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. 2012 Dec 26;109(52):E3640-8.
doi: 10.1073/pnas.1218406109. Epub 2012 Nov 26.

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

Fadila Hadj-Bouziane  1 , Ning Liu, Andrew H Bell, Katalin M Gothard, Wen-Ming Luh, Roger B H Tootell, Elisabeth A Murray, Leslie G Ungerleider
Affiliations

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

Fadila Hadj-Bouziane et al. Proc Natl Acad Sci U S A. .

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.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Responses to neutral and emotional faces in the control animals. (A) Examples of monkey facial-expression stimuli used in the experiments. Animals were presented with 32-s–long blocks of various facial expressions consisting of exemplars of monkey faces (eight different identities). (B) Face-responsive (neutral faces > scrambled faces) regions (yellow) and face-selective (neutral faces > non-face objects) regions (red) are shown on inflated cortical surfaces for monkey K. as, arcuate sulcus; ls, lateral sulcus; ps, principal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus. (C) Profile of responses to the various facial expressions (N, neutral; T, threat; F, fear grin; L, lip smack) within the anterior and posterior face-selective regions for the three control animals. As shown previously (16), facial expressions modulated face-related activations within the temporal cortical face-selective regions. Asterisks on histograms indicate a significant difference from neutral (P < 0.05).
Fig. 2.
Fig. 2.
Face-responsive regions in the amygdala illustrated on a coronal section for monkey K and profiles of responses to the various facial expressions for the three control animals. Asterisks on histograms indicate a significant difference from neutral (P < 0.05). N, neutral; T, threat; F, fear grin; L, lip smack.
Fig. 3.
Fig. 3.
The extent of amygdala lesions along the anterior-to-posterior axis is shown on coronal sections for the three operated animals. The orange outlines represent the estimated amount of sparing within each hemisphere based on the examination of MR scans performed postsurgery and used to calculate the volume of the spared tissue (also see Table 1 for the extent of spared amygdala tissue expressed as a function of the mean amygdala volume in controls). For illustrative purposes, we have reproduced the outlines using a heavier line weight. On the left are images of Nissl-stained histological sections through the monkey amygdala, along the anterior-to-posterior axis [+23 mm to +15 mm, according to a standard monkey brain atlas (31)]. In monkeys C and P, the lesions were bilateral, as intended. In monkey P, the lesions were symmetrical; in monkey C, there was bilateral sparing in the anterior portion of the amygdala (AP ≥ +19 mm) but unilateral sparing in the posterior portion of the amygdala (AP < +19 mm) in the right hemisphere only. In contrast, in monkey M, the left hemisphere was left intact, but in the right hemisphere only the posterior portion of the amygdala (AP < +19 mm) was spared. amts, anterior middle temporal sulcus; rs, rhinal sulcus; sts, superior temporal sulcus.
Fig. 4.
Fig. 4.
Face-responsive regions within the spared amygdala tissue in three operated animals. (A) Coronal sections illustrating face responses (neutral faces > scrambled faces) through the anterior (AP ≥ +19 mm) and posterior amygdala (AP < +19 mm). In monkey C, we found face responses bilaterally within the anterior portion of the amygdala but in only the right of the posterior portion of the amygdala. In monkey P, we found face responses bilaterally within both the anterior and posterior portions of the amygdala. In contrast, in monkey M, we found face responses bilaterally within the posterior portion of the amygdala but in only the left of the anterior amygdala. (B) Profiles of responses to the various facial expressions within the right and left spared amygdala tissue in the three operated animals. In the spared amygdala tissue of the three animals, fearful faces consistently elicited significantly greater activation than neutral faces, as indicated by asterisks (P < 0.05). ANT, anterior; POST, posterior; N, neutral; T, threat; F, fear grin; L, lip smack.
Fig. 5.
Fig. 5.
Face-responsive (neutral faces > scrambled faces) regions (yellow) and face-selective (neutral faces > non-face) regions (red) in the animals with amygdala lesions, illustrated on inflated cortical surfaces. As in control animals, face-responsive regions were distributed mainly along the temporal cortex. We identified two bilateral face-selective regions (black circles) within the IT cortex in the three animals with amygdala lesions.
Fig. 6.
Fig. 6.
Profile of responses to the various facial expressions in the anterior and posterior face-selective regions of the IT cortex in the right and left hemispheres of the three operated animals. These data indicate that the amygdala’s influence on the responses within the IT cortex follows an anterior-to-posterior gradient. N, neutral; T, threat; F, fear grin, L, lip smack.
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