Lesions of inferior temporal (