Auditory attention — focusing the searchlight on sound
Jonathan B Fritz, Mounya Elhilali, Stephen V David
and Shihab A Shamma
Some fifty years after the first physiological studies of auditory
attention, the field is now ripening, with exciting recent insights
into the psychophysics, psychology, and neural basis of
auditory attention. Current research seeks to unravel the
complex interactions of pre-attentive and attentive processing
of the acoustic scene, the role of auditory attention in mediating
receptive-field plasticity in both auditory spatial and auditory
feature processing, the contrasts and parallels between
auditory and visual attention pathways and mechanisms, the
interplay of bottom-up and top-down attentional mechanisms,
the influential role of attention, goals, and expectations in
shaping auditory processing, and the orchestration of diverse
attentional effects at multiple levels from the cochlea to the
cortex.
Addresses
Centre for Auditory and Acoustic Research, Institute for Systems
Research, University of Maryland, College Park, MD 20742, USA
Corresponding author: Fritz, Jonathan B (ripple@isr.umd.edu)
Current Opinion in Neurobiology 2007, 17:437–455
This review comes from a themed issue on
Sensory systems
Edited by Peter Mombaerts and Tony Zador
Available online 21st August 2007
0959-4388/$ – see front matter
Published by Elsevier Ltd.
DOI 10.1016/j.conb.2007.07.011
of auditory attention. Although of great interest, we will
say little about the psychophysics of selective auditory
attention in extracting salient ‘signals’ from a complex
and noisy acoustic ‘background’, as this topic has recently
been reviewed elsewhere [7]. Since tremendous insights
have been gathered on the mechanisms and effects of
attention in other modalities, particularly visual attention
[8,9], we shall discuss some of the emerging parallels (and
differences) between visual and auditory attention. We
shall focus on recent advances that reveal different ways
in which the neural representation of sound is influenced
by task-specific demands, expectations, and the focus of
attention [10,11,12,13,14,15].
Since the pioneering work of Hubel, Galambos and colleagues [16], it has been known that the responses of
neurons in auditory cortex can be strongly modulated by
attention. Other neurophysiological studies confirmed
these effects of auditory attention, and subsequent human
studies showed that event-related potential (ERP)
responses, including early responses (the P20–P50 — a
mere 20–50 ms after stimulus onset) and the N1 waveform
(100 ms latency) could be influenced by attention
[17,18]. Since these early single-unit and ERP studies,
there has been a gathering interest in the neurobiology of
auditory attention, using a variety of approaches and techniques, including psychoacoustic, behavioral, neurophysiological (in single-unit, multi-unit, local field potential
(LFP) and whole brain EEG studies), MEG (magnetoencephalography), and functional neuroimaging (PET and
fMRI), all of which have added considerably to our insights
into the nature of auditory attention.
Introduction and overview
Auditory attention allows us to rapidly and precisely direct
our acoustic searchlight toward sounds of interest in our
acoustic environment. Attention can be top-down (voluntary or task-dependent) or bottom-up (sound-based salience). At the interface of perception and action, top-down
attention leads to enhanced information processing, behavioral sensitivity, and shortened response latencies. Topdown attention is a selection process that focuses cortical
processing resources on the most relevant sensory information in order to maintain goal-directed behavior in the
presence of multiple, competing distractions and comprises
several distinct behavioral and neural processes operating
at multiple levels [1,2,3,4,5]. Bottom-up ‘pop-out’ attention also plays an important role in ‘reading’ the acoustic
scene and selectively gating incoming salient signals [6].
This review seeks to provide a roadmap to current
insights and outstanding questions in the neurobiology
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One important methodological caveat and conceptual
caution is that while many human and animal studies
infer the presence of auditory attention (or its absence)
from a combination of task design, subject behavioral
performance, and the ensuing neural effects — attention
itself can be flickering and elusive. It is notoriously
difficult to precisely measure its highly variable selectivity, intensity, and duration. The lack of a commonly
accepted, quantifiable measure of attention bedevils
cross-study comparisons. Although the magnitude of
attentional modulation of neuronal activity may scale
with increasing task difficulty [19,20], this correlation
can be confounded with the effects of task design and
subject behavioral strategy [20]. In studies of human
auditory attention, typical controls are to direct the subject to view a silent video or read a book and to ignore
auditory input, but it is quite possible that the subject
could sneak an occasional ‘listen’ or auditory peek. These
Current Opinion in Neurobiology 2007, 17:437–455
438 Sensory systems
Glossary
A1: Primary auditory cortex.
ACC: Anterior cingulate cortex — medial prefrontal structure likely to
be important in control of attention.
ASA: Auditory scene analysis — decomposition of complex mixture
of incoming sounds into individual sound sources and sound streams.
ERP: Event-related brain potentials (averaged EEG segments timelocked to stimulus onset).
FBD: Foreground–background decomposition — separation of
foreground sound stream of interest from background acoustic
scene.
MMN: Mismatch negativity — a negative waveform in the deviant
ERP response that occurs about 150–200 ms after stimulus onset,
evoked by an ‘oddball’ stimulus in a sound sequence in which rare
sounds (‘deviants’) ‘pop-out’ in contrast to the repeated ‘standard’
sound. MMN is based on largely pre-attentive mechanisms, but can
be influenced by attention.
N1 (also known as the N100): First negative wave in ERP, occurring
100 ms after sound onset, followed by the N2 wave, occurring
200 ms after sound onset (later N2b is associated with auditory
attention).
P2 and P3 (also known as the P200 and P300): ERP positive waves
following the N1, occurring 180 ms and 300 ms after sound onset
(like N2b, later P3b is also associated with auditory attention).
PFC: Prefrontal cortex — important component of frontal–parietal
attentional network and likely to play a major role in setting goals and
expectations, allocating and directing attentional resources,
monitoring ongoing events in a short-term memory buffer. PFC is also
a source of top-down projections that can dynamically shape sensory
cortex in accord with changing task demands.
SSA: Stimulus-specific adaptation — in probabilistic settings, in
which one stimulus is common and another is rare, responses to
common sounds adapt more strongly than responses to rare sounds.
SSA, measured at a cellular level in auditory cortex, precedes and
may induce the neural activity giving rise to MMN.
SNR: Signal-to-noise ratio — in a physical acoustics sense, the ratio
of the target signal amplitude in comparison to background noise
(clutter) amplitude.
STRF: Spectrotemporal receptive field — a characterization of both
the spectral and temporal tuning properties of an auditory neuron,
usually measured with reverse correlation or related regression
techniques.
difficulties present real challenges for experimentalists
studying auditory attention in both humans and animals.
Relationship between pre-attentive and
attentive processes in auditory scene analysis
In order to focus auditory attention on specific acoustic
objects of interest in the real world, we typically make use
of a combination of auditory spatial cues and auditory
feature cues to solve the pattern recognition problem of
foreground–background decomposition (FBD). This is
illustrated by one of the best known examples of auditory
attention, the ‘cocktail party effect’, in which we can
attend and selectively eavesdrop on different speakers in
a crowded room brimming with multiple conversations.
