An Event-Related Examination of Neural Activity During Social Interactions
An Event-Related Examination of Neural Activity During Social Interactions
An Event-Related Examination of Neural Activity During Social Interactions
1093/scan/nss058
Social exclusion is known to cause alterations in neural activity and perceptions of social distress. However, previous research is largely limited to
examining social interactions as a unitary phenomenon without investigating adjustments in neural and attentional processes that occur during social
interactions. To address this limitation, we examined neural activity on a trial-by-trial basis during different social interactions. Our results show conflict
monitoring neural alarm activation, indexed by the N2, in response to specific exclusionary events; even during interactions that are inclusionary overall
and in the absence of self-reported feelings of social pain. Furthermore, we show enhanced attentional activation to exclusionary events, indexed by the
P3b, during exclusionary, compared with inclusionary, interactions, and this P3b activation was associated with self-reported social distress following
prolonged social exclusion. Finally, both the N2 and P3b showed larger amplitudes in the earlier stages of exclusion compared with later stages,
suggesting heightened early sensitivity for both components. Together, these findings provide novel insights into the dynamic neural and perceptual
processes of exclusion that exist during social interactions and the relationship between discrete events within interactions and the more general
contexts of the social interactions.
Keywords: social exclusion; event-related brain potentials (ERPs); N2; P3b; conflict monitoring
INTRODUCTION
Social exclusion gives rise to a diffuse pattern of behavioral and neural
changes that can lead to severe emotional, cognitive, social and
developmental impairments in targets of exclusion (Williams, 2001;
Baumeister et al., 2002; Eisenberger et al., 2003; Masten et al., 2009).
These effects include increases in aggressive social behavior, anxiety
and depression (MacDonald and Leary, 2005; Williams et al., 2005)
and decreases in self-esteem and the fulfillment of needs (Williams
et al., 2001). Additionally, different patterns of neural activation are
present during exclusion compared with inclusion, with enhanced
activation of the anterior cingulate cortex (ACC) and right ventral
prefrontal cortex (RVPFC) during exclusion (Eisenberger et al., 2003,
2007). In these studies, measures of neural activation were aggregated
within blocks of social interactions, which show the overall patterns of
activation for each type of interaction (i.e. inclusionary and exclusionary) but not the alterations in neural activation over the course of the
interactions. This allows for general characterizations of the relationship between neural activation and self-reported feelings following
exclusion but does not allow for the examination of adjustments
in neural processes during social interactions. To address this issue,
we conducted an event-related brain potential (ERP) study of social
exclusion. ERP measurement allows for the examination of specific
events within a larger social interaction due to the excellent temporal
resolution of ERPs compared with other neuroimaging techniques and
methodologies (e.g. functional magnetic resonance imaging; fMRI),
which are temporally limited to examinations of social interactions
at the level of the entire interaction. Therefore, we were able to examine specific patterns of neural activity in response to discrete events
during ongoing social interactions, including neural alarm activation
and related task-relevant attentional activations, within the larger contexts of different types of social interactions.
The Author (2012). Published by Oxford University Press. For Permissions, please email: journals.permissions@oup.com
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that is present throughout environmental interactions that can be positive or negative in nature or can be personally experienced or observed.
Alternatively, the regulation of conflict is a conscious process meant to
modify behavior to achieve desired outcomes through the implementation of cognitive control, which adjusts the activation of attentional
control networks to deal with the sources of the conflict or to cope
with the consequences of the behavior.
Therefore, conflict monitoring theory suggests that the ACC-based
neural alarm system, similar to the one activated during social exclusion (Eisenberger et al., 2003, 2007), is active in response to conflict
regardless of the behavioral or emotional outcomes and can be present
even before the outcome of an event or interaction is determined
(Botvinick et al., 2001; Yeung et al., 2004). Thus, any specific exclusionary event, even a brief moment of exclusion within the context of
a largely inclusionary interaction, should be sufficient to elicit neural
alarm activation, without leading to perceptions of exclusion and
corresponding self-reported feelings of social distress. Alternatively,
the conscious control and allocation of attention toward perceptions
of exclusion and exclusionary events would be more specifically
associated with negative feelings and reports of social pain.
