E.R.B. and E.L.N.; Analysis, E.R.B.; Writing—original draft, E.R.B.;
Writing—review & editing, E.R.B. and E.L.N.
Funding: This research received no external funding.
Acknowledgments: We thank Monkey Jungle for supporting this project and members of the HANDS Lab for
their assistance with data collection, and Starlie Belnap for her input on the statistical analysis. Alyssa Seidler
provided the drawings in the graphical abstract. This is DuMond Conservancy publication no. 60.
Conflicts of Interest: The authors declare no conflict of interest.

16
Symmetry 2018, 10, 390

Appendix

Table A1. Individual Raw Frequency Scores.

Monkey Sex Embrace Face-Embrace

Bon Jovi (Bon) M 92 16
Butch (Bu) M 107 39
Carmelita (Carm) F 36 17
Cleo F 126 63
CJ F 78 14
Dusky (Dusk) F 92 27
Mason (Mas) M 181 61
Mints (Min) F 47 2
Molly (Mol) F 81 11
Sunday (Sun) M 151 22
Uva M 198 80
M = Male, F = Female. Frequency is summed across interactions where the monkey initiated or received the behavior.

(A) (B)
Figure A1. Global embrace and global face-embrace networks differ.

(A) (B)
Figure A2. Global left affiliative and global right affiliative networks differ. Red denotes females,
and blue denotes males. Nodes are weighted such that the larger the node, the higher the degree
centrality. Edges are weighted such that thickness denotes frequency of interactions.

17
Symmetry 2018, 10, 390

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© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

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SS symmetry
Article
Meta-Control in Pigeons (Columba livia) and the Role
of the Commissura Anterior
Emre Ünver 1, *, Qian Xiao 1,2 and Onur Güntürkün 1
1 Department of Biopsychology, Institute of Cognitive Neuroscience, Faculty of Psychology,
Ruhr University Bochum, 44801 Bochum, Germany; qianxiao@moon.ibp.ac.cn (Q.X.);
Onur.Guentuerkuen@ruhr-uni-bochum.de (O.G.)
2 Key Laboratory of Interdisciplinary Science, Institute of Biophysics, Chinese Academy of Sciences,
Beijing 100101, China
* Correspondence: emre.uenver@rub.de; Tel.: +49-234-32-26213

Received: 30 November 2018; Accepted: 16 January 2019; Published: 22 January 2019

Abstract: Meta-control describes an interhemispheric response conflict that results from the
perception of stimuli that elicit a different reaction in each hemisphere. The dominant hemisphere for
the perceived stimulus class often wins this competition. There is evidence from pigeons that
meta-control results from interhemispheric response conflicts that prolong reaction time when
the animal is confronted with conflicting information. However, recent evidence in pigeons
also makes it likely that the dominant hemisphere can slow down the subdominant hemisphere,
such that meta-control could instead result from the interhemispheric speed differences. Since both
explanations make different predictions for the effect of commissurotomy, we tested pigeons in a
meta-control task both before and after transection of the commissura anterior. This fiber pathway
is the largest pallial commissura of the avian brain. The results revealed a transient phase in which
meta-control possibly resulted from interhemispheric response conflicts. In subsequent sessions
and after commissurotomy, however, the results suggest interhemispheric speed differences as a
basis for meta-control. Furthermore, they reveal that meta-control is modified by interhemispheric
transmission via the commissura anterior, although it does not seem to depend on it.

Keywords: birds; hemispheric interactions; brain asymmetry; reaction time; color discrimination

1. Introduction
Meta-control refers to the one hemisphere taking charge of response selection when the
two hemispheres are brought into conflict [1–3]. This phenomenon was first demonstrated in
split-brain patients and healthy people [1,4], but was also later revealed in monkeys [5], chicken [6],
and pigeons [2,3,7]. It is often assumed that meta-control results from one hemisphere inhibiting
the other via the various commissures that connect the two halves of the brain at the midbrain and
telencephalic level [8,9].
Meta-control becomes especially visible in species with pronounced brain asymmetries.
Depending on the type of stimulus, one or the other hemisphere regularly gains control. Birds are
ideal subjects for these studies [10]. Their left hemisphere is superior in discrimination, categorization,
and memorization of visual patterns (chicks: [11]; quail: [12]; pigeons: [13,14]) and visuomagnetic
cues (pigeons: [15]; chicks: [16]), while their right hemisphere is superior in visually guided
interactions with emotionally charged stimuli (chicks: [17]), attentional shifts (chicks and pigeons: [18]),
social interactions (chicks: [19]), as well as in relational and spatial analyses of visual information
(chicks: [20]; pigeons: [14,21]).
Meta-control could result from either inter-hemispheric response conflict or differences in
hemisphere-specific speed. If inter-hemispheric response conflict was the cause, situations in which

Symmetry 2019, 11, 124; doi:10.3390/sym11020124 20 www.mdpi.com/journal/symmetry

Symmetry 2019, 11, 124

each half-brain competes to present a different response should produce longer reaction times than
non-conflicting situations [2,8]. This is because decision making with two incompatible options
usually requires a longer processing time [10]. If, however, meta-control simply results from
hemisphere-specific processing speed, the outcome would be different. The decision time would
be determined solely by the faster hemisphere, which would always win. Two competing hemispheres
would then be as fast as the faster hemisphere.
A recent study conducted by Ünver & Güntürkün [2] in pigeons collected evidence for the
inter-hemispheric response conflict model. In their study, pigeons were trained by a forced-choice
color discrimination task monocularly, and each hemisphere learned to discriminate between its
own stimulus pair. Then, under binocular conditions, the birds were exposed to two types of test
stimuli. These test stimuli were created by combining positive and negative patterns learned by each
hemisphere. If the animal had to discriminate between a stimulus pair that consisted of two positive
(left- and right-hemispheric) patterns on one pecking key and two negative patterns on the other,
the choice was easy. Both hemispheres agreed to peck the pattern combination that was positive for both
half-brains. Consequently, the animals responded quickly to this “super stimulus”. The situation was
different when each stimulus was composed of the positive pattern of one hemisphere and the negative
pattern of the other hemisphere. In the case of such an “ambiguous stimulus”, the overall pattern
signaled an interhemispheric reward history conflict. As it turned out, the ambiguous stimulus caused
a significant response delay. This makes it likely that meta-control rests mainly on an inter-hemispheric
response conflict and not on hemisphere-specific speed.
A recent study, however, proposed a different mechanism. Qian Xiao & Güntürkün [22] recorded
signals from the sensorimotor arcopallium of pigeons while the birds were conducting a color
discrimination task under monocular conditions. All birds in their study learned faster and responded
more quickly with their right eye/left hemisphere. The arcopallium not only harbors descending
premotor neurons but also commissural neurons that constitute the commissura anterior—the largest
avian interhemispheric connection at the pallial level. As shown by Letzner et al. [23], the commissura
anterior originates from the telencephalic arcopallium/amygdala-complex and contains a small cluster
of non-GABAergic sensorimotor and amygdaloid fibers that project onto a wide range of contralateral
structures such as the posterior amygdala, the sensorimotor arcopallium, as well as further sensory
and motor components of the nidopallium. We chose this commissure for our study due to these
widespread projections onto the contralateral hemisphere. Xiao & Güntürkün [22] transiently blocked
the arcopallial activity of one hemisphere and recorded from the contralateral arcopallium during
color discrimination to determine the effect of left-to-right and right-to-left information transfer.
They discovered that the left hemisphere was able to modify the timing of individual activity patterns
of the neurons in the right hemisphere via asymmetrical commissural interactions. In contrast to that,
right arcopallial neurons were hardly able to alter the activity pattern of left arcopallial cells. Thus,
under conditions of interhemispheric competition, left arcopallial neurons could delay the contralateral
spike time of those in the right hemisphere. As a result, the neurons of the right hemisphere would
come too late to control a response and the left hemisphere would govern decisions. This finding
could imply that hemispheric dominance in birds is realized at least in part by time shifts of the neural
activity of one or the other hemisphere.
The studies by Ünver & Güntürkün [2] and Xiao & Güntürkün [22] make contradictory predictions
of the mechanisms of meta-control. Both would assume that the commissura anterior plays a decisive
role in inter-hemispheric response conflicts but would predict different choice patterns from birds
in a meta-control task after commissurotomy. Ünver & Güntürkün [2] would infer that the loss of
the commissura anterior should reduce reaction times when presented with an ambiguous stimulus
because an inter-hemispheric response conflict could no longer result in an inter-hemispheric delay
in processing time. In contrast, Xiao & Güntürkün [22] would not expect a change in reaction
times under the ambiguous stimulus because the dominant hemisphere already determines the
response. They would, however, expect that the dominance of the left hemisphere would weaken