Cherry [21] speculated on possible cues to its solution,
including location, lip-reading, mean pitch differences,
different speaking speeds, male/female speaking voices,
and distinctive accents. Beyond the cocktail party
example, sound sources may differ in a variety of acoustic
Current Opinion in Neurobiology 2007, 17:437–455
dimensions (such as location or trajectory, instantaneous
fundamental frequency, harmonicity, intensity, duration,
rhythm, or the patterns of energy envelope modulation in
different frequency bands) that facilitate grouping. Whatever the combination of cues, or the exact mechanisms
involved in deciphering them [22], we accomplish this
remarkable feat of selective attention to a single stream
on a daily basis in varied acoustic environments with
multiple sound sources. In order to do this, listeners must
develop great proficiency at auditory scene analysis (or
ASA), the process of segregating and grouping sounds
from the mixture of sources that typify our acoustic
environment to form representations of relevant auditory
streams or objects [23–25]. This process of selectively
directing attention to a single auditory stream in a complex, multisource auditory scene with different auditory
elements vying and jostling for attention, may actually
shape our perceptual organization of the elements in the
scene [26]. Another familiar variation of the cocktail party
effect occurs in the musical version when a listener
focuses on the ‘voice’ of a single musical instrument
playing in an ensemble [27]. Many animals are also
extraordinarily adept at ASA, and there are numerous
ethological parallels to the cocktail party, such as emperor
penguins identifying the display call of their mate or
offspring in the midst of a raucous cacophony of colony
babble [28], or vampire bats identifying characteristic
individual human snoring and breathing sounds [29] in
polyphonic jungle soundscapes.
Some have argued that an auditory stream can be formed
completely without attention [30], but once formed it can
become an object of attention. Others have presented
experimental evidence in favor of a role for attention in
the formation of auditory streams [31]. The controversy
about the contribution of attention to ASA and stream
formation has led to considerable experimentation on this
fundamental question, which continues to be the focus of
intensive research. Overall, the extraction of signal from
noise and the separation of foreground from background
is likely to be a multi-stage process that draws on bottomup gestalt grouping primitives, on auditory memory (our
prior knowledge or expectations of the auditory ‘players’
in the acoustic scene), on attention, as well as other forms
of top-down control (Elhilali et al., unpublished data)
[32,33].
A crucial and ubiquitous survival skill in the toolkit of
animal hearing is the ability to detect the presence of
novel or ‘deviant’ sounds amidst the familiar hum of
background environmental noise. There is evidence that
the brain has evolved a fairly sophisticated novelty detection system that includes an automatic, pre-attentive
component that assists in parsing the acoustic scene into
streams and analyzes stability and novelty, even for taskirrelevant streams [34–37]. In this system, repetitive
stimuli are generally ignored and deviant or ‘oddball’
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Auditory attention — focusing the searchlight on sound Fritz et al. 439
stimuli ‘pop-out’. Oddball detection has been particularly
well studied in the auditory system, but is likely to share a
common neural network with deviance detection in other
modalities [38,39].
The acoustic change-detection system comprises an interconnected set of elements, including ‘adaptive’ neurons,
with generalized stimulus adaptation responses, and also
more specialized acoustic ‘novelty’ detection neurons that
encode stimulus deviation from the pattern of preceding
stimuli. ‘Novelty’ signals have been studied primarily at a
cortical level, but may occur as early as inferior colliculus
[40], suggesting the possibility that subcortical pathways
for change detection may play a role in directing attention
to novel sounds. However, an alternative explanation [41]
is that the ‘novelty’ responses in the inferior colliculus arise
from top-down cortical projections. Two EEG signatures
for change detection have been described in the human
brain: first, the attenuation of an early (100 ms) N1
response with repeated stimulation and secondly, the
evocation of a later (100–200 ms) mismatch negativity
(MMN) response when a novel stimulus occurs after a
repetitive sequence of acoustic ‘standard’ stimuli [42].
Although the N1 wave may represent change-detection
processes distinct from MMN [43], the main focus of
change-detection studies has been on MMN. As mentioned, MMN is evoked in response to any infrequent,
discriminable acoustic change in the stimulus stream and
can be elicited by deviations in stimulus frequency, intensity, duration or spatial location, or by irregularities in
spectrotemporal sequences (over periods as long as 20 s),
or in other patterns of complex sounds including speech
[44,45] and music [46,47]. MMN has been shown to be
sensitive to changes in global acoustic context. Since
MMN to elementary acoustic events can be evoked in
sleep or under anesthesia, or when attention is diverted to
other modalities, these novelty responses are believed to
be largely pre-attentive. This deviancy detection system
continuously monitors the auditory environment, tracks
changes, and dynamically updates its representation of the
acoustic scene [44] and is likely to be composed of parallel
sensory (refractory-response-based) and cognitive (memory-comparison-based) components [48]. The source of
MMN may shift depending upon the auditory areas analyzing the deviant acoustic change. The underlying basis of
MMN is thought to be that incoming sounds are compared
with the current neural representation of regularities in the
acoustic scene and ‘oddball’ sounds that do not match the
representation elicit MMN. Once the novel sounds are
identified by the automatic detection system, they activate
an attentional ‘interrupt’ involving frontal activation.
These ‘flagged’ novel sounds can then be analyzed further
to see whether they may merit attention and behavioral
response (the pre-attentive salient filters may also automatically enhance responses to stimuli that have instinctive or learned biological importance). Although MMN can
be elicited independent of attentional state, under certain
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conditions it can also be modulated by attention [18,30,49–
53] and hence may be thought of as ‘semi-automatic’. Topdown control may trump involuntary attention switching to
task-irrelevant distractor sounds through attentional
modulation by the prefrontal cortex of the deviance detection system in the auditory cortex [54]. In target detection,
the ‘pre-attentive’ MMN can also occur in conjunction
with other later ERP components associated with focused
attention (the N2b (200–300 ms after stimulus onset) and
the P3b (300–350 ms after stimulus onset), which may be
generated by activity in the anterior cingulate and prefrontal cortices [55]. The presence or absence of these late
ERP components can be used to ascertain whether or not
subjects actually attended to sounds detected by their preattentive deviance detection system. There is also a ‘cognitive’ component of the MMN as shown by its sensitivity
to linguistic change. Recent studies have reported a leftlateralized ‘phonological MMN’ for native phonetic features. MMN has been reported to reflect categorical perception of consonants and vowels, and MMN response
characteristics are influenced by the lexical status and
grammaticality of a word string, and even the semantic
meaning of words used as deviant stimuli [45]. A preattentive ‘cognitive’ ERP, similar to MMN, can be elicited
by violations of musical harmony or syntax [56]. Thus,
MMN can be evoked by changes in a series of highly
complex acoustic stimuli, and by cognitive rules, as well as
by low-level acoustic changes in tone-pip frequency or
intensity.
Considerable effort has been directed to discovering the
neural basis of this fast, pre-attentive, ‘bottom-up’ novelty
detection system in the human brain, and there is debate as
to whether the dominant locus of MMN cortical generation
in auditory cortex might vary as a function of changing
acoustic features. A recent study [57], combining EEG
and fMRI, suggests that at least three cortical regions are
involved in MMN, including primary auditory cortex,
cortical areas in the planum temporale and neighboring
posterior superior temporal gyrus, and ventrolateral prefrontal cortex. The authors conjecture that these regions
may comprise a functional hierarchical network, with corresponding initial detection of acoustic change in A1 (or
below), further feature analysis of the identified change in
higher auditory areas, and attentional gating in prefrontal
cortex if the acoustic change is deemed sufficiently novel or
salient [57]. Although the MMN has been attributed to a
comparison of incoming sounds with a sensory memory
‘trace’ of previous repetitive acoustic features, questions
remain about the relative contributions of the temporal and
frontal lobe generators [58], and a recent combined MEG
and fMRI neuroimaging study [59] suggests instead that
the MMN is generated as a result of differential stimulusspecific adaptation of two distinct auditory cortical N1
sources. Recent promising animal studies have emphasized the importance of stimulus-specific adaptation (SSA)
in A1 as a possible neuronal mechanism underlying this
Current Opinion in Neurobiology 2007, 17:437–455
440 Sensory systems
initial stage of ‘oddball’ detection [60,61]. In these studies,
SSA was not observed at the thalamic level [60]. As few
neurophysiological studies of SSA have been performed in
higher auditory areas [41,62], it remains to be seen whether
single-unit studies of SSA can help pinpoint the source of
MMN generation. Although detailed mechanisms are still
unknown, MMN generation, but not early stimulus onset
responses, is suppressed by blockade of NMDA receptors
[63]. Although promising, further studies of the molecular
and cellular basis of MMN must await further development of a good animal model system, ideally one in which
simultaneous event-related potentials (with results comparable to human MMN) and single-unit recordings can be
conducted simultaneously [41].
