Functional Anatomy of Face Processing in the Primate Brain

National Institute Of Mental Health

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Abstract

Lesions of the inferior temporal (IT) cortex in humans can result in the clinical syndrome termed prosopagnosia, an inability to recognize familiar faces. Single-cell recordings from the IT cortex of monkeys have revealed the existence of neurons that are selectively activated by visual images of faces. More recently, brain imaging studies in both humans and monkeys have demonstrated face-selective regions, in which the fMRI signal evoked by faces is greatly enhanced compared to that evoked by other object categories, such as non-face objects and places. However, relatively little is known about the individual neuronal responses within versus outside these fMRI-defined regions. In one study, we examined the relationship between fMRI-identified face-selective regions in the IT cortex of monkeys, relative to the selectivity of single neurons and local field potentials (LFPs), located within vs. outside these regions. We confirmed that face-preferring neurons were most concentrated in areas corresponding to the fMRI-identified face-selective regions. However, we also found such face-preferring neurons outside of the fMRI-defined regions, at decreased concentrations. These two populations differed qualitatively: neurons located within the fMRI-defined face patches showed greater selectivity to faces, compared to those located outside these regions. Thus, fMRI-identified face-selective regions correspond to a high proportion of face-responsive neurons that are highly selective for faces. These findings help to clarify the relationship between fMRI-defined regions and the neuronal processes within them. Although face-selective regions have been reported in temporal and prefrontal cortex of both human and monkey subjects, the neural circuitry underlying face selectivity remains unclear. To clarify this, we studied the functional connectivity, which has been demonstrated to be an efficient method for revealing neural circuits, among these face-selective regions in rhesus monkeys in the resting, awake state. First, we mapped the face-selective regions by contrasting fMRI activation to images of monkey faces versus non-face objects. Two face-selective regions in the inferior temporal cortex were typically found in each hemisphere: the anterior and posterior face patches. Then, the animals underwent ten minutes of resting-state scans. Resting-state average time courses from the anterior and posterior face patches of each hemisphere were used as a seed for functional connectivity analyses. We found that a seed placed in the posterior face patch of one hemisphere correlated with activity in the posterior face patch of the other hemisphere and in the anterior patch, prefrontal face-selective areas and the amygdala of both hemispheres. A seed placed in the anterior face patch showed similar functional connectivity, but with different connectional strengths: stronger in the amygdala and weaker in the prefrontal face-selective areas. These results demonstrate that there is a functional network among the face-selective regions, which can be detected by studying the intrinsic, spontaneous fMRI signal fluctuations. Moreover, the functional connectivity appears to reflect the underlying neuroanatomy. We had previously shown that facial expressions modulate fMRI activity in face-responsive regions of the monkeys amygdala and visual cortex. Specifically, facial expressions of emotion yield greater activation than neutral faces, a phenomenon known as the valence effect. We next tested the idea that amygdala lesions would eliminate emotional modulatory feedback to the visual cortex, thus disrupting valence effects seen there. We performed selective amygdala lesions in monkeys and then used fMRI to compare the valence effects within the visual cortex in these animals to the effects in normal control animals. Four different facial expressions were tested: neutral, aggressive (open mouth threat), fearful (fear grimace) and appeasing (lipsmack). In controls, faces with emotional expressions relative to neutral faces produced enhanced responses in face-selective regions, as expected. Fear grimace expressions consistently elicited the greatest responses. In monkeys with amygdala lesions, the valence effects within the visual cortex were greatly disrupted. The most striking demonstration of this disruption was found in the hemisphere with the most complete amygdala lesion. In this hemisphere, although face-selective patches were found in IT cortex, their activity was not modulated by facial expressions. Conversely, in three hemispheres with spared tissue in the anterior part of the amygdala (which was activated by neutral faces and modulated by facial expressions), the valence effects in the face-selective patches of IT cortex were present. Just as in controls, in these hemispheres with anterior amygdala sparing, fear grimace expressions evoked the greatest response. Overall, our data demonstrate that the amygdala is the source of the valence modulatory effects seen in the visual cortex. These results make a significant contribution to our understanding of the neural processing of facial stimuli with emotional content.