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after commissurotomy because the left-to-right control of the neuronal spike times could no longer
be executed. To test these predictions, we conducted a meta-control study as published by Ünver &
Güntürkün [2], and subsequently transected the commissura anterior to re-test the animals with the
same task.

2. Materials and Method

2.1. Subjects
Nine naïve pigeons of unknown sex were used in the study. All pigeons were housed in single
cages with other conspecifics and maintained on a 12:12 h light–dark cycle. Their body weight was
maintained at 80–90% of their free-feeding weight by feeding diet food on weekdays and a mixture of
peas, corn, and sunflower seeds on the weekends. Water was provided ad libitum. For the monocular
sessions, velcro rings were fixed around the eyes of the pigeons using glue that was non-irritating
to the skin. Cone-shaped eye caps that were attached to the other sides of the velcro rings at their
bases and were created using cardboard. These eye caps could be easily attached and removed from
the rings surrounding the eyes for monocular testing (Figure 1). All procedures were conducted in
compliance with the guidelines for the care and use of laboratory animals and approved by the local
committee (LANUV).


Figure 1. The stimuli used in the experiment. Super stimuli consisted of a combination of two positive
and two negative stimuli presented to the left eye (LE) and right eye (RE) during the training phase.
Ambiguous stimuli were created by combining a negative stimulus for one hemisphere and a positive
stimulus for the other. Both eyes (BIN = binocular) were open during the test phase. The color
combinations shown in the figure are merely examples of the various combinations used. Below are
photographs showing the animals with a cap on one eye (left) or both eyes uncovered (right).

2.2. Apparatus
A custom-made operant chamber measuring 40 × 35 × 35 cm (W × D × H) in size was used
for the experiment. The chamber was equipped with a feeder and illuminated using a house light.
The feeder was immediately illuminated when food was presented. The stimuli (5 × 5 cm in size) were
introduced on a TFT LCD touchscreen monitor with 1024 × 768 resolution. The monitor was placed
on the same side of the chamber as the feeder to ensure that the pigeons could easily reach the feeder

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immediately after pecking at the stimuli on the screen. The experimental sessions were controlled by a
custom-written MATLAB program (MathWorks, Natick, MA, USA) using the Biopsy Toolbox [24].

2.3. Procedure
Before learning the color discrimination task, all pigeons were trained in autoshaping sessions
consisting of 40 trials. In these sessions, the pigeons were made to peck on a white square presented
on the screen under monocular conditions. The white square was presented for 4 s, and food was
delivered immediately following a single peck on the white square. These sessions were conducted
according to a fixed ratio (FR1) schedule. The birds were trained in a counterbalanced manner—on one
day, only the left eye (LE) was blocked, whereas on the next day, only the right eye (RE) was blocked.
Response to the white square in >85% of the trials in two consecutive sessions per eye condition
was set as the criterion for progress to the subsequent schedules. Once the birds met this criterion,
their training progressed to a variable ratio (VR) schedule wherein they were progressively trained
with variable ratios VR2, VR4, and VR8 under monocular conditions again, with the same criterion.
All the sessions in the VR schedule consisted of 40 trials.
Once the birds met the response criterion for the VR, we commenced the color discrimination
training. Rectangles of four different colors (red, yellow, green, or blue) were used as stimuli. The color
discrimination sessions were conducted under monocular conditions, and the color combinations were
balanced among pigeons to prevent color preferences. As shown in Figure 1, they were always placed
in a compound at the upper or lower position of a larger white rectangle. Each eye of the pigeons was
exposed to a different pair of stimuli (e.g., red and yellow for the LE; blue and green for the RE). One of
these colors served as S+ and the other as S− for each eye. The pigeons had to choose between an
upper and a lower compound stimulus that each consisted of a colored and a white rectangle. Pecks on
the S+ compound were rewarded regardless of whether the peck location was on the colored or on
the white part of the compound. The same rule was applied for the S− compound. The monocular
sessions were conducted in a counterbalanced manner, similar to the autoshaping sessions.
The stimuli were presented for 4 s. A single peck on the S+ compound immediately activated
the feeder for 2 s, whereas a peck on the S− compound resulted in switching off the house lights
for 5 s and playing a loud noise for 1 s. Once the birds responded to the S+ compound in >85% of
the trials in two consecutive sessions for each eye condition, the number of trials per session was
increased to 200 in steps of 20. The criteria that was applied in each step was that the pigeons had to
make at least 85% correct choices (responses to the S+ compound) for each eye condition in a single
session. As the number of trials in each session was increased, the reward ratio (responses to S+) was
decreased in steps of 10% until reaching 40%. This procedure was employed to prevent extinction
learning in subsequent catch trials. As a final step, a new stimulus pair, a white (S+) square and a
gray (S−) square, were introduced. Because the birds had already been trained to respond to the
white square during the autoshaping sessions, we expected them to be able to rapidly discriminate
between this new stimulus pair. This white/gray “dummy” discrimination procedure was necessary
to maintain the birds’ responses during the critical test sessions that included catch trials. In the catch
trials, the colored stimuli were re-arranged to create “super” and “ambiguous” stimuli that were not
rewarded. Each of the final sessions consisted of 200 trials, with 80% of the stimuli being presented
as white (S+) and gray (S−) dummy stimuli. As outlined above, both S+ (the S+ of the LE and the S+
of the RE) on one pecking key and both S− on the other key were termed super stimuli. Unlike the
other sessions, the critical test sessions were performed under binocular conditions. The gray/white
stimuli represented a common associative background for both stimuli. This was not applied to the
ambiguous stimuli. On each key, the S+ of one hemisphere was always combined with the S− of
the other hemisphere. The proportion of catch trials in the final session was 20% (i.e., the number
of catch trials was 40, with 20 being ambiguous and 20 being super stimuli). The remaining trials
consisted of the white/gray stimuli pair (the number of white/gray stimuli was 160). No feedback
for the catch trials was available, whereas the white/gray stimuli discrimination had a 40% reward

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probability. Following the first critical test session that included catch trials, the pigeons were further
trained using the well-known training stimuli under monocular conditions. These sessions using
the well-known training stimuli between each critical test session were conducted because it was
necessary to maintain the pigeons’ response at a stable level during the subsequent critical test sessions.
Therefore, this sequence was repeated until enough catch trial responses were collected.
After six sessions at most of testing for meta-control, pigeons underwent a commissurotomy
operation. After a two-week recovery period, the same task and procedure were applied, and data
were collected.