The common behavioral design of many human MMN
studies consists of subjects listening passively to a stream
of auditory stimuli in the oddball paradigm — with no
measure of the behavioral effects of the deviant acoustic
stimulus in the stream. Without such a measure, it is not
possible to distinguish between automatic neural
responses arising from acoustic variability and responses
related to ‘attentional capture’. In fact, the network
activated during involuntary auditory stimulus-driven
‘attentional capture’ [64] is neuroanatomically similar
to the dorsal fronto-temporal spatial attention network
[65,66] activated during voluntary focus of auditory attention and may be complementary to the ventral ‘MMN’
network composed of bilateral superior temporal gyri and
inferior frontal gyri, which automatically responds to
acoustic variability independent of task salience or auditory attention.
The automatic component of the change-detection system
may rely upon a concatenated set of basic habituation
mechanisms and what Bregman referred to as a ‘bottomup’ or ‘primitive’ grouping [23]. Automatic pre-attentive
ASA is certainly not the only route to acoustic scene
segregation — for example, attention may play an important role by limiting the processing of unattended input in
favor of attended streams of input [37]. In addition, Bregman suggested a set of top-down grouping processes that
he termed ‘schema-driven’ mechanisms on the basis of
acquired expectations from prior experience or knowledge.
Recent results also suggest the presence of at least two
cortical mechanisms of streaming — an automatic ‘preattentive’ segregation of sounds and a streaming mechanism that builds up over a period of up to several seconds
that can either be pre-attentive or modulated by attention
[24,30,31,34,67–69]. Additional areas may be recruited,
such as the intra-parietal sulcus [70], which was differentially activated depending upon whether subjects heard
either one or two streams (this same area is activated in
visual scene segregation and may be involved in supramodal scene analysis). The process of auditory scene analysis
sets the stage for further attentional selection and seamlessly interacts with the auditory attention system
Current Opinion in Neurobiology 2007, 17:437–455
[36,48,71]. The existence of this capacity for automatic
pre-attentive scene analysis can free up attentional
resources to ‘fine-tune’ segmentation of a complex acoustic scene [31], or focus on individual streams and extract
meaning from the attended stream [30]. Thus, even a
simplified explanation of the cocktail party effect must
include an understanding of the interplay between ASA,
and our abilities to selectively direct spatial attention to
specific sound sources within the acoustic scene and to
direct featural attention by focusing on distinctive acoustic vocal features (such as fundamental frequency, timbre, accent, intonation) in order to identify individual
speaker voices, all interwoven with top-down disambiguation processes, that assist in the retrieval of lexical
information in noisy speech conditions [72] and help
parse phonetic input in accord with the semantic line
of the conversation.
Auditory spatial attention
Depending upon whether an auditory task requires
attending to a spatial location, or to an auditory feature
or object, there may be differential activation of the
auditory ‘what’ and ‘where’ pathways [73–75]. Attentional
mechanisms can modulate neural activity encoding the
spatial location and/or the acoustic attributes of the
selected targets and the early sensory representation of
attended stimuli [2]. For simplicity, we shall distinguish
between auditory spatial and non-spatial featural attention in the present and subsequent sections, although as
our discussion of the cocktail party problem illustrates, we
are usually confronted in the real world with acoustic
challenges that require a combination of both.
Spatial attention is supramodal — in the sense that crossmodal (visual or tactile) spatial cues can enhance the
auditory ERP for acoustic stimuli presented in the same
location [76]. A series of recent neuroimaging papers has
emphasized the presence of a shared frontoparietal neural
network for both visual and auditory spatial attention
[65,66,77]. Impairment of this network, which includes
medial frontal cortex and frontal eye fields, cingulate and
posterior parietal cortex and anterior insula, can lead to
combined visual and auditory neglect [78–80]. In the
overlapping auditory and visual spatial attention network,
the PFC plays important roles in tracking task goals and
biasing sensory cortices toward task-relevant stimuli, the
ACC is critical for executive attentional control, the FEF
contributes to attentional orienting, and posterior parietal
cortex in the human superior parietal lobule (and homologous monkey LIP) also shows enhanced responses to
salient stimuli [81,82].
Top-down modulation of spatial attention in the visual
system appears to work at multiple cortical and thalamic
processing levels to achieve different functional goals [4].
The latency of attentional effects can be variable depending upon the task — a recent study [83] of top-down
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Auditory attention — focusing the searchlight on sound Fritz et al. 441
feedback underlying visual spatial attention demonstrated relatively long-latency (150–250 ms) attentional
effects in V1, occurring well after the initial stimulusdriven response (60–90 ms). A recent study has shown
that microstimulation of the FEF (frontal eye fields) at
levels too small to elicit eye movements leads to increased
behavioral sensitivity for visual motion or stimulus change
at that location and other attention-like enhancement of
V4 responses [84]. Although these results suggest that a
tight coupling can exist between planned eye movements
and predictive attentional gain increases in the primate
visual system, however other recent work has shown that
the oculomotor system can be decoupled from the attention system. There is evidence that FEF is a component
of a spatial attention system independent of eye movements [82,85,86] and plays a role in covert spatial attention (without eye movements). Nevertheless, given the
presence of increased FEF activity preceding aurally
guided saccades [87], one might predict selective gain
increases in auditory cortical activity following FEF
microstimulation.
In fact, evidence for top-down modulation of spatial
attention in the auditory system has recently been
obtained in studies of the barn owl [88]. The barn
owl is a superb animal model for auditory attention since
it has developed neural mechanisms for exquisitely
focused spatial auditory attention in order to optimize
sensory processing by using an ‘auditory searchlight’
directed toward its prey. Microstimulation of the forebrain gaze control field in the barn owl (analogous to the
frontal eyefields in primates) sharpened the spatial
selectivity and enhanced the responsiveness of matched
space-specific neurons in the topographic map of auditory space in the deep layers of the midbrain tectum. By
contrast, responses of neurons with preferred sound
receptive fields outside the stimulated arcopallial gaze
field (AGF) location suppressed responses. Moreover,
since the AGF controls both visual and auditory gaze,
this suggests multimodal integration and shared
mechanisms for visual and auditory attention (Winkowsky and Knudsen, unpublished data) [89]. In a
natural context, such top-down attentional signals in
the owl could spotlight a spatial location and by sharpening auditory as well as visual tuning, it could enhance
precision of spatial localization for sounds and visual
stimuli emanating from this point in space. As mentioned, these results are especially intriguing because
the pathways for top-down modulation of auditory and
visual attention in the owl are so closely parallel those
described for descending modulation of visual attention
in the primate from the frontal eyefields to the superior
colliculus [84]. These results also suggest that the
strategy that the brain uses to direct the spatial attentional spotlight is common to both sensory modalities,
and the pattern of top-down modulation may be highly
conserved across species [5].