J. R.Themanson et al.
(i.e. ERPs), may yield additional important information regarding
neural activation during social exclusion.
We suggest that the neural alarm is active in response to social pain
experienced following exclusion, consistent with the findings of
Eisenberger et al. (2003, 2007). However, we suggest that the neural
alarm is not exclusion specific but is a more sensitive and generic
conflict monitor that is also proactively sensitive to exclusionary
events similar to pain-inducing phenomena that may, or may not,
lead to complete exclusion. Further, we suggest that the enhanced
activation of the remaining self-regulatory neural circuitry following
exclusion, including the prefrontal cortex and related parietal attentional network regions, is more closely associated with self-reported
perceptions of exclusion and feelings of social distress.
Current study
To examine the dynamic relationships between neural and behavioral
indices of social exclusion, we conducted an ERP study that assessed
the responsiveness of neural alarm activity and other self-regulatory
attentional processes to exclusionary events within the larger contexts
of different social interactions. ACC-based neural alarm activation was
indexed by the N2 component of the stimulus-locked ERP, whereas
conscious cognitive control and attentional processes were indexed by
the P3b component. The N2 component is a multifaceted component
that has been linked to multiple cognitive processes (Folstein and Van
Petten, 2008). Recently, a differentiation in N2 functionality has
separated anterior N2s from posterior N2s, with anterior N2s related
with wither the detection of novelty and mismatch or with error/
conflict detection and cognitive control processes (Folstein and Van
Petten, 2008). In the current investigation, we will be examining the
influence of conflict derived from social interactions on the anterior
cognitive control N2. This conflict N2 is negative-going component
that is maximal over fronto-central recording sites, peaks between
150 and 350 ms after stimulus presentation and is believed to be a
psychophysiological index of conflict monitoring that originates
from the ACC (van Veen and Carter, 2002; Yeung et al., 2004;
Folstein and Van Petten, 2008). Scalp recordings of this component
reflect the detection of conflict that occurs without action errors or
error feedback, including conflict associated with the inhibition of
action (Braver et al., 2001) and conflict existing outside ones
awareness (Leuthold and Kopp, 1998) during correct task execution.
Thus, the conflict N2 reflects the activity of a pre-conscious conflict
monitoring system that can be activated before the execution of
unintended behavioral responses (Yeung et al., 2004). The P3b is
a consciousness-dependent ERP component that is sensitive to task
difficulty and the subjective probability of task stimuli or conditions
(Kok, 2001; Polich, 2007). The P3b is believed to reflect neuronal
activity involved with basic cognitive functions such as memory
updating and event categorization (Polich and Kok, 1995) and has
been theorized to index the allocation of attention to task-relevant
external stimuli (Donchin, 1981; Kok, 2001; Polich, 2007). The P3b
is a positive-going component that is maximal over parietal recording
sites and peaks between 300 and 800 ms after stimulus presentation.
The P3b has multiple neural generators, including frontal and parietal
activations (Polich, 2007). Therefore, in our investigation of the
conflict N2 and P3b, we examined conflict monitoring neural alarm
activation during the course of social interactions and activation
associated with ongoing alterations in attentional allocation. On the
basis of previous event-related research examining conflict monitoring
and cognitive control and studies detailing the neural correlates of
social exclusion, we hypothesized that: (i) neural alarm activation,
indexed by the conflict N2, would be present in response to any
event where the participant was excluded, regardless of the larger
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for data analysis. Every participant completed the same three blocks
of the Cyberball paradigm (inclusion, exclusion and re-inclusion),
completing the needs and feelings questionnaire and PANAS assessment before the first block and after each block. In each block, the
Cyberball game was set for 80 throws, with the computerized players
waiting between 2 and 3 s after receiving the ball to make a throw to
enhance the sense that the player was actually playing the game and
making a choice about which other player should receive the ball.