2.4. Surgery
Before surgery, nine birds participating in the experiment were given a mixture of ketamine
(ketamine hydrochloride, 100 mg/mL; Zoetis, Berlin, Germany) and xylazine (xylazine hydrochloride,
23.32 mg/mL, methyl-4-hydroxybenzoate, 1.5 mg/mL; Bayer Vital, Leverkusen, Germany) by
intramuscular injection (7:3 ratios, 0.12 mL/100 g body weight). The anesthetized birds were placed
on a warming pad in a stereotaxic device. Their heads were fixed at a 45◦ angle in the head holder
according to the coordinates of the pigeon brain atlas [25]. Prior to the commissurotomy, the scalp was
opened and a window was opened in the skull with a drill, centered at the anterior 7.75 and lateral
0.0 coordinates. Then, the dura mater was removed. The main vessel in the gap between the two
hemispheres was delicately pulled aside with a hand-made hook. Finally, a 2-mm-wide, 0.3 mm thick
blade was slowly lowered into the region with the following coordinates: Anterior 7.75, lateral 0.0 at
a depth of 9.0 mm from the surface of the brain [25]. The blade was lowered in increments of 1 mm,
with a 2 min pause between each increment. Thus, the risk of damage to the brain due to the pressure
caused by the blade was minimized. At the end of the operation, the knife was removed in the same
manner, i.e., by lifting 1 mm every 2 min. The skin was stitched after a medical sponge was placed
on the operation area. Finally, a painkiller was sprayed over the operation area and an antibacterial
powder (Tyrasor; Engelhard Arzneimittel, Niederdorfleben, Germany) was applied. In addition,
an intramuscular painkiller (Rimadyl, 0.04 mL/100 g body weight; Pfizer, GmbH, Münster, Germany)
was administered. The pigeons were kept in their individual cages for one week to allow them to
overcome the effects of the operation. Then, the tests were conducted.

2.5. Histology
The pigeons were deeply anesthetized with equithesin (0.55 mL/100 g body weight) and
perfused with 4% paraformaldehyde (VWR Prolabo Chemicals, Leuven, Belgium) after the last
post-operation tests. The brain was removed, immersed in gelatin (Merck, Darmstadt, Germany) and
sectioned into 40-μm frontal slices using a freezing microtome (Leica Microsystems Nussloch GmbH,
Nussloch, Germany). Sections were mounted, nissl and klüver-barrera stained, and the success of the
commissurotomy was verified microscopically. In all nine birds, the commissura anterior was verified
to be completely sectioned (Figure 2). In some animals the blade had been successfully lowered along
the midline (Figure 2b), in others it was slightly off the midline and had damaged the medial most
parts of the hemispheres in the medial meso- and nidopallium, as well the area above the commissura
anterior (Figure 2a). These are not areas associated with the visual system and we could not see any
correlation between our histological verifications and our behavioral results.

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Figure 2. A nissl (a) and a nissl/klüver-barrera (b) stained frontal section of two pigeons with
transections of the commissura anterior. The straight arrows point to the tissue rupture resulting
from the passing of the blade, while the broken arrows indicate remaining fibers of the commissura.
Note that in (a) the blade has damaged the area above the commissure since it was slightly off the
midline. This is not the case in (b). Scale bar in (b) also applies to (a).

3. Results
Two variables were important in studying the effect of the commissurotomy on meta-control. First,
how many individuals display significant meta-control before vs. after commissurotomy? Meta-control
in our task is defined as a significantly higher number of choices that are dominated by one hemisphere
being faced with an ambiguous pattern. Second, how did the reaction times to ambiguous- and
super-stimuli change after the commissurotomy?
Meta-control: A meta-control effect was observed in three out of nine birds before
commissurotomy (for each individual: chi square test, p <0.05). In two birds the right eye dominated
the decisions of the animal, and in one bird the left eye was dominant. Overall, this number was not
sufficient to produce a significant meta-control effect at the population level (paired-sample t-test,
t = 0.246, p = 0.812, n = 9). These three birds all ceased to demonstrate meta-control after
commissurotomy. On the other hand, post-commissurotomy meta-control was observed in two
different animals (one left, one right eye) that had not exhibited meta-control before the operation
(chi square test, each p < 0.05). During the post-commissurotomy period, no significant meta-control at
the population level was observed (paired-sample t-test, t = 0.939, p = 0.375, n = 9).
Reaction times: When first confronted with the ambiguous stimulus, the birds showed
significantly higher reaction times to the ambiguous (1.14 s) than to the super stimulus (1.03 s)
(paired-sample t-test, t = 2.540, p = 0.035, n = 9). In the second and subsequent sessions, however,
this effect disappeared, such that the reaction time responses to super and ambiguous stimuli were
no longer significantly different from each other (super stimulus: 1.07 s; ambiguous stimulus: 1.1 s;
(paired-sample t-test, t = 0.479, p = 0.646, n = 8)). There were no significant reaction time differences to

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the super stimulus between session 1 and sessions 2–6 (paired sample t-test; t = 0.755, p = 0.475, n = 8).
The same applied to the ambiguous stimulus (paired-sample t-test; t = 0.033, p = 0.975, n = 8). Note that
the average values of sessions 2–6 were derived from 8 birds, since one pigeon stopped working on the
task after session 1 (and then restarted after surgery). Similarly, in the post-surgery tests, no significant
differences in the reaction times between super and ambiguous signals were observed (super stimulus:
1.24 s; ambiguous stimulus: 1.29 s; (paired-sample t-test, t = 0.614, p = 0.556, n = 9)). Moreover, there
was no significant difference between the response times to the two stimulus types in the pre-surgery
sessions (excluding session 1) and post-surgery sessions (mean of super stimulus sessions 2–6: 1.07 s;
post-surgery session: 1.15 s; (paired-sample t-test, t = 0.680, p = 0.518, n = 8); mean of ambiguous
stimulus sessions 2–6: 1.1 s; post-surgery session: 1.22 s; (paired-sample t-test, t = 1.097, p = 0.309,
n = 8)) (Figure 3).

Figure 3. Average reaction times of subjects to ambiguous and super stimuli during sessions prior to
the commissurotomy and in the first session after the commissurotomy. Significant differences are
indicated by an asterisk (p <0.05). Error bars are ±1 SEM. Note that the averages of sessions 2–6 were
derived from 8 birds, because one pigeon stopped working on the task after session 1, but restarted
after surgery.

4. Discussion
Meta-control can occur when the two hemispheres compete with each other to produce a
hemisphere-specific response [1,2,4,5,7]. In studies with birds working on color discrimination tasks,
the dominant hemisphere is usually the left [10,11,13]. Concomitantly, there is some evidence for a
higher incidence of left-hemispheric meta-control in such tasks with pigeons [7]. The present study
tested two different possible mechanisms of meta-control. One of these assumes that meta-control
results from each hemisphere inhibiting the other [8]. Such a mechanism should cause conflicting
(in our case ambiguous) stimuli to produce longer processing times, resulting in longer reaction times.
A recent study found evidence supporting this prediction, and therefore suggested that meta-control
results from the interhemispheric conflict [2]. An electrophysiological study, however, found evidence
for a different mechanism: Xiao & Güntürkün [22] discovered that arcopallial neurons of the left
hemisphere dominate the response of the animal during color discrimination through a faster activation
of motor responses. Furthermore, the left hemisphere controls the right hemispheric spike times, and is
thus able to delay reaction times of the other hemisphere. This effect would increase the advantage of
the left hemisphere. These findings make different predictions for the effect of the commissurotomy on