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Auditory feature and object attention —
extracting signals from background
A variety of complex, shifting acoustic soundscapes present enormous challenges for acoustic scene analysis and
for attentional focus on auditory features or objects such
as environmental soundscapes (such as a morning chorus
of birds), polyphonic music and speech. Top-down attention can selectively focus on a limited range of an acoustic
feature dimensions [7], or can even focus on the expected
(or recalled) features of an auditory target [15]. Although
bottom-up salience certainly plays a vital role, voluntary
auditory attention is the key to highlighting foreground
over background and switching attentional focus to different features, objects, or streams of interest within the
acoustic scene [10,11,13,27,34,90,91].
In an ongoing set of animal studies on auditory attention,
selective spectral attention in single tone and multi-tone
detection and two-tone discrimination tasks has been
shown to rapidly reshape neuronal receptive fields in
primary auditory cortex to enhance responsiveness at the
target frequency and suppress responsiveness at adjacent
spectral frequencies [10,11,12,92,93]. Similar spectral
receptive-field effects were observed when the task was
to detect a target tone signal in the midst of a noisy
background [94]. By contrast, a distinctive set of
temporal changes in cortical spectrotemporal receptive
fields was found [95] when the animals engaged in
temporal tasks (such as silent gap detection, duration
discrimination, or click rate discrimination). These
results suggest that top-down signals can adjust attentional filters precisely and rapidly to dynamically reshape
receptive fields in the primary auditory cortex in accord
with salient target features and task demands [12].
Recordings from the orbital prefrontal cortex of the
behaving ferret [96] have shown rapid onset (75–
150 ms latency) phasic and sustained target responses,
independent of the acoustic characteristics or identity of
the target stimulus. These prefrontal target responses
were often behaviorally gated, developed rapidly and
may contribute to target recognition during task performance. Future experiments will investigate whether such
prefrontal activity plays a role in top-down influence over
primary sensory filter properties.
Most studies of attentional effects in visual cortex have
emphasized modulatory changes in background firing rate
and contrast gain control, and hence an additive or multiplicative enhancement of feature tuning curves [97].
However, there is recent evidence in V4 for modulatory
effects of attention, leading to shifts in neuronal tuning,
and hence in the neural representation of stimuli [98,99].
These results in visual cortex, and parallel findings in the
auditory cortex, are consistent with a matched filter
model, in which neurons shift their tuning properties
toward attended features in order to increase processing
efficiency (David et al., unpublished data) [10,11,12].
Current Opinion in Neurobiology 2007, 17:437–455
442 Sensory systems
Human behavioral studies have shown a dissociation
between a pre-attentive, low-level sound segregation
process and an attention-dependent process that can be
called into play in forming perceptual objects and
streams. The perception of streaming can take up to
several seconds to build up, and this attention-dependent
streaming mechanism can be reset by an attentional shift
[31]. There is a similar build-up at the neural level,
measured by modulations in ERP in auditory temporal
cortex [69] and in a recent MEG study [34].
Considerable work on the neural basis of attention to
speech has recently been reviewed [100], focusing on
neuroimaging studies of the attentional selection of foreground speech, differing by location or speaker identity
from concurrent background speech. Selective attention to
the human voice (compared with a silent reading condition) enhanced brain activity bilaterally in the superior
temporal sulcus, higher auditory cortex, inferior frontal
cortex, though not in the prefrontal cortex [101]. This
was not the case for a selective-attention working memory
task where subjects were asked to attend to either voice
identity or location [102]. In this study, attention to voice
location evoked greater activation in the dorsal prefrontal
cortex, whereas relatively greater activation for voice identity was observed in the ventral prefrontal cortex. As might
be expected, task conditions could also change the pattern
of brain activation for attention to speech — for example,
the left hemisphere temporal areas were dominant during
speech comprehension tasks, whereas right hemisphere
temporal areas were activated preferentially during attention to prosody [100]. If subjects were presented with the
same set of speech stimuli but were asked to attend to
specific linguistic stimulus categories in different task
conditions, striking differences were observed in the pattern of activation with temporal lobe auditory areas [103].
Moreover, our greater familiarity with speech than with
other acoustic stimuli may cause differential effects in
otherwise similar task conditions. For example, although
the PFC is activated in listening tasks that require selective
attention to location, pitch cues, or even attentional listening to dichotic CV syllables [104], PFC was not activated
during selective attention to the human voice [101]. ERP
recordings showed a very different pattern of activity when
listeners either were asked to identify concurrent vowels,
or were asked whether one or two auditory objects were
present using mistuned harmonic information [25]. Given
the paramount importance of speech to our daily lives,
research on both pre-attentive and attentional processing
of speech is valuable — to study speech comprehension
and auditory selective attention to speech as an information
channel in the presence of background noise (which may
help to develop improved automatic speech recognition
systems) and also to understand the process of attention to
the vocal features that reveal speaker vocal identity and
vocal prosodic qualities that color speech (such as mood,
emotional inflection, and nuance).
Current Opinion in Neurobiology 2007, 17:437–455
Research has also begun to explore the neural basis of
auditory attention to music, which presents a complex
challenge similar to that presented by selective auditory
attention to speech [56]. As an example of future directions, a recent study [105] has shown that attention can
enhance ERPs elicited by deviations in harmonic context.
Auditory attention in time
Precisely focused temporal expectancies, such as musical
expectancies, are likely to be very important in auditory
processing since many auditory patterns unfold in time. A
recent ERP study has shown that auditory attention can
be temporally directed to focus on events that are projected to occur at a particular future point in time [106]. In
another study, subjects engaged in an auditory task could
avoid involuntary attentional capture by distracting
acoustic stimuli, by foreknowledge of when the taskirrelevant acoustic changes would occur [107]. Performance improved for subjects who were cued when to listen
for an acoustic target [108]. A combination of temporal
and spatial cues was particularly effective [106,108].
Temporal foreknowledge of acoustic events can lead
not only to enhancement of cortical responses but also
to their suppression, particularly when the sounds are
self-triggered [109]. Recent research has also begun to
explore other aspects of timing in auditory attention, such
as the role of attention in auditory temporal discrimination [110] and in event segmentation in music [111].
General principles are likely to apply to both auditory and
visual attention selectively directed to different points in
the dimension of time [8]. There is evidence that the
neural basis for temporal expectancies and temporal
discrimination is supramodal [112–114] and involves a
network including prefrontal cortex, basal ganglia, and
cerebellum. Top-down modulation of neural responsiveness during temporal attention, can be precise and influence timing in primary and higher order visual cortex
[115,116]. There is abundant experimental evidence for
unimodal and crossmodal temporal attentional effects for
auditory as well as for somatosensory and visual tasks.
