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Distant influences of amygdala lesion on visual cortical activation during emotional face processing

Abstract

Emotional visual stimuli evoke enhanced responses in the visual cortex. To test whether this reflects modulatory influences from the amygdala on sensory processing, we used event-related functional magnetic resonance imaging (fMRI) in human patients with medial temporal lobe sclerosis. Twenty-six patients with lesions in the amygdala, the hippocampus or both, plus 13 matched healthy controls, were shown pictures of fearful or neutral faces in task-releant or task-irrelevant positions on the display. All subjects showed increased fusiform cortex activation when the faces were in task-relevant positions. Both healthy individuals and those with hippocampal damage showed increased activation in the fusiform and occipital cortex when they were shown fearful faces, but this was not the case for individuals with damage to the amygdala, even though visual areas were structurally intact. The distant influence of the amygdala was also evidenced by the parametric relationship between amygdala damage and the level of emotional activation in the fusiform cortex. Our data show that combining the fMRI and lesion approaches can help reveal the source of functional modulatory influences between distant but interconnected brain regions.

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Figure 1: Sample visual stimuli.
Figure 2: Activation by attention and emotion.
Figure 3: SPMs of emotion × group interaction (threshold P < 0.01 for illustration).
Figure 4: SPM parametric analysis.

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Acknowledgements

Thanks to the patients and their families for participating; to clinicians at the Department of Clinical and Experimental Epilepsy (J. Duncan, L. Sander, M. Walker, H. Cock, S. Sisodiya and M. Koepp) for referring the patients; to P. Bartlett, chief radiographer at the Chalfont Centre for Epilepsy, for providing MRI volume and T2 data; and to P. Rotshtein and J. Winston for providing data from their behavioral testing of the patients. Supported by a Swiss National Science Foundation grant (P.V.), a Fellowship of the Medical Research Council (MPR), a Royal Society-Wolfson Research Merit Award (J.D.) and Wellcome Trust Programme Grants (R.J.D and J.D.).

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Correspondence to Patrik Vuilleumier.

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Supplementary information

Supplementary Fig. 1

Main effect of facial expression (fearful minus neutral faces, irrespective of spatial attention). (Upper row) Right amygdala activation overlaid on the mean anatomical scan for each group separately: N = normal controls; H = patients with hippocampal damage only; AH = patients with both amygdala and hippocampus damage. (Lower row) Parameter estimates of activity in right amygdala across all stimulus conditions, for each group, showing increased responses to fearful faces both when these appeared at task-relevant locations and when they appeared at task-irrelevant locations. This pattern corroborates our previous findings in a different group of healthy participants in the same paradigm11. See table 2 for coordinates and statistical data.. (PDF 231 kb)

Supplementary Fig. 2

Correlations between T2 sclerosis intensity in amygdala and magnitude of emotional activation (fearful minus neutral faces). Such correlations are shown for different regions in the ipsilateral or contralateral hemisphere, across the 26 patients (from AH and H groups). As for the left amygdala and left fusiform shown in Figure 4D of main paper, there was a reliable inverse relationship between (a) left amygdala and left occipital cortex when faces were either task-relevant or task-irrelevant (R = –0.48 and –0.36, respectively) but not between (b) right amygdala and left fusiform (R = 0.12 and 0.11). Similarly, there was no correlation between (c) right fusiform increases and left amygdala sclerosis (R = –0.18 and 0.02), but (d) a reliable negative correlation between right fusiform and right amygdala (R = –0.39 and –0.48). These data illustrate the consistently ipsilateral nature of functional relationships between structural amygdala integrity and functional modulation of visual responses to emotional faces, irrespective of task-relevance. (PDF 148 kb)

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Vuilleumier, P., Richardson, M., Armony, J. et al. Distant influences of amygdala lesion on visual cortical activation during emotional face processing. Nat Neurosci 7, 1271–1278 (2004). https://doi.org/10.1038/nn1341

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