Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex

Fadila Hadj-Bouziane, Ning Liu, Andrew H. Bell, Katalin M Gothard, Wen Ming Luh, Roger B H Tootell, Elisabeth A. Murray, Leslie G. Ungerleider

Research output: Contribution to journalArticle

54 Citations (Scopus)

Abstract

We previously showed that facial expressions modulate functional MRI activity in the face-processing regions of the macaque monkey's amygdala and inferior temporal (IT) cortex. Specifically, we showed that faces expressing emotion yield greater activation than neutral faces; we term this difference the "valence effect." We hypothesized that amygdala lesions would disrupt the valence effect by eliminating the modulatory feedback from the amygdala to the IT cortex. We compared the valence effects within the IT cortex in monkeys with excitotoxic amygdala lesions (n = 3) with those in intact control animals (n = 3) using contrast agent-based functional MRI at 3 T. Images of four distinct monkey facial expressions - neutral, aggressive (open mouth threat), fearful (fear grin), and appeasing (lip smack) - were presented to the subjects in a blocked design. Our results showed that in monkeys with amygdala lesions the valence effects were strongly disrupted within the IT cortex, whereas face responsivity (neutral faces > scrambled faces) and face selectivity (neutral faces > non-face objects) were unaffected. Furthermore, sparing of the anterior amygdala led to intact valence effects in the anterior IT cortex (which included the anterior face-selective regions), whereas sparing of the posterior amygdala led to intact valence effects in the posterior IT cortex (which included the posterior face-selective regions). Overall, our data demonstrate that the feedback projections from the amygdala to the IT cortex mediate the valence effect found there. Moreover, these modulatory effects are consistent with an anterior-to-posterior gradient of projections, as suggested by classical tracer studies.

Original languageEnglish (US)
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number52
DOIs
StatePublished - Dec 26 2012

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Facial Expression
Temporal Lobe
Amygdala
Haplorhini
Magnetic Resonance Imaging
Macaca
Lip
Contrast Media
Fear
Mouth
Emotions

Keywords

  • Neuroimaging
  • Nonhuman primate
  • Social stimuli
  • Temporal lobe

ASJC Scopus subject areas

  • General

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Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex. / Hadj-Bouziane, Fadila; Liu, Ning; Bell, Andrew H.; Gothard, Katalin M; Luh, Wen Ming; Tootell, Roger B H; Murray, Elisabeth A.; Ungerleider, Leslie G.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 52, 26.12.2012.

Research output: Contribution to journalArticle

Hadj-Bouziane, Fadila ; Liu, Ning ; Bell, Andrew H. ; Gothard, Katalin M ; Luh, Wen Ming ; Tootell, Roger B H ; Murray, Elisabeth A. ; Ungerleider, Leslie G. / Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex. In: Proceedings of the National Academy of Sciences of the United States of America. 2012 ; Vol. 109, No. 52.
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