Attentive imagery in silence and hallucinations
In auditory induction (such as the familiar psychoacoustic
phenomena of FM completion or phonemic restoration)
the auditory system fills in occluded information, as when
missing foreground sound segments are perceptually
restored in the presence of background sound
[23,117,118]. Although it might seem at first glance like
a reasonable candidate for top-down effects, there is
considerable evidence for pre-attentive mechanisms in
auditory induction [118], though this may be influenced
by attention in phonemic restoration [119]. However,
there can be remarkably strong effects of top-down attention on auditory processing in active listening, as observed
in studies that have shown that human auditory cortex
is activated in silence, in the complete absence of any
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Auditory attention — focusing the searchlight on sound Fritz et al. 443
real-world acoustic stimulation, when there is simply an
inner expectation of sound [66,120,121], during the short,
quiet interlude of musical transitions [111], or when
subjects are imagining auditory stimuli [122], or when
they are prompted by silent visual stimuli that are usually
accompanied by sound [123,124]. In a recent neuroimaging study of auditory attention [125] subjects were
asked to indicate when they heard a noise burst following
a silent period of variable duration. In addition to activation of frontal cortical areas implicated in attentional
control, imaging also revealed increased activity in auditory cortex contralateral to where the sound was expected
to occur while the subjects listened in silence (as well as
enhanced responses to the stimulus itself). In another
recent neuroimaging study [126] subjects also listened to
musical passages in which silent gaps had been introduced. If the subjects were familiar with the music, they
heard ‘the music in their mind’ throughout the silence,
although this was not the case with unfamiliar music. This
is an extraordinary display of the importance of attentive
expectation in shaping cortical responses. Activation of
auditory cortex was greater during the silent gaps inserted
in familiar songs than during silence in unknown songs,
showing the continuous interaction of attention and
memory during active, expectant listening. Auditory cortical activation has also been reported during silent lipreading [123,127,128] or during observation of silent
piano playing [124]. There are parallel findings in the
visual system, indicating top-down attentional increases
in cortical activity in V1 [129] and enhanced reward
timing expectancies [116] even in the absence of a visual
image. These compelling results suggest a general set of
attentional mechanisms for top-down priming of sensory
cortices. Modulatory effects of attentive expectation may
be very similar to the top-down effects of perceptual
decisions and can influence the earliest stages of cortical
auditory processing. This is shown by an ERP study of a
difficult acoustic target detection task [130] in which
activation was highest for subjective perceptual decisions
leading to target-present behavioral responses (even in
cases of false alarms in which the subjects incorrectly
believed that the target was present, in the physical
absence of the target stimulus).
In order to differentiate between imaginary and realworld sound, the brain may rely on a validation system,
dependent upon reciprocal interactions in a neural network including auditory cortex, frontal cortex, and
anterior cingulate cortex (ACC). A recent imaging study
[131] of speech-sensitive auditory cortex during silence
found spontaneous, intermittent episodes of increased
neural activity. In light of previous observations that the
ACC is activated during auditory hallucinations, it may be
that in the ‘default mode’ of the brain, endogenous
activity within auditory regions is modulated by the
ACC. Such spontaneous activity of the auditory cortex
during silence may offer a neural substrate for the dewww.sciencedirect.com
velopment of auditory hallucinations in patients with
acquired deafness or schizophrenia [9,131–133,134].
Effects of auditory attention on receptive-field
plasticity
The adaptive functions of the cerebral cortex rely upon
flexibility and plasticity of information processing networks. Since the topic of plasticity of auditory cortical
processing has been recently reviewed [135], we will
focus in this section on the evidence that attention
may play a decisive role in triggering auditory plasticity,
particularly in the adult brain [12,136]. Parallel studies
have shown that attention can initiate plasticity in other
sensory cortices, as well as in motor cortex [137]. Unlike
experience-induced plasticity in juvenile animals, where
experience alone can induce plasticity by mere exposure
during the sensitive period, adult animals must generally
attend to an acoustic cue for plasticity to be induced for
the attended auditory feature [12,135,136]. A recent
animal study [138] showed that two very different forms
of auditory cortical global plasticity arose during perceptual learning over a period of weeks when rats were
trained, and presumably attended, to different features
(frequency or intensity) of the same acoustic stimulus set.
In another study of global plasticity in A1, rats were
trained on an operant auditory conditioning task. In a
cleverly designed parametric set of task conditions, rats
were variably motivated to respond to the conditioned
stimulus, and a range of performance levels was obtained
corresponding to behavioral importance of the CS [139].
Subsequent A1 mapping showed a CS-specific expanded
representation whose area was directly correlated with
performance level, showing that behaviorally important,
and presumably attended, sounds gain relative representational area.
A complementary set of experimental studies, designed
to explore local neuronal plasticity over a much shorter
timescale (a period of minutes) for animals trained on
multiple tasks, indicates that shifting the selective attentional focus to different acoustic dimensions or features
may be instrumental in dynamically shifting acoustic
spectral filter properties of A1 neurons and swiftly changing from one cortical state to another [10,11]. These
results suggest that rapid auditory task-related plasticity is
an ongoing process that occurs as the animal switches
between different tasks and changes its focus to new,
salient acoustic cues and goals. These changes are persistent and widespread — as many as two-third of cortical
neurons in A1 showed such frequency-selective enhancement during, as well as following, tone detection or tone
discrimination task performance [10,140]. This suggests
that adaptive changes in receptive fields and frequency
response profiles of A1 neurons that shift cortical states or
filter properties depending upon the behavioral demands
of the ongoing task demands can be attentionally gated.
In this view, attention is the key trigger that initiates a
Current Opinion in Neurobiology 2007, 17:437–455
444 Sensory systems
cascade of events leading to the dynamic receptive field
changes to enhance figure/ground separation, by using a
contrast matched filter to filter out the background, while
simultaneously enhancing the salient acoustic target in
the foreground [12]. A recent set of studies examined
attentional modulation for auditory features in a frequency-independent task [141,142,143] and demonstrated a long-term increase in the proportion of
neurons preferring downward contours in A1 of monkeys
trained on a frequency-independent tone contour task (in
which reward was associated with downward contours).
Preliminary evidence from our current studies of A1
activity during a similar frequency-independent contour
task indicates that changes in preferred directional contour also occur dynamically, at short-term as well as longterm time frames [144].
Three relevant sets of animal studies also emphasize the
importance of auditory spatial attention in relation to
plasticity. The optic tectum (OT) of the barn owl contains
matched topographic maps of auditory and visual space.
Barn owls raised during a crucial developmental period
with horizontally displacing prisms rapidly acquire a new
auditory space map in the OT that restores alignment with
the prismatically displaced visual map. Although juvenile
owls readily acquire these new aligned maps of auditory
space as a result of experience, this plasticity is severely
reduced in adults. Similar age dependencies have been
shown for plasticity of the auditory space map in the
superior colliculus in ferrets [145]. In previous studies in
owls, the plasticity of the space map was tested in owls that
were fed dead mice. However, when adult owls were given
the opportunity to hunt live prey for a short period each
day, drawing on their extraordinary nocturnal hunting
skills, and powers of attentive listening, their auditory
maps showed greatly increased adaptive plasticity. This
increased adaptive map plasticity correlated with behavioral improvements in the owls’ hunting prowess [146].
There are multiple factors in the hunting condition that
may have contributed to the increase in map plasticity,
including increased arousal, and what is likely to be the
key, greater auditory and visual attention to a highly salient
bimodal source (movements of the live mice prey provided
the owl with correlated auditory and visual information)
that could enhance crossmodal integration and thus help
calibrate the auditory and visual space maps. Additional
recent experimental evidence also shows that training can
induce enhanced plasticity of auditory localization in the
adult mammalian brain [147]. Adult ferrets rapidly
relearned to localize sounds following reversible occlusion
of one ear, but only if they performed an auditory localization task that used these cues, not if they performed a
comparable visual localization task. In both examples,
auditory attention appears to be essential to elicit adult
plasticity. The third study is a preliminary investigation of
behaviorally driven plasticity in the spatial sensitivity of
neurons in the dorsal zone of the cat primary auditory
Current Opinion in Neurobiology 2007, 17:437–455
cortex [148]. The spatial tuning curves of dorsal zone
neurons were sharpened when the animals performed a
sound localization task, compared with the same neurons
when the animal was either engaged in a simple sound
detection task, or listened passively to the stimuli. Thus,
selective attention to a spatial task can lead to rapid spatial
receptive-field plasticity results from selective attention to
the spatial task.