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meta-control. The mechanism based on the interhemispheric conflict would imply that a section of the
commissura anterior should reduce reaction times to ambiguous stimuli (no commissural exchange
→ no interhemispheric conflict), whereas the model based on hemisphere specific speed would not
predict post-surgery changes in reaction time to ambiguous stimuli (no commissural exchange → no
change in hemisphere-specific speed). At the same time, the results of Xiao & Güntürkün [22] suggest
that the advantage of the left hemisphere would be smaller after commissurotomy (no commissural
exchange → no possibility to further delay response execution of the right hemisphere). Our findings
suggest that the birds only experience interhemispheric conflict on the first session with ambiguous
stimuli, and the effect disappears in the following sessions. A subsequent commissurotomy does not
alter reaction times to ambiguous stimuli but does modify meta-control. Overall, our data would be
compatible with a model according to which interhemispheric conflict occurs in a short, initial period,
but then gives way to lateralized reaction patterns determined by hemisphere-specific speed.
As visible in Figure 3, reaction times to super and ambiguous stimuli were the most different in
the first session in which the animals were first presented these two stimulus types under binocular
conditions. However, in subsequent sessions reaction times became increasingly similar. Ünver &
Güntürkün [2] had based their conclusion of interhemispheric conflict on the first session after
introducing ambiguous stimuli. This conclusion may remain valid but is obviously restricted to
this initial session. In subsequent sessions, a different mechanism seems to prevail. It is indeed
conceivable that the animals quickly learned about the absence of negative or positive feedback
when responding to the ambiguous stimuli. It is known that pigeons are extremely sensitive to
reward alterations in operant categorization tasks, and subsequently tend to bias their choices towards
initially favored alternatives [26]. Similar findings were also observed in studies with monkeys [27,28].
This makes it likely that our commissurotomy was performed at a point in time in which the pigeons
were no longer pondering response conflicts but instead biased their choices according to mechanisms
based on hemisphere-specific speed. Consequently, response times to ambiguous stimuli were not
altered by commissurotomy.
This scenario is compatible with the explanation that each hemisphere rushes with its own
hemisphere-specific speed to motor areas. During color discrimination, the left hemisphere usually
produces faster reaction times. This has been observed in various studies with pigeons [29] and
other birds [17,30]. This was also observed by Xiao & Güntürkün [22] when recording from the
pigeon arcopallium during color discrimination. This study also offers a mechanistic explanation
of this observation by revealing that the left hemisphere can modify the spike time of the right
hemisphere. Thus, under conditions of conflict, the left hemisphere could delay the right hemispheric
response speed, thereby accelerating its own advantage. From this point of view, a transection of the
commissura anterior should reduce, but not completely terminate the left hemispheric superiority.
Indeed, we observed major alterations of meta-control after surgery. Usually, an individually significant
extent of meta-control is observed in only a fraction of pigeons [2,3,7]. With the procedure used in this
study, it was mostly the left hemisphere that evinced meta-control [2,7]. In the current experiment,
three out of nine birds demonstrated meta-control before commissurotomy (two left hemispheric,
one right hemispheric). This is a typical result pattern [2,7]. After transecting the commissura anterior,
however, all three birds lost their hemisphere-specific advantage. Instead, two other birds displayed
significant meta-control (one left, one right). Although this is certainly not a strong proof of the
conclusion of Xiao & Güntürkün [22], it is conceivable that the changes observed in meta-control
in our nine pigeons resulted from the loss of a left hemispheric advantage that resulted in biased
interhemispheric interactions. If indeed neuronal speed differences cause the bias towards the right
eye in metacontrol studies, the large individual differences may result from the fact that neurons show
within the pigeon’s visual system substantial latency differences between individual birds [22,31–33].
It is known that the commissura anterior connects with the anterior and intermediate arcopallium.
These structures project onto a wide cluster of visual and sensorimotor areas. Our study focused on
the contribution of the commissura anterior to visual asymmetries. However, further commissural

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systems may also play a role in metacontrol since studies of both chicks [34] and pigeons [35–37]
suggested that subpallial commissures also play key roles in visually-guided lateralized behavior.
The supraoptic decussation (DSO) is one such subpallial connection, and is known to be responsible
for interocular transfer during visual discrimination [38]. This may be due to the indirect connection
of the DSO to telencephalic visual structures such as Wulst. More recently, it has been shown that the
nucleus of the lateral ponto-mesencephalic tectum (nLPT), a midbrain structure, contains GABAergic
neurons and its projections terminate in the contralateral optic tectum (TeO) via the commissura
tectalis [39]. Therefore, this midbrain commissure may also play a crucial role during meta-control.
Thus, the present study must be complemented by further experiments to reveal the full scenario of
interhemispheric interactions of lop-sided bird brains.
Although our study was centered on the mechanisms of meta-control, it might also offer some
more general insights on the behavior of organisms with lateralized brains. A key problem of these
species is the production of a single response from two asymmetrically specialized hemispheres.
Our results suggest that the default option in such situations could be to let both hemispheres compete
based on hemisphere-specific processing speed. Because the dominant hemisphere for a certain
stimulus class usually produces faster responses [22], the most competent half-brain would primarily
determine the response. The commissural slowing mechanism discovered by Xiao & Güntürkün [22]
would amplify this interhemispheric speed difference to ensure that the dominant hemisphere controls
the overall response.

Author Contributions: Conceptualization: Q.X. and O.G.; designed experiment: Q.X. and O.G.; performed
experiment: E.Ü.; statistical analysis: E.Ü. and O.G.; manuscript preparation: E.Ü. and O.G.; funding acquisition
and project supervision: O.G. All authors revised and approved the paper.
Acknowledgments: We are grateful for the support of Annika Simon during surgery and the conduct of the
histological procedure. We also thank Felix Ströckens and Sarah von Eugen for help during documentation of
histological results. Supported by the Deutsche Forschungsgemeinschaft through SFB 874.
Conflicts of Interest: The authors declare no conflict of interest.

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interactions in the pigeon (Columba livia) and their potential role in brain lateralisation. Brain. Res. 2000, 852,
406–413. [CrossRef]
38. Watanabe, S. Interhemispheric transfer of visual discrimination in pigeons with supraoptic decussation
(DSO) lesions before and after monocular learning. Behav. Brain Res. 1985, 17, 163–170. [CrossRef]
39. Stacho, M.; Letzner, S.; Theiss, C.; Manns, M.; Güntürkün, O. A GABAergic tecto-tegmento-tectal pathway
in pigeons. J. Comp. Neurol. 2016, 524, 2886–2913. [CrossRef]

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

30
SS symmetry
Article
Lateral Asymmetry of Brain and Behaviour in the
Zebra Finch, Taeniopygia guttata
Lesley J. Rogers *, Adam Koboroff and Gisela Kaplan
School of Science and Technology, University of New England, Armidale, NSW 2351, Australia;
akoboroff@gmail.com (A.K.); gkaplan@une.edu.au (G.K.)
* Correspondence: lrogers@une.edu.au; Tel.: +61-266-515-006

Received: 1 November 2018; Accepted: 29 November 2018; Published: 1 December 2018

Abstract: Lateralisation of eye use indicates differential specialisation of the brain hemispheres.
We tested eye use by zebra finches to view a model predator, a monitor lizard, and compared
this to eye use to view a non-threatening visual stimulus, a jar. We used a modified method of
scoring eye preference of zebra finches, since they often alternate fixation of a stimulus with the
lateral, monocular visual field of one eye and then the other, known as biocular alternating fixation.
We found a significant and consistent preference to view the lizard using the left lateral visual field,
and no significant eye preference to view the jar. This finding is consistent with specialisation of the
left eye system, and right hemisphere, to attend and respond to predators, as found in two other avian
species and also in non-avian vertebrates. Our results were considered together with hemispheric
differences in the zebra finch for processing, producing, and learning song, and with evidence of
right-eye preference in visual searching and courtship behaviour. We conclude that the zebra finch
brain has the same general pattern of asymmetry for visual processing as found in other vertebrates
and suggest that, contrary to earlier indications from research on lateralisation of song, this may also
be the case for auditory processing.