In the first block (inclusion), the participant had a 50% chance of
receiving the ball each throw. In the second block (exclusion), the
participant had the same 50% chance of receiving the ball until receiving a total of 10 throws from the other participants. Following this
initial inclusionary phase, the participant was no longer included in
any of the remaining approximately 50 throws in the block. The third
block (re-inclusion) returned the game to the original probability
parameters described for the inclusion block.
Event-related markers were created on a computer collecting ERP
data from the participants while they were engaged in the Cyberball
paradigm. The event markers were inserted at the first frame in each
ball toss where information was provided on which player was going to
be the recipient of the ball toss (i.e. throw to human participant and
throw to computerized player). The inclusion of these event markers
allowed for the quantification of moment-to-moment ERP activity in
response to inclusionary (throw to human participant) or exclusionary
(throw to computerized player) events that were present in the context
of larger interactions that were either generally inclusive or exclusive
for the participant overall (Figure 1).
Neuroelectric assessment
The electroencephalogram (EEG) was recorded from 64 sintered
AgAgCl electrodes with an average-ear reference and forehead
ground (AFz). Vertical and horizontal bipolar electrooculographic
activity was recorded to monitor eye movements. A Neuroscan
Synamps2 bioamplifier (Neuro Inc., El Paso, TX, USA) was used to
continuously digitize (500 Hz sampling rate) and low-pass filter
(30 Hz; 24 dB/octave) the raw EEG signal. Offline processing of the
stimulus-locked ERP included eye blink correction using a spatial
filter (Compumedics Neuroscan, 2003), creation of stimulus-locked
epochs (800 to 2500 ms relative to the event marker), baseline
removal (800 ms pre-stimulus interval) and artifact rejection (epochs
with signal that exceeded 75 mV were rejected). The N2 component
was quantified as the average amplitude in the discrete latency window
running from 200 to 320 ms after the event marker at FCz, whereas the
Fig. 1 Timing of ERP markers during throws in ongoing Cyberball game. Markers were inserted at the first informational frame providing information about the recipient of each throw. The remaining throw
frames displaying the completion of the throw are not displayed.
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J. R.Themanson et al.
Fig. 2 Participants self-reported feelings relating to each scale of the Positive and Negative Affect
Schedule (PANAS; A) and the Need-Threat Scale (NTS; B) during baseline and following each block of
the Cyberball paradigm (inclusion, exclusion and re-inclusion). Error bars represent standard errors in
both graphs. Note: Belong Need for Belonging; SE Need for self-esteem; Control Need for
Control; Meaning Need for Meaningful Existence; Mood Extent Feeling a Positive Mood and
Ignored Extent Feeling Ignored and Excluded.
both the N2 [F(1,21) 57.6, P < 0.001, partial 2 0.73] and P3b
[F(1,21) 111.9, P < 0.001, partial 2 0.84] revealed significant
effects of throw type, with larger N2 amplitude and smaller P3b amplitude for ETs [N2 M(SD) 0.3(1.7) V; P3b M(SD) 0.8(1.9) V]
compared with ITs [N2 M(SD) 3.1(2.0) V; P3b M(SD) 7.6(2.9)
V]. These findings indicate that the neural responses to conflict and
the related adaptations in attentional allocation were active during
each social interaction (inclusion, exclusion and re-inclusion) but
were sensitive to the specific momentary exclusionary events during
each of the social interactions rather than the larger overall contexts of
the social exchanges. Figure 3 provides ERP waveforms by Cyberball
block and throw type, highlighting the observed differences in N2
and P3b amplitudes.