In addition to the evidence from animal studies, attention-driven plasticity has also been shown to occur in the
human auditory cortex for spectral, temporal, complex
spectrotemporal, and spatial processing [32,110,149–152].
For example, in a study of the neural basis of rapid
perceptual learning, listeners were trained to segregate
concurrent double-vowel stimuli [33]. In parallel with
improved performance, there were rapid changes in
ERP amplitude within the first hour of training, consistent with top-down modulation. By contrast, no changes in
ERP amplitude were observed in the absence of attention
to the double-vowel stimuli (this was shown in a separate
group of participants, given the same acoustic exposure,
but instructed to ignore the double-vowel stimuli and
attend visually to a muted movie of their choice). The
presence of dynamic plasticity in cortical representation
of acoustic space has been suggested by studies of the
ventriloquism after effect [153] and supported by subsequent research showing that spatial auditory attention
can also drive auditory spatial plasticity [152]. Attention
to target frequency in a discrimination task rapidly changed the tonotopic map in primary auditory cortex,
expanding the distance between the two discriminant
tone pair frequencies [152]. In all of the studies described
in this section, attention appears to have fast and also
slow, lingering plastic effects — raising twin questions:
specifically, what determines the duration of the persistent plasticity triggered by attention, and more generally,
what is the nature of the neural trace that attention leaves
in its wake?
Intermodal and crossmodal interactions
between auditory and visual attention
There are many similarities between attention in the
auditory and visual modalities, where a two-component
framework for attentional selection (top-down and bottom-up) has also emerged from psychophysical, behavioral, and neurobiological studies. Two sets of
mechanisms are thought to operate in parallel in both
modalities: using either bottom-up, automatic, imagebased saliency cues or top-down, attentional, task-dependent cues. Another fundamental similarity is that
attention can modulate both spatial and non-spatial feature processing in both modalities. Moreover, in addition
to these similarities, there is now mounting neuroimaging
evidence for visual modulation of activity in many auditory cortical fields [154] and a growing realization that all
cortex is multisensory [155] that was presaged by earlier
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Auditory attention — focusing the searchlight on sound Fritz et al. 445
work, such as a pioneering neurophysiological study of
auditory and visual responses in auditory cortex of monkeys performing a modal selective-attention task [156].
If the brain were to use common but limited attentional
resources, then intermodal attention (attending to only
one relevant sensory modality) might necessitate suppressing responses to the irrelevant sensory input. Several
studies have examined how responses in auditory cortex
to an acoustic stimulus are affected by other (attended or
unattended) ongoing sensory events. In keeping with a
limited resources model, a common finding is that when
attention is drawn away from an auditory event (by the
presence of a visual stimulus and particularly, by attending to a visual task (compared with a no-competitivestimulus baseline)) then auditory cortex generally shows
decreased activity in acoustic stimuli [157–160,161], but
not always [162,163]. Conversely, many of these studies
also find that attention to auditory stimuli enhances
activity in auditory cortex. These basic results were
confirmed and extended in studies [3,164] that examined
unimodal and bimodal task conditions. In the unimodal
auditory task, there are generally greater responses,
particularly in secondary auditory cortical areas when
the subjects were actively, rather than passively, listening
to the acoustic stimuli. In the bimodal case, enhanced
responses in auditory cortex were seen during the auditory attention task and suppressed responses observed
during the visual attention task. Analysis of the functional
connectivity between auditory and visual cortical regions
in visual and auditory tasks indicated a reciprocal inverse
relationship — increases in auditory activation were
directly correlated with decreases in visual activation
(and vice versa). The ability to divide (and switch)
attention between unrelated visual and auditory stimuli
was decreased following transcranial magnetic stimulation that disrupted function of the dorsolateral PFC
[165], thus emphasizing the importance of the PFC in
allocating limited attention and working memory
resources and in balancing simultaneous multiple attentional demands. A related neuroimaging study also used a
bimodal behavioral paradigm [166] to create a conflict
between an auditory or visual target, and a crossmodal
distractor. As the distracting stimulus in the task-irrelevant sensory channel was increased, there was a compensatory increase in selective attention to the target in the
relevant channel and a corresponding increase in activation in the relevant sensory cortex. Moreover, the larger
this increase, the less behavioral interference was
observed. The results of these studies suggest a form
of top-down sensitivity control that regulates the flow of
attended information by modulating the relative
strengths of different sensory information channels.
There are multiple possible levels for intermodal effects
on auditory processing and attention. It is truly remarkable that many of these attentional effects can be
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observed not only at the cortical level but also at the
auditory periphery. A recent study [167] confirmed earlier
work suggesting that visual attention can modulate peripheral auditory responsiveness in the cochlea and in the
cochlear nucleus. In cats, acoustic attention can enhance
auditory responses in the dorsal cochlear nucleus. In
contrast, visual attention to a mouse or olfactory attention
to fish odors reduces auditory responses in the dorsal
cochlear nucleus. In contrast, visual attention [168], and
a visual discrimination task reduces auditory nerve
responses to clicks [169,170]. In humans, evoked otoacoustic emissions can be modulated by auditory attention
in a frequency-specific manner [171]. The massive auditory corticofugal system is ideally suited for attentional
modulation and hence many of these early peripheral
effects are likely to reflect top-down influences. For
example, in mustached bats, cochlear hair cells can be
modulated by activity in the auditory cortex [172].
Another intriguing set of results also bears on the potentially distracting effects of visual stimuli on auditory
attention. In trace auditory fear conditioning there is a
time gap between the end of the conditioned stimulus
(such as a conditioning tone) and the start of the unconditioned stimulus (such as tailshock) in mice. Recent studies have shown that trace auditory fear conditioning
requires attention in mice [173] and also in humans
[174]. Supporting this attentional requirement, trace
auditory fear conditioning is associated with increased
activity in the anterior cingulate cortex (ACC) and is
impaired by lesions of the ACC that may disrupt attention
to the tone-shock contingency [173]. The key point is that
trace auditory fear conditioning can be impaired by distracting visual stimuli, adding yet another twist to the
story of manifold visual influences on auditory attention,
auditory behavior, and auditory-driven brain activity.
Although our previous discussion has emphasized competition between sensory channels in the limited
resources model, in relatively simple low-level task contexts (such as pitch discrimination or contrast discrimination) there may be no conflict over limited attentional
resources since there are apparently sufficient separate
attentional resources for both vision and audition [175].
There are clearly other cases where auditory and visual
inputs both contribute to information processing. Such
cooperative interactions lead to early multimodal integration [176] or to multisensory enhanced activation in
primary and secondary auditory cortex, as in lipreading
[123,127,128], attention to complex audiovisual combination stimuli [177], source localization with bimodal cues
[108,178], ventriloquism [179], or visual cueing in auditory scene analysis [180]. The neural representation of
human walking in the temporal biological motion area is
another example of higher level audiovisual integration — in which both visual and auditory inputs (sound
of footsteps) activate the same area [181]. An early study
Current Opinion in Neurobiology 2007, 17:437–455
446 Sensory systems
[156] showed that neuronal responses in auditory cortex
(during a selective-attention task in which different auditory and visual cues were associated with a two-choice
lever push) were stronger when visual and auditory cues
were in agreement and were reduced when the bimodal
cues were in conflict [156]. A recent physiological study
[143] demonstrated enhanced spike activity in monkey
auditory cortical neurons to task-related visual inputs
(that signaled task onset), but only in an auditory behavior
task-context, suggesting attentional gating of relevant
visual input to auditory cortex. Such attentional or behavioral gating of task-relevant visual input was also
observed in the inferior colliculus of monkeys trained
to saccade to an acoustic target [182].
