Article

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

ABSTRACT 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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    • "According to anatomical data obtained in animal studies, the former is considered the major input system of the amygdala, receiving inputs from various sensory systems (Amaral et al., 1992; LeDoux, 1996), whereas the latter is considered a major output system of the amygdala, communicating with cortical systems through its connections with various neuromodulatory systems, such as the basal forebrain (Kapp et al., 1994; Jolkkonen et al., 2002). Despite the limited spatial resolution of fMRI, a similar anatomical distinction within the amygdala has been observed in a number of recent human fMRI studies, including those with resolution levels (i.e. 3 Â 3 Â 3 mm 3 voxel size) that are routinely employed by numerous neuroimaging laboratories (Morris et al., 2001; Whalen et al., 2001; Kim et al., 2003; Davis et al., 2010; Gamer et al., 2010; Bach et al., 2011). Furthermore, the regional differences within the amygdala that were observed in this study nicely corresponded to the known anatomy of the human amygdala, as well as to a recent theoretical framework about the functional dissociation between the amygdala subregions, which argues that the amygdala, particularly its dorsal subregion, is a key structure in detecting and resolving predictive uncertainty in an emotional context (Whalen et al., 2001; Kim et al., 2003). "
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    • "Given our previous demonstrations of amygdala responses to ambiguous facial expressions during passive viewing (Davis et al., 2010; Whalen et al., 2009; Kim et al., 2003 "
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