Keywords: asymmetry of brain function; lateralised behaviour; song; songbirds; zebra finch;
predator inspection; eye preference; hemisphere differences; monocular viewing; general pattern
of lateralisation

1. Introduction
It is timely to bring together and discuss the evidence for asymmetry of brain function in the zebra
finch for two reasons. Firstly, the zebra finch is a model species used frequently to understand the links
between neural structure and behaviour. Secondly, early research reporting lateral asymmetries in the
species was equivocal, largely because it seemed to be at odds with lateralities reported in other avian
species and because results of different studies were not always consistent. Therefore, we decided to
summarise the available literature showing, or not showing, lateralisation in the zebra finch and to
add some data on eye preference to view a predator.
The zebra finch has featured amongst those songbirds investigated for song learning, song
production, and perception. Zebra finch song is stereotyped and has a rich spectro–temporal structure,
which some researchers have compared to human speech sounds [1]. Furthermore, male zebra finches
learn their song from other birds, by imitating the song of a tutor heard during a sensitive period of
development [2,3]. These and other aspects of zebra finch song have been studied in considerable
detail and compared to speech in humans [4–7].
Another feature of song is differential control of its production and processing by the left and
right hemispheres. This has been studied in number of avian species, and studies of species other
than the zebra finch have demonstrated a dominant role of song centres in the left hemisphere for

Symmetry 2018, 10, 679; doi:10.3390/sym10120679 31 www.mdpi.com/journal/symmetry

Symmetry 2018, 10, 679

controlling song production [8,9] and differential roles of the hemispheres in perception of song [10].
However, lateralisation of the song system in the zebra finch seemed not to fit this pattern.
Initially, Nottebohm et al. [10] cited unpublished observations that indicated little hemispheric
asymmetry of song control in the zebra finch, and differing from the canary, zebra finches were
reported to have no asymmetry in the size of the left and right hypoglossal nuclei, i.e., the collections
of cell bodies with axons that form the hypoglossal nerves, a branch of which innervates the syringeal
muscles used to produce song [11]. However, later research revealed the presence of asymmetry for
song in the zebra finch, albeit not the same as that found in other passerine species.
Williams et al. [12] found right hemispheric control of song production in zebra finches; opposite
to the direction of asymmetry reported for other songbirds. Lesioning the auditory areas of the right
hemisphere of zebra finches was found to decrease the birds’ ability to process harmonic structure in
song [13]. Floody and Arnold [14] also reported evidence that the right song system is dominant in the
zebra finch. Using functional magnetic resonance imaging (fMRI), Voss et al. [15] revealed hemispheric
asymmetry in neural activity during stimulation by song: significant discrimination between songs
was found only in the right hemisphere. Recognition of the zebra finch’s own song versus the song of
a conspecific was also found to be biased to the right hemisphere [16]. All of these studies indicated
that perceptual production and processing was a function of the right hemisphere in zebra finches,
and thus the asymmetry seemed to be reversed compared to other songbird species studied. However,
measuring expression of the immediate early gene ZENK in zebra finches exposed to the auditory
and/or visual aspects of courtship, Avery et al. [17] found left hemispheric dominance (i.e., hearing
courtship song and seeing dancing by the courting male causes more neural activity in the left than
the right hemisphere). Recent studies have demonstrated that both hemispheres attend to song but
to different aspects of it [1], and that the direction of asymmetry depends on whether the memory of
song is old or new [6].
It is possible that variation in the direction of asymmetry occurs depending on previous exposure
to song and to what extent the birds recalled their previous exposure to song. Demonstrating that the
direction of lateralisation depends on learning and memory, Moorman et al. [18] reported left-sided
dominance of ZENK expression in the higher vocal centre of juvenile male zebra finches exposed to
their tutor’s song but not in those exposed to unfamiliar song. Olson et al. [6] found that the direction
of laterality of song memory depends on strength of learning; the more the zebra finches learnt and
remembered the song of their first tutor, the more right lateralised they were, as assessed by ZENK
expression. By contrast, the more they learnt from a second tutor, the more left-lateralised they were.
Hence, new and old memories of song appear to be located in opposite hemispheres; older memories
in the right hemisphere and newer memories in the left hemisphere. In fact, Yang and Vicario [7]
showed that exposure of adult zebra finches to novel hetero-specific sounds (vocalisations of canaries)
can shift lateralisation for song processing from the right to the left hemisphere.
Using fMRI measurements of neural processing of song in zebra finches, Van Ruijevelt et al. [1]
provided evidence that the spectral aspect of song is processed in the right hemisphere. By comparison,
presentation of song with the spectral component filtered out, but with the temporal component
remaining, led to greater neural activity in the left hemisphere [1]. Hence, the left hemisphere processes
the temporal domain of song, whereas the right hemisphere processes the spectral component of song.
This role of the left hemisphere in processing temporal aspects of song is supported by finding higher
expression of ZENK in regions of the left hemisphere in males when they responded to arrhythmic,
but not rhythmic, song [19].
A female zebra finch hearing a male’s song directed towards her (as compared to the
song produced by the male when he is alone) expresses a higher level of activity in the
caudocentral–nidopallial region of the left hemisphere and the caudomedial–mesopallial region of the
right hemisphere, as shown by functional magnetic imaging (fMRI) and early gene expression [20].
This result demonstrates that both hemispheres respond to hearing the song, but in each hemisphere
the information is processed in different regions.