Neural networks of auditory attention
Auditory attention can be selectively directed to a rich
variety of acoustic features including spatial location,
auditory pitch, frequency or intensity, tone duration,
timbre, FM direction or slope, speech versus nonspeech
streams, and characteristics of individual voices. Given
the multiplicity of acoustic dimensions to which we can
attend and the richly interconnected auditory processing
networks, there are likely to be multiple neural loci for
auditory attention. In fact, the locations of the multiple
loci of attentional influence on auditory information processing are flexible and are likely to be dependent upon
the specific demands of the behavioral task being performed. This has also been suggested to be the case in the
visual system [9,183]. Neuroimaging studies examining
the common neural circuitry underlying the control of
both visual and auditory attention have revealed a largely
overlapping frontoparietal network [66]. Depending upon
task, there may be a segregation of attentional effects
along the what/where pathways, as suggested by a recent
MEG/fMRI paper [2] that provides further evidence for
the presence of dual-selective-attention effects on sound
localization and identification.
Most functional imaging, EEG, MEG (but not physiological) studies find overall enhancement of auditory cortex
activity by selective attention to sound [17,157,184–186].
However, one source of controversy has arisen over
whether attentional effects are found predominantly in
primary or secondary auditory cortex, or can be equal in
magnitude throughout auditory cortex depending upon
attentional demands. In the visual system, there is some
evidence consistent with increased attentional effects at
higher cortical processing areas compared with earlier
cortical areas, but high levels of thalamic modulation [4]
are inconsistent with an ‘attentional progressive hierarchy’,
a concept that has recently been critiqued [9]. In any case,
physiological studies of cortical plasticity induced by auditory attention have shown clear modulation of neuronal
responses in primary auditory cortex [10,11]. Although
some human imaging studies have also shown attentional
modulatory effects in A1 [157,184], as well as in other
Current Opinion in Neurobiology 2007, 17:437–455
primary and secondary auditory cortical regions, another
study [160] has reported greater effects of auditory attention in higher auditory association areas, at least in an
intermodal, dual task paradigm (comparing responses
when one sensory modality is attended and the other is
ignored). Since attentional effects are highly task-dependent, it may be premature to accept the attentional progressive hierarchy model in auditory cortex. As recent
studies have shown, task-specificity of processing and
attentional demands can differentially activate selective
areas of prefrontal and auditory cortex during the performance of different auditory tasks. A preliminary study in the
ferret [187] showed differential patterns of brain activation
in prefrontal cortex and in primary and secondary auditory
cortices using expression of the immediate early gene, cFos, while the animals were engaged in one of two listening
tasks (sound localization or detection of tones embedded in
a noise). The results of this animal study parallel findings of
two recent human neuroimaging studies that also mapped
differential activation in ‘what’ and ‘where’ tasks [2,102].
The task-dependent shift in the distribution of attention
leads to dynamic re-allocation of cortical resources depending upon task demands and underlines the flexibility in
auditory processing.
In addition to auditory cortical areas, there are cortical
association areas whose activity is influenced by auditory
attention. Association areas in the supramodal frontoparietal attentional network [188] are also activated in auditory
attention — such the left precentral gyrus and the right
posterior parietal cortex [65,77,161]. A study of the neural
dynamics of event segmentation in musical symphonies
revealed a right-lateralized network , with peak cortical
activation during the silent period between musical movements [111]. There were successive waves of activity in
two distinct functional networks – first in a ventral frontotemporal network involved in the automatic detection of
salient acoustic events , swiftly followed by activation of a
dorsal frontoparietal network, which may direct attention
to the acoustic event boundary and update the perceptual
scene. This study illustrates the broad range of brain
regions activated during auditory attention. Even a partial
list of additional areas includes limbic cortex, anterior
cingulate cortex, basal ganglia, thalamus (medial geniculate nucleus, pulvinar nucleus), superior colliculus, inferior
colliculus, cerebellum, dorsal cochlear nucleus, and
cochlea. Recruitment of additional brain areas may be
dependent upon task conditions — for example, orbitofrontal cortex and hippocampal paralimbic belt areas are
activated during auditory target detection tasks where the
stimulus decision is based upon ambiguous sensory information [189]. On the basis of computational modeling
[190], neuroimaging [191], physiological [192], and neuroanatomical evidence [193,194] the reticular nucleus of
the thalamus may also be an important site of attentional
modulation, but it has not yet been studied physiologically
during auditory attention.
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Auditory attention — focusing the searchlight on sound Fritz et al. 447
Thus, attentional effects in the auditory system can occur
selectively and at multiple stages throughout auditory
processing [195] and may even occur as early as the
cochlear nucleus or even earlier, in the sensory transduction phase in the cochlea, as demonstrated by studies
of crossmodal selective attention [167,168]. These peripheral attentional effects may be partly driven by local
‘bottom-up’ processes such as habituation, but may also
be influenced by top-down effects mediated by the
descending olivocochlear bundle projections. Given the
range of neural loci where auditory attention is likely to
modulate processing, there may very well be a variety of
mechanisms in play, giving rise to the question of how
these multiple mechanisms are coordinated, orchestrated,
and enacted in concert. It is, of course, possible, that these
multiple levels of attentional modulation operate relatively independently.
In fact, recent studies underline the point that attentional
effects on auditory processing are likely to occur in a
distributed and widespread pattern throughout the auditory cortex. Research on a ‘deaf-hearing’ neurological
patient with extensive bilateral destruction of auditory
cortices (including the primary auditory fields) demonstrated that the patient was still able to marshall sufficient
auditory attention to perceive sound onsets and offsets.
Conscious attentive perception of sound occurrence in
this patient may have arisen from top-down projections
from prefrontal cortex to the remaining non-primary
auditory cortex or multimodal association cortex. Other
insights into attention have arisen from neurological
studies of two forms of auditory neglect: one an attentional deficit associated with basal ganglia lesions, and the
other an auditory spatial deficit associated with parietoprefrontal lesions [78,79].
At a global level, selective attention may channel information into specialized cortical modules localized in one
hemisphere and hence lead to lateralized patterns of
activation. There is considerable evidence for hemispheric specialization of the attentional system — for
example, a study by Zatorre et al. [158] suggests that
auditory attention to either spatial location or tonal frequency activates a common network of right hemisphere
cortical regions (although one may argue that lateralized
functional specialization arises first and that the hemispheric differences in attentional modulation are a consequence). Additional evidence for lateralization was
provided by a recent ERP study [32] that observed plastic
changes in event-related potentials during rapid perceptual learning that occurred in right auditory cortex and
right anterior STG/inferior prefrontal cortex and were
dependent upon auditory attention to the phonetic discrimination task. Clearly, attentional effects may be
highly dependent on task paradigm. For example, differentially lateralized patterns of hemispheric activation
were demonstrated in subjects attending to one of two
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different features (duration or contour) of the same
acoustic stimulus set [13].
