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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    • "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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    • "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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    • "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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