32
Another random document with
no related content on Scribd:
for a minute, gave a whisk with his tail and bounded off across a bed
of artichokes which a gardener was cultivating on the Palatine Hill.
The poor man complained that he had lost all his chickens by the
depredations of these marauders.
Everybody has heard of the Vatican. This is an immense palace
adjoining St. Peter’s, formerly the residence of the Pope, and now
famous for its pictures and statues. I hardly knew which of the two
struck me with the greater astonishment—St. Peter’s, with its
stupendous architecture and gorgeous embellishments, or the
Vatican, with its endless treasures of art. Gallery, hall and saloon
open upon you, one after another, till there seems literally to be no
end of statues, vases and columns of precious marble and porphyry.
Beautiful fountains of water are playing in the pavilions, and long
vistas of sculpture carry the eye a quarter of a mile in length. The
apartments amount to many thousands: the wonder is that any man
ever undertook to count them. All description of this place seems an
utterly vain attempt. It is realizing the dreams of fairy splendor to
wander over it.
After the ceremonies of the Holy Week are over, strangers
generally leave the city, and Rome becomes a quiet place. There is
little traffic or industry here, although the population is nearly double
that of Boston. No rattling of carts over the pavements, no throng of
busy passengers in the streets, give tokens of active business. The
shopkeepers sit idly at their counters, and look as if a customer
would astonish them. Two or three little feluccas lie at a landing-
place in the Tiber, unloading coffee and sugar from Marseilles, and
this is all that looks like commerce. Rome has nothing to export but
rags and pozzolana, or volcanic sand, which, mixed with lime, forms
the composition known as Roman cement. At sunset the genteel
classes ride out in their carriages to the gardens in the neighborhood
of the city, and this gives some appearance of life to the place at that
time. But far the greater part of the day the streets are lonely and
still. The shopkeepers close their doors after dinner and go to sleep.
Rome is full of splendid palaces and churches, profusely and
magnificently adorned with pictures, sculptures, precious stones,
gilding, and every other sort of embellishment. The shrines of the
saints are very curious. They are covered all over with votive
offerings from persons who have been sick or have escaped from
accidents. If a man is in danger of drowning, or is run over by a
horse, or gets a bang on the shin, or has a sore finger, he makes a
vow to his favorite saint, and, after his escape or recovery, gives him
a present of a little silver ship, or leg, or finger, which is stuck up in
the church as a memento of the saint’s intercession and the man’s
gratitude. In this manner you may see the walls of a church covered,
for many yards square with silver legs, toes, arms, hands, fingers,
hearts, ears, noses, and nobody knows what else. A traveller
unacquainted with the fact might take them for hieroglyphics. All
sorts of rich offerings are made to these shrines. I have seen the
figure of a saint in a glass case completely covered with gold
watches, rings, bracelets, necklaces, &c. When the saint finds
himself so overloaded with ornaments as to leave no room for any
more, he allows himself to be stripped. The watches and jewels are
sold, and the shrine is open for new presents. It is easy to see how,
in a long course of years, this practice, and others similar, have
brought into the treasury of the church that abundance of wealth
which has been lavished upon the magnificent edifices of this
country. The votive offerings above described are so numerous and
constant that the silversmiths have always for sale, heads, legs,
hearts, arms, &c., of all sizes, to suit the customer as to wealth or
devotion. Sometimes the offering is accompanied with a painting
descriptive of the event commemorated; and you see a portion of the
church walls covered with the oddest pictures in the world. A man is
tumbling down a ladder; another is run over by a carriage; another is
knocked on the head with a club; another is kicked by a horse;
another is running for life, with a mad bull at his heels; another is sick
abed, with a most alarming array of doctors and apothecaries around
him, &c.
Fountains are abundant throughout the city: and it is most
agreeable, in the hot weather which prevails here for the greater part
of the year, to hear the murmur and bubbling of the rills and jets of
water which adorn every street. When we consider the enormous
sums of money which the ancient Romans expended upon their
aqueducts, and behold the immense lines of arches that stretch
across the country, we cannot be surprised that the modern city is
better supplied with water than any other place in the world. It is
brought from a great distance, as the water in the neighborhood is
very bad. In one of my rambles, a few miles from the city, I passed a
stream running into the Tiber, which appeared almost as white as
milk, and had a strong smell of sulphur. All the country round here is
of volcanic origin; yet there has been no eruption or appearance of
subterranean fire within the memory of man.
Rome is a fine residence for a person with a small income, no
business to do, and the wish to get as much as possible for his
money. House-rent is as low as one can reasonably desire. You may
lodge in a palace with galleries paved with marble and the walls
covered with the finest paintings; for the Roman nobles are poor and
proud; they will not sell their palaces or pictures, even though
threatened with starvation; but they let their best rooms to lodgers,
and live in the garrets. In all Rome I saw but one new house:—a
sure sign of the low value of real estate. The markets are cheap;
clothing costs about half what it does in America. The people have
some queer ways in buying and selling. Many things sell by the
pound, which we never think of putting into scales: apples, cherries,
green peas, firewood, charcoal, &c. I inquired as to a pair of woollen
stockings at a shop, and the goods were weighed before I could be
told the price. I bespoke a pair of boots, and calling one day to see if
they were done, I found the shoemaker at work upon them, but the
leather had never been colored. “Body of Bacchus!” said I—for that
is the current Roman exclamation—“I don’t want yellow boots,
Signior Lapstonaccia!” I was surprised, however, to be told that the
Roman cobblers always made the shoes first and colored the leather
afterwards.
The greater part of the campagna or open country about the city
is kept waste by the malaria or unwholesome air of summer. What is
the cause or nature of this noxious vapor, no one has yet been able
to discover. The soil is perfectly dry, and there is no marshy land or
stagnant water in the neighborhood which can impart unhealthy
moisture to the atmosphere. The sky is beautifully clear in almost
every season, and each breeze that blows seems to savor of nothing
but balmy purity. Nevertheless, the country for miles is uninhabitable,
and shows a desolate plain, with a field of wheat here and there, or a
few scattered willow trees and thickets of bramble. Shepherds feed
their flocks among the ruins during the healthy season; but there are
no villages till you come to the hills of Albano, Frascati and Tivoli, in
which neighborhood the Romans have their country seats.
The malaria also infests the city, particularly the ruinous portion.
Strangers seldom pass the summer in Rome on this account,
although I was told there is no danger of sickness for any one who
does not go out at night, and takes care to sleep with the windows
shut. The unhealthy season is from June to September. During the
remaining months Rome is thought to be as healthy as any spot in
the world. The winter is delightful, being mostly like the finest
October weather in New England.
I could fill a book with stories about this wonderful place; but the
brief space allotted to me makes it necessary to pass on in my story.
 The Deluge.

This event, described in the sixth and seventh chapters of

Genesis, is one of the most wonderful that is recorded in the history
of the world. It was a judgment sent upon the earth by the Almighty,
in consequence of the great wickedness of mankind. His purpose
was to destroy not man only, but the animal tribes, except a pair of
each species, so as to repeople the earth, after having thus set
before the world, for all future time, a fearful warning against
disobedience of his commands.
This great catastrophe occurred 1656 years after the creation,
and more than 4000 years ago. We have not only the testimony of
the Bible to assure us that this event actually occurred, but most
nations, particularly those of high antiquity, have either historical
records or traditions of such an occurrence. The account given of it
in Genesis is one of the finest pieces of description that has ever
been penned; but it is very general, and gives us few details, or
minute incidents. Yet the imagination can easily portray many
affecting scenes that must have been witnessed in the fearful
overthrow of the great human family.
 Noah, who was a good and wise man, was forewarned of the
coming destruction, and, by the command of God, he built an ark, of
vast dimensions, and which cost him the labor of a hundred years. It
was a sort of bark, being shaped somewhat like a chest or trunk. It
was larger than the largest vessels of modern times. It is a large ship
that measures a thousand tons, yet Noah’s ark measured forty-two
thousand tons!
Into this ark Noah collected his family, and a pair of each kind of
bird, each kind of quadruped, and each kind of reptile. Under the
guidance of the Almighty, this vessel and its numerous inhabitants
floated safely on the water for a whole year. Here they were fed, and
here the lion was made to lie down with the kid. When, at last, the
waters had subsided, and the ark rested upon the land, then they all
came forth.
This story of Noah and his family is not only interesting as a
wonderful piece of history, but it conveys to us an important lesson. It
teaches us that wisdom is imparted to the children of God, which is
not enjoyed by the wicked; that there is an ark of safety provided for
the true believer, while the scoffer is left to work out his own
destruction.

Anecdote.—On Saturday last, says the Philadelphia North

American, Lord Morpeth visited the Philadelphia Alms-House,
Blockley. Considerable anxiety was manifested among the inmates
to obtain a sight of the distinguished stranger. After he had departed,
a little boy, the son of Mr. S——, who was present, remarked to his
mother that “he did not know that there were two Lords—he thought
there was but one, who lived up in the sky.”
 A Page for Little Readers.

One of my young black-eyed friends, who has just learned to

read, has asked me to give some simple stories, in the fashion of
Peter Parley. I have promised to comply with this, and therefore give
two pieces from “Parley’s Picture Book,” a little volume full of
pictures and stories, which may be found in the bookstores.

BOYS AT PLAY.

Here are three boys at play. Each boy has a hoop, which he
strikes with a stick, and it rolls along. It is very pleasant to roll a
hoop. If you strike it hard, it flies along very fast, and you must run
with all your might to catch it.
You must take care not to drive your hoop among horses. I once
knew a little boy playing with his hoop in a street. A horse was
coming along, but the boy was looking at his hoop, and he did not
see the horse. His hoop rolled close to the horse’s fore feet, and the
boy ran after it.
 The horse was going fast, and he struck the boy with his foot. The
boy fell dawn, and the horse stepped on his leg. The poor boy’s leg
was broken, and it was many weeks before he got well.
 THE GIRL AND KITTEN.
“Come, pretty Kit, come, learn to read;
Here with me sit; you must indeed.
Not know your letters! fie, fie! for shame!
The book I’ll hold; come! spell your name!
Now try to say K I T, Kit;
For you may play where you think fit,
Upon the bed, or on the tree,
When you have said your A B C.”
’T was snug and warm in Mary’s lap,
So pussy thought she’d take a nap.
She went to sleep,—the lazy elf!
And Mary read the book herself.
She learned to read, she learned to spell,
And said her lesson very well.
And now, my little reader, say,
If you from books will turn away,
And be like Kit, an idle thing,—
Now catch a mouse, now twirl a string;
Or will you learn to read and spell,
And say your lessons very well?
 Varieties.