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A
FCz
-4
N2
-4
731
FCz
N2
-2
Amplitude (V)
Amplitude (V)
-2
0
2
4
6
8
10
-200
200
400
4
First 20 Exclusionary Throws
Second 20 Exclusionary Throws
6
-200
600
800
200
400
600
800
600
800
Time (ms)
Time (ms)
B
B
-6
Pz
-2
-4
Amplitude (V)
-2
Amplitude (V)
-4
Pz
0
2
4
4
P3
6
8
6
-200
P3
10
-200
200
400
Time (ms)
200
400
600
800
Time (ms)
Fig. 3 Grand-averaged stimulus-locked ERP waveforms during Cyberball for the inclusion, exclusion
and re-inclusion blocks (solid, dotted and dashed lines, respectively) for inclusionary throws
(thick lines) and exclusionary throws (thin lines) at FCz (A) and Pz (B) electrode sites. Relative to
inclusionary throws, exclusionary throws are characterized by larger N2 amplitudes at FCz and smaller
P3b amplitudes at Pz. Additionally, P3b amplitude to exclusionary throws was larger during the
exclusion block compared with both the inclusion and re-inclusion blocks, with no differences present
in P3b amplitude across blocks for inclusionary throws.
Fig. 4 Larger N2 amplitude at FCz (A) and P3b amplitude at Pz (B) during the first 20 (thick
lines) versus second 20 (thin lines) complete-exclusion exclusionary throws during the exclusion
block.
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J. R.Themanson et al.
or strength of that activation resulting from negative feelings of social
distress. Instead, it seems that the association is due to the increased
frequency of conflict-based neural activations over repeated ETs during
exclusion compared with inclusion, which were aggregated over the
duration of the entire social interaction.
Moreover, our findings suggest the explicit awareness or perception
of being excluded and the related allocation of attention to the exclusionary experience, indexed by the P3b, may be more closely associated
with self-reported social distress outcomes of exclusion. Thus, in contrast to previous hypotheses (Eisenberger et al., 2003), our findings
indicate that reports of social pain would not be reported following
an implicit social exclusion condition (Eisenberger et al., 2003) even
though conflict-based ACC activation was present. Rather, in this
condition, we suggest that self-reported levels of social distress
would be similar to levels shown during an inclusion condition as
the participant would not develop explicit perceptions of being
excluded and would not display enhanced neural activations in parietal
attentional networks reflecting the conscious allocation of attention
toward being excluded.
These findings are consistent with the hypothesis that any event,
or string of events, that is powerful enough to warrant the perception
of exclusion and direct ones attention toward being excluded is
powerful enough to elicit the damaging cognitive and emotional consequences of exclusion. This is similar to how exclusion can work in
the real world (Williams, 2001), where one could be fully included for
an interaction or series of interactions, but one important exclusionary
moment or event can lead to devastating outcomes (Williams, 2001;
Baumeister et al., 2002; MacDonald and Leary, 2005; Williams et al.,
2005). Accordingly, perceptions of social exclusion and feelings of
social distress could result from almost any type of social interaction,
even those that are largely inclusionary, as long as conscious
self-regulatory control processes, and the related allocation of attention
toward the exclusionary events, are engaged.
With respect to alterations in neural activity over the course of
extended exclusionary events, these changes could reflect a decrease
in exclusion-related conflict and attentional allocation over time,
implying that the participants effectively became habituated or desensitized to the exclusionary experience over time (Rule et al., 2002;
Nieuwenhuis et al., 2003). Alternatively, the prolonged repetition
of exclusionary events could have depleted the neural alarm and
self-regulatory attentional systems, resulting in social cognitive deficits
similar to those hypothesized in cognitive deconstruction (Baumeister
et al., 2002), leaving targets of exclusion unable to properly respond to
being excluded from an interaction. On the basis of the present data,
we cannot determine which explanation is most likely as both could
potentially elicit the observed reductions in N2 and P3b amplitudes
over the course of exclusion.
Limitations and future directions
Although our analyses were able to determine the extent to which
patterns of neural activation were independently associated with
specific events during social interactions, it is important to note the
limitations of this study. The relatively small sample size, the severe
constraints used to create the exclusionary interaction and the poor
spatial resolution of ERPs limit the strength of the findings. Future
examinations should implement a broader array of exclusion manipulations and even combined multiple measures of neural activation
(fMRI and ERP) to more completely assess the relationships between
neural alarm activation, attentional allocation and self-reported social
distress during a variety of exclusionary social interactions. Further,
future studies examining more participants and their individual differences are warranted to investigate key variables that may moderate
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