Regional Response Differences Across the Human Amygdaloid Complex during Social Conditioning

Department of Psychological & Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755, USA.
Cerebral Cortex (Impact Factor: 8.67). 07/2009; 20(3):612-21. DOI: 10.1093/cercor/bhp126
Source: PubMed


The amygdala is consistently implicated in biologically relevant learning tasks such as Pavlovian conditioning. In humans, the ability to identify individual faces based on the social outcomes they have predicted in the past constitutes a critical form of associative learning that can be likened to "social conditioning." To capture such learning in a laboratory setting, participants learned about faces that predicted negative, positive, or neutral social outcomes. Participants reported liking or disliking the faces in accordance with their learned social value. During acquisition, we observed differential functional magnetic resonance imaging activation across the human amygdaloid complex consistent with previous lesion, electrophysiological, and functional neuroimaging data. A region of the medial ventral amygdala and a region of the dorsal amygdala/substantia innominata showed signal increases to both Negative and Positive faces, whereas a lateral ventral region displayed a linear representation of the valence of faces such that Negative > Positive > Neutral. This lateral ventral locus also differed from the dorsal and medial loci in that the magnitude of these responses was more resistant to habituation. These findings document a role for the human amygdala in social learning and reveal coarse regional dissociations in amygdala activity that are consistent with previous human and nonhuman animal data.

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Article: Regional Response Differences Across the Human Amygdaloid Complex during Social Conditioning

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    • "As a consequence, it remains unclear whether socially anxious individuals react more sensitive to socially relevant stimuli. So far, there is only little research investigating the neural correlates of social conditioning, which is the associative process whereby humans learn to identify individuals that have predicted threats or rewards in the past (Davis et al., 2010). Davis examined social learning with neutral faces and written verbal feedback and reported increased amygdala activation in response to faces paired with negative and positive comments . "
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    ABSTRACT: In search of causative factors of social anxiety disorder (SAD), classical conditioning has been discussed as a potential trigger mechanism for many years. Recent findings suggest that the social relevance of the unconditioned stimulus (US) might play a major role in learning theories of SAD. Thus, this study applied a social conditioning paradigm with disorder-relevant US to examine the electrocortical correlates of affective learning. Twenty-four high socially anxious (HSA) and 23 age- and gender-matched low socially anxious (LSA) subjects were conditioned to 3 different faces flickering at a frequency of 15 Hz which were paired with auditory insults, compliments or neutral comments (US). The face-evoked electrocortical response was measured via steady-state visually evoked potentials and subjective measures of valence and arousal were obtained. Results revealed a significant interaction of social anxiety and conditioning, with LSA showing highest cortical activity to faces paired with insults and lowest activity to faces paired with compliments, while HSA did not differentiate between faces. No group differences were discovered in the affective ratings. The findings indicate a potentially impaired ability of HSA to discriminate between relevant and irrelevant social stimuli, which may constitute a perpetuating factor of SAD.
    Social Cognitive and Affective Neuroscience 10/2014; 10(7). DOI:10.1093/scan/nsu140 · 7.37 Impact Factor
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    • "Most likely, this short-term plasticity related to the individual learning history is due to re-entrant modulations of visual areas both by sub-cortical areas such as the amygdala as well as top-down influences of the fronto-parietal attention network. This corroborates findings which demonstrated that the amygdala shows elevated responses to socially conditioned stimuli [13], [14], [16]. Findings of conditioned responses in the lateral amygdala [46] and thalamus [47] preceding those that are observed in the primary sensory cortices support the notion that subcortical centers are necessary for the induction of sustained fear-related plasticity in the cortex. "
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    ABSTRACT: Humans form impressions of others by associating persons (faces) with negative or positive social outcomes. This learning process has been referred to as social conditioning. In everyday life, affective nonverbal gestures may constitute important social signals cueing threat or safety, which therefore may support aforementioned learning processes. In conventional aversive conditioning, studies using electroencephalography to investigate visuocortical processing of visual stimuli paired with danger cues such as aversive noise have demonstrated facilitated processing and enhanced sensory gain in visual cortex. The present study aimed at extending this line of research to the field of social conditioning by pairing neutral face stimuli with affective nonverbal gestures. To this end, electro-cortical processing of faces serving as different conditioned stimuli was investigated in a differential social conditioning paradigm. Behavioral ratings and visually evoked steady-state potentials (ssVEP) were recorded in twenty healthy human participants, who underwent a differential conditioning procedure in which three neutral faces were paired with pictures of negative (raised middle finger), neutral (pointing), or positive (thumbs-up) gestures. As expected, faces associated with the aversive hand gesture (raised middle finger) elicited larger ssVEP amplitudes during conditioning. Moreover, theses faces were rated as to be more arousing and unpleasant. These results suggest that cortical engagement in response to faces aversively conditioned with nonverbal gestures is facilitated in order to establish persistent vigilance for social threat-related cues. This form of social conditioning allows to establish a predictive relationship between social stimuli and motivationally relevant outcomes.
    PLoS ONE 07/2014; 9(7):e102937. DOI:10.1371/journal.pone.0102937 · 3.23 Impact Factor
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    • "The discrepancies among these findings might reflect the insufficient resolution of conventional fMRI for investigations of the human amygdaloid complex. In fact, recent studies have sought to dissociate the different functional subregions of the amygdala through the use of high-resolution fMRI (Davis et al., 2010;Gamer et al., 2010). Our findings from the current study indicating that the amygdala is preferentially involved in processing valence rather than arousal are consistent with the results of these recent studies, which have demonstrated greater activity in the lateral subregion of the amygdala in response to unpleasant faces than in response to pleasant faces (Davis et al., 2010;Gamer et al., 2010). "
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    ABSTRACT: OUR UNDERSTANDING OF FACIAL EMOTION PERCEPTION HAS BEEN DOMINATED BY TWO SEEMINGLY OPPOSING THEORIES: the categorical and dimensional theories. However, we have recently demonstrated that hybrid processing involving both categorical and dimensional perception can be induced in an implicit manner (Fujimura etal., 2012). The underlying neural mechanisms of this hybrid processing remain unknown. In this study, we tested the hypothesis that separate neural loci might intrinsically encode categorical and dimensional processing functions that serve as a basis for hybrid processing. We used functional magnetic resonance imaging to measure neural correlates while subjects passively viewed emotional faces and performed tasks that were unrelated to facial emotion processing. Activity in the right fusiform face area (FFA) increased in response to psychologically obvious emotions and decreased in response to ambiguous expressions, demonstrating the role of the FFA in categorical processing. The amygdala, insula and medial prefrontal cortex exhibited evidence of dimensional (linear) processing that correlated with physical changes in the emotional face stimuli. The occipital face area and superior temporal sulcus did not respond to these changes in the presented stimuli. Our results indicated that distinct neural loci process the physical and psychological aspects of facial emotion perception in a region-specific and implicit manner.
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