Musical Dialogue.—“Major,” said a minor to an elderly

gentleman, “I must say your speech to-day was very flat.” “That,”
said the major, “is very sharp for a minor.”

Singular, not plural.—​The mayor of a small town in England,

thinking that the word clause was in the plural number, always talked
of the last claw of parliament.

A Dutchman.—A Dutchman was seen one day bidding an

extraordinary price for an alarm clock, and gave as a reason, “Dat
ash he loffd to rise early, he had nothing to do but bull the string, and
he could wake himself.”

Long Bills.—Gentlemen of the medical profession in London are

said to be called snipes, from the unconscionable length of their bills.

Poetry and Prose.—“I say, Pomp, wat be de diffrence ’ween

poetry and de wat you call plank verse?”
“Why, I gib you something, Sip, I think will be lustratious of de
subject:
‘Go down to mill-dam
And fall down slam’—

dat be poetry; but

‘Go down to mill-dam,
And fall down whapp’—
dat be blank verse.”

Good.—“Bill, lend us your knife.” “Can’t; haven’t got any; besides,

want to use it myself.”

Wit.—Three gentlemen meeting to sup at a hotel, one of them

wished for partridges. A brace was accordingly brought, and set
upon the table, which he accordingly began to carve. He deliberately
took one of them upon his own plate, leaving the other one for his
two friends. “Hold!” cried one of them; “that is not fair!” “Perfectly fair,
I think,” said the gentleman; “there is one for you two, and here is
one for me too.”
 To my Correspondents.

Almost every person has some trouble, real or imaginary. I have

seen a story of a philosopher who travelled over the world in search
of a person who was perfectly happy. He visited the halls of the rich
and the hovels of the poor, and everywhere found each individual
afflicted with some rooted sorrow, care, or vexation. At last, as he
was about giving up the search in despair, he fell in with a shepherd
who seemed perfectly free from every evil. He had a pleasing wife,
lovely children, a competent support, and good health. What could
he desire beside?
“Nothing—nothing,” said the philosopher; but when he asked the
shepherd if he was happy—“Alas! alas!” said the man; “I am far from
it. There is a black sheep in my flock that is forever running off and
leading the rest astray. While I am awake, that black sheep is the
torment of my life; and when asleep, it disturbs my dreams!”
It is said that Sir Walter Scott was talking on this subject, one day,
with some gentlemen—he contending that no one was perfectly
happy, and they maintaining the reverse—when a half-witted fellow,
whom they knew, came up. It was agreed to settle the question by
appealing to him.
“Good day to ye, Sawney!” said Sir Walter. “Good day,” said
Sawney, in reply. “Well now, Sawney,” said Sir Walter, “how does the
world use you?”
“Well—well, your honor.”
“Have ye plenty to eat?”
“Yes.”
“And to drink?”
“Yes.”
 “Good clothes?”
“Yes.”
“Then you have nothing to trouble you?”
“No—nothing but the bubly Jock,” (a cock-turkey.)
“Ah, what of the bubly Jock?”
“Oh, he is always running after me; night or day, asleep or awake,
I can always see him—gobble, gobble!”
“There!” said Sir Walter to the gentlemen; “the decision is in my
favor. This poor simpleton, though he is provided with every comfort,
is still beset by a tormentor. It matters not that it is invisible—that it
exists only in his fancy—it is to him a real bubly Jock, and as truly
disturbs his peace as if it were a thing of flesh, and strutted forth in
feathers.”
And now I must tell of my troubles. Perhaps you will laugh—but
one thing that frequently makes me very fidgety, is an itching in the
great toe of my wooden leg! If you think this nonsense, just ask any
old soldier who has lost a limb, and he will tell you, if it is a foot or a
hand, that he has all the sensations of heat or cold in the fingers or
toes of the absent member, just as distinctly as if it was in its place
and as sound as ever. This is no joke—it is a reality that you can
easily verify.
Well, now, it seems to me that my lost foot is really where it used
to be; and the worst of it is this, that, when it itches, I can’t scratch it!
It does no good to apply my fingers to the wooden stick, you know;
this only reminds me of my misfortune, and brings on a fit of the
blues. But there is one thing to be considered—there is medicine, if a
person will seek it, for almost all diseases, whether real or fanciful;
and, thanks to my young friends who write me letters, I find these
very letters a pretty certain cure for the fidgets which I spoke of.
When I sit down to read them, and find them full of kind and pleasant
feelings, I readily forget the cares, the vexations—the dark weather
of life, that beset even such a humble career as mine.
So much for the introduction—and now to business.
 The following letter is very welcome. Can Harriet venture to tell us
who the author of this capital riddle really is?
Newport, March 28, 1842.
Friend Merry:
In looking over, a few days since, some old papers
belonging to my father, I found the following riddle. My father
informs me that it was written many years ago, by a school-
boy of his, then about fifteen years old, and who now
occupies a prominent place in the literary and scientific world.
If you think it will serve to amuse your many black-eyed and
blue-eyed readers, you will, by giving it a place in the
Museum, much oblige a blue-eyed subscriber to, and a
constant reader of, your valuable and interesting Magazine.
Harriet.
riddle.
Take a word that’s much used,—’tis a masculine name,
That backward or forward doth spell just the same;
Then a verb used for dodging—a right it will claim
That backward or forward it spells just the same;
The form of an adjective, none can exclaim
That backward or forward it spells not the same;
Then a chief Turkish officer’s title or name,
That backward or forward doth spell just the same;
The name of a liquor, its friends all will claim
That backward or forward is still just the same;
Then a word used for jest, or doth triumph proclaim,
That backward or forward still spells just the same;
Then a verb in the imperfect, which also doth claim
That backward or forward it spells just the same;
The name of a place which geographers fame,
That backward or forward doth still spell the same;
Then a very queer word, ’t is a Spanish ship’s name,
That backward or forward doth spell just the same;
Then a verb that’s well known, I refer to the same,
That, backward or forward spelt, makes but one name;
Then a name that is given to many a dame
That backward or forward still spells just the same.
 A Set of initials the above will afford—
R-Ove through them in order, they form a droll word.
I L-eave you to solve it—’t will cure a disease;
De-Velop the riddle—’t will set you at ease.
D-Espair not, but hope; ’t is easily guessed:
L-Ike etching on copper in gay colors dressed,
E-Tch it down on your hearts, and there let it rest.

Elizabeth Town, N. J., April 9, 1842.

Dear Sir:
Though perhaps not so young as the generality of your
admiring readers, I am confident that there can be none who
are more delighted than myself with your works, and
particularly your Museum, which is now being published. Of
course, I was the more pleased when I noticed the addition of
a “puzzle column,” of which I am decidedly fond. I have
solved with correctness all the puzzles that have appeared in
your Museum, with the exception of Puzzle No. 5 in the April
number, which so far passes my comprehension, that, after
repeated endeavors after its solution, I have flattered myself
that it is a hoax; but if it is not, I must confess it is the hardest
puzzle I have seen for some time. Are not the following
correct answers to the April puzzles?—No. 1, “Mother.” No. 2,
“Charles Dickens.” No. 3, “Boston and Worcester Railroad.”
No. 4, “Prince de Joinville;” and Master Bare-Head’s,
“Massachusetts.” I forward you an original puzzle, for which I
do not profess any very extraordinary difficulty.
I am a name of 23 letters.