A neuroimaging study [27] explored the neural basis of
foreground–background decomposition, by comparing
brain activation patterns when listeners performed a
match-to-sample task for harmonic target tones (drawn
from a stimulus set of tones with distinctive timbres from
15 different musical instruments) against a continuous FM
(frequency modulated) background, to activity arising the
FM background-alone stimulation. They reported
increased foreground-signal related activity in posterior
regions of left auditory cortex, which was insensitive to
masking influence of the background. Admittedly, one
potential complication of foreground–background
decomposition neuroimaging studies, even when using
low-noise fMRI, is that the subjects are already engaged
in distinguishing task-related foreground signals from
background magnet noises (created by switching of magnetic gradients during imaging). However, notwithstanding these technical challenges, a subsequent neuroimaging
study [91] of intentional stream segregation using timbre
cues (comparing activation patterns in an alternating dual
stream of ABAB sequences from two different musical
instruments — trumpet and organ versus a single stream
AAAA or BBBB from either instrument alone), also found
enhanced left hemisphere activation in posterior areas of
the auditory cortex, similar to the activation pattern
described in earlier studies of foreground/background
decomposition [27] and of selective tracking of individual
melodic streams in polyphonic music [196]. This pattern of
activation may be the result of the involvement of working
memory as well as selective auditory attention in performing these tasks.
A recent MEG study explored the neural basis of the nonspatial aspects of attention in the cocktail party effect
using a clever reversal of foreground and background
attentional foci [34]. Subjects engaged in a set of complementary tasks that changed foreground and background
using the same acoustic stimulus set, involving either
listening for frequency change in a rhythmically repeating, constant-frequency target stream amidst a dense
background texture of irregular, random-frequency notes
(‘target’ task), or instead by listening for duration changes
in the dense texture of changing notes and ignoring the
rhythmic, constant-frequency stream (‘masker’ task).
The subjects’ behavior was correlated with their MEG
neural responses indicating that auditory attention
strongly modulated the relative neural representation
of the target. Furthermore, the time course of the neural
build-up of target representation correlated with the
subjects’ gradual perceptual learning and improvement
in target detection.
These data suggest that one important mechanism for
top-down attentional control is through enhancement of
Current Opinion in Neurobiology 2007, 17:437–455
448 Sensory systems
coherent or synchronous neural activity in sensory cortex,
a finding supported by recent results in the somatosensory
[197] and the visual system [198–200]. In the auditory
system, the early ‘transient’ gamma-band response in
primary and secondary auditory cortex has also been
shown to be related to top-down selective attention to
auditory stimuli [72], which may be mediated by the
dorsal anterior cingulate cortex [201,202].
Attention can influence neural activity not only through
synchrony but also through an array of other mechanisms.
Previous neurophysiological studies of visual attention
have suggested that a possible biasing mechanism for
top-down selective attention is an increase in baseline
spiking activity in relevant sensory cortex [203]. Although
such attentional increases have been observed in the visual
cortex, they have not yet been demonstrated in auditory
cortex. Preliminary data from A1 recordings in the behaving rat [204] indicate that there were no consistent changes
in spontaneous activity during a two-tone frequency discrimination task. Surprisingly, evoked multi-unit and LFP
responses were larger in the non-attending condition than
in the attending condition. However, opposite results were
obtained in recordings from the medial geniculate (auditory) thalamus, where an increase in spontaneous activity
was observed during auditory task performance. At present, there is no compelling single-unit neurophysiological
evidence for attention-related increased baseline firing rate
in auditory cortex. On the contrary, all recent single-unit
physiological studies indicate either a decrease in baseline
firing in the attentive state or a lack of consistent gain
changes during auditory attention [10,11,156,205] with
one earlier exception [206]. One puzzle to be resolved in
future research is how to reconcile these physiological
findings from single-cell recordings in the auditory cortex
that indicate an absence of gain changes during attention,
with the results from many physiological studies in the
visual system that show the opposite. Also, how can the
single-unit data from auditory cortex be reconciled with
neuroimaging data that suggest enhanced activity in auditory cortex during attention?
Other mechanisms of attention, observed in physiological
studies of visual attention, are multiplicative modulation of
neuronal responses and attentional increase in effective
stimulus contrast (or contrast gain). Although both are
perfectly plausible mechanisms in auditory attention, such
systematic multiplicative changes in response gain or
changes in stimulus contrast gain during attention without
any change in receptive-field tuning have not yet been
observed in the auditory system. These differences could
be a matter of task design or data analysis, or simply reflect
the paucity of physiological studies of auditory attention
that have been conducted at a single-unit level.
However, as mentioned earlier, there is compelling evidence for an alternate mechanism in primary auditory
Current Opinion in Neurobiology 2007, 17:437–455
cortex in which attention plays a role in adaptively
reshaping receptive fields, depending upon salient task
cues and behavioral context [10,11,12]. Convergent
evidence for matched filter changes in receptive-field
tuning has come from studies in the visual system
[98,99]. Task-dependent sharpening of auditory spatial
receptive fields was also observed in primary auditory
cortex [148] and also been described in visual cortex
[206]. Such adaptive mechanisms enable neurons to
rapidly multiplex in a task-dependent (or state-dependent) manner as has been shown in the visual system [9].
Thus selective attention could be based on short-term
feature-specific plasticity of auditory cortical neurons,
enhancing their selectivity for task-relevant information,
rather than amplifying overall responses. It is an open
challenge to determine the role that these various mechanisms may play in auditory attention.
Summary
Auditory attention involves a distributed network of
auditory cortical and subcortical structures that are activated selectively in a task-specific manner during auditory processing, which also integrate with a generalized
multisensory attentional network that includes parietal,
frontal, and anterior cingulate cortical regions [74,207–
210]. Recent research has revealed a richly interconnected network for auditory attention that assists in the
computation of early auditory features and acoustic scene
analysis, the identification and recognition of salient
acoustic objects, enhancement of signal processing for
the attended features or objects, priming of persistent
plastic changes that may enhance future processing, and
the planning of actions in response to incoming auditory
information. Auditory attention is dynamic and flexible,
modulates many levels of auditory processing from association cortex to cochlea, and may rely upon adaptive
mechanisms that rapidly reshape receptive fields in
accord with current task demands and behavioral context.
Many outstanding questions remain to be answered by
future research. We still do not know the synaptic mechanisms and cellular architecture [211] underlying auditory
attention, nor the manner in which attentional effects at
multiple levels in the distributed attentional system are
orchestrated and directed. How much of the acoustic
novelty system can be explained by simple habituation
mechanisms? How are learned ‘bottom-up’ salience filters
formed? (for highly meaningful and over-learned stimuli
such as one’s own name). Do attentional effects in the
auditory system increase with task-difficulty as they do in
the visual system? [19,20]. What are the differences and
similarities between visual and auditory attention? What
are the pathways for crossmodal and intermodal attention? What is the interaction between the neural systems
for arousal, vigilance, and attention? [212]. What is the
relationship between attention and its close companions — expectation, reward, short-term memory, and
www.sciencedirect.com
Auditory attention — focusing the searchlight on sound Fritz et al. 449
plasticity? [5,136,213]. How does top-down auditory
attention modulate acoustic scene analysis, interact with
the ‘pre-attentive’ acoustic novelty detection system and
also with bottom-up ‘pop-out’ auditory attention? This
fascinating array of questions will keep neuroscientists
interested in auditory attention quite busy for years to
come.
Acknowledgement
We gratefully acknowledge funding from NIH R01 DC005779.
References and recommended reading
Some articles have been marked as worthy of special interest. All
papers in this subjective category are recent (publication within the last
five years) and relevant (results making an important contribution to the
field of auditory attention).
of special interest
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which subjects simultaneously heard novel melodies and viewed geometric shapes, and in different conditions, were instructed to attend to
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time (bimodal divided attention). Bimodal selective attention lead to
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in irrelevant sensory cortex. Thus top-down attentional effects modulate
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