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Cerebral Cortex Advance Access published online on June 25, 2009

Cerebral Cortex, doi:10.1093/cercor/bhp126
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© The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Regional Response Differences Across the Human Amygdaloid Complex during Social Conditioning

F. Caroline Davis1, Tom Johnstone2, Emily C. Mazzulla3, Jonathan A. Oler4 and Paul J. Whalen1

1 Department of Psychological & Brain Sciences, Dartmouth College, Hanover, NH 03755, USA, 2 School of Psychology and Clinical Language Sciences, University of Reading, Earley Gate, Whiteknights, Reading RG6 6AL, UK, 3 Department of Psychology, University of Vermont, Burlington, VT 05405, USA, 4 Department of Psychiatry, University of Wisconsin-Madison, Madison, WI 53719, USA

Address correspondence to F. Caroline Davis, BA, Department of Psychological & Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755, USA. Email: Frances.C.Davis{at}dartmouth.edu.

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.

Key Words: arousal • dorsal amygdala • fMRI • habituation • valence • ventral amygdala


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