My 5th, 21st, 7th, 10th, 22d, is a Russian noble.

My 17th, 18th, 20th, 20th, 12th, 2d, is a .
My 1st, 10th, 15th, 16th, is a legal writing.
My 4th, 14th, 13th, 17th, 12th, is a pleasant amusement.
My 11th, 3d, 8th, is seen whenever it is not invisible.
My 2d, 12th, 21st, 4th, 12th, 2d, is what if all men were,
the world would be happier.
 My 19th, 12th, 7th, 7th, 23d, 9th, 19th, 6th, 9th, 12th, 6th,
19th, is the title of a justly celebrated periodical.
My 22d, 3d, 9th, 9th, 14th, 6th, is a street where my
whole is found.

If you think the above worthy a place, you can publish it.
You may hear from me again soon. My sheet is full, so I have
but to subscribe myself,
Very respectfully,
W. F. W.

Saturday, April 8, 1842.

Dear Sir:
I have taken the liberty to send you this puzzle, which I
suppose almost any of your readers can unravel.
I am a name of 13 letters.

My 1st, 5th, 6th, 4th, and 2d, is a girl’s name.

My 3d, 5th, 10th, and 11th, is what every bird has.
My 9th, 6th, 4th, 10th, 11th, 12th, and 13th, is what
physicians often use.
My 3d, 4th, 3d, and 5th, is a number.
My 11th, 5th, and 3d, is also a number.
My 13th, 8th, and 1st, is a color.
My whole is the name of a distinguished orator and
statesman.

From a constant reader, who signs himself,

Respectfully yours,
Alexis.

Dear Mr. Merry:

 I have been trying my hand at puzzles since the reception
of the April number of the Museum. I have guessed out No. 4,
as you will see below.
Sarah.
Answer to Puzzle No. 4, in the April number of the
Museum.

The first, the “mechanic,” I doubt not a bit,

Is the joiner, well known by rustic and cit;
The second, a word highly prized by us all,
For all would be loved, whether great, whether small;
The third, Mr. Puzzler, a pin, I should guess,
For fastening a plank, or a fair lady’s dress;
The fourth—let me see; I’ll think in a trice—
I have it at last! it is very fine rice;
The fifth, it is said, “is French for a city,”—
Now that must be ville—how exceedingly pretty!
The sixth, and the last, it seems very clear,
Will never spell Yankee, but p-e-e-r.
Prince de Joinville.

Gloucester, April, 1842.

Mr. Merry:
I have found out the answers to the puzzles in the April
number, as follows: 1st puzzle, the answer is, Mother; 2d,
Charles Dickens; 3d, Boston and Worcester Railroad; 4th,
Prince de Joinville; 5th, ——; 6th, Massachusetts. And now,
Mr. Merry, I take the liberty to send you one, which, if you
think worthy, I should like to have you publish in your
Magazine, and oblige
Your blue-eyed Friend,
F. W. C.
I am a sentence of 11 letters.

My 6th, 4th, 7th, and 8th, is a fruit.

 My 1st, 10th, 7th, and 3d, is used for fuel.
My 11th, 2d, 9th, and 9th, is a loud screech.
My 2d, 7th, and 3d, is what every one does.
My 9th, 4th, 7th, and 1st, is a long stride.
My 1st and 7th is an abbreviation for father.
My 3d, 7th, 6th, 10th, and 8th, is a small light.
My 4th, 7th, 5th, and 9th, is a person of rank.
My whole has written many interesting books.

Dear Sir:
My little daughter has handed me the following puzzle to
send to you for your next number, which please insert, and
oblige
A Subscriber.

My 8th, 2d, 9th, 19th, 24th, 4th, was a celebrated English

poet.
My 3d, 26th, 14th, 16th, 27th, is one of the elements.
My 21st, 11th, 6th, 7th, 26th, 8th, exists only in
imagination.
My 14th, 9th, 10th, 5th, 19th, is a gaudy flower.
My 4th, 11th, 20th, 13th, 17th, 16th, 26th, 9th, was a
Swiss philosopher.
My 19th, 1st, 5th, 22d, is various in form and expression.
My 9th, 15th, 28th, 26th, 14th, is an article of extensive
commerce.
My 12th, 13th, 9th, 4th, 19th, 24th, 27th, was strikingly
exemplified in
My 4th, 7th, 8th, 1st, 26th, 4th, 6th, 14th, 1st, 16th, 14th,
15th, 5th, 4th, 6th.
My 19th, 26th, 19th, 26th, 3d, is a foreign production.
My 14th, 16th, 23d, 10th, was a famous archer.
My 13th, 14th, 26th, 14th, 9th, 16th, is pale and
motionless.
My 24th, 26th, 25th, 18th, 23d, is much used in one of
the polite arts.
 My 6th, 2d, 13th, 14th, 14th, 1st, 2d, 9th, 26th, 8th, 8th,
2d, 22d, 6th, asks your opinion of my whole.

Philadelphia, April 6, 1842.

Mr. Merry:
You will pardon the liberty that one of your juvenile
admirers has taken, by sending you a puzzle for your
invaluable Museum. The subject is one that you are very
familiar with, and as I have but just made it my subject,
perhaps full justice may not have been done to its character. I
have at least tried to make the best of it.
Elizabeth.
I am composed of 9 letters.

My 4th, 8th, 6th, is the retreat of a wild beast.

My 9th, 2d, 4th, is the name of the Creator.
My 4th, 2d, 5th, is a female deer.
My 6th, 8th, 4th, is a nickname for a boy.
My 3d, 2d, 8th, is what cloth is made from.
My 1st, 3d, 5th, is a scripture denunciation.
My 7th, 5th, 9th, is a part of the human frame.
My 9th, 2d, 9th, is a record kept by seamen.
My 2d, 4th, 8th, is a piece of poetry.
My 4th, 3d, 6th, is a Spanish title.
My 4th, 2d, 9th, is a sagacious animal.
My 9th, 8th, 7th, 6th, is a romantic spot.
My 6th, 3d, 4th, is where Adam’s first son went and
dwelt.
My 7th, 8th, 6th, 4th, is an act of friendship.
My 4th, 3d, 1st, 6th, is an article of commerce.
My 9th, 3d, 1st, 6th, is a female dress.
My 9th, 2d, 1st, 8th, 6th, is a Scottish name for a small
flower.
My 8th, 4th, 5th, 6th, is the first spot inhabited by human
beings.
My 9th, 3d, 2d, 4th, is what all people should be.
 My whole is what my friend Robert Merry has found very
useful to himself in moving through the world.

Utica, April 9, 1842.

Mr. Merry:
I am a subscriber to your Museum and have been very
much pleased with it. I write to let you know that I wish very
much to have you continue the story of Philip Brusque. I wish
to know whether the people lived contented under the
government of M. Bonfils, and if they ever got away from the
island. I live at Utica, and was much pleased with the account
of your visit to this place thirty-five years ago.
From a Blue-eyed Friend,
Samuel L********.

Dear Mr. Merry:

If it is not too much trouble, I should like to know what
became of Brusque, and if Mr. Bonfils made a good king. With
some assistance, I have found out the answers to three of
those puzzles which were in the last Magazine. The first is
Mother, the second Charles Dickens, and the fourth
Prince de Joinville.
If the following be worthy a place in your Magazine, by
inserting it you will oblige
A New Hampshire Boy.
I am a name of 11 letters.

My 10th, 11th, 8th, is a useful grain.

My 3d, 4th, 8th, is an industrious insect.
My 1st, 2d, 7th, 4th, is an ancient city.
My 6th, 2d, 5th, 11th, is a name often given to a royalist
in the Revolution.
My 9th, 2d, 3d, 3d, 4th, 5th, is a bad man.
My whole, Mr. Merry, you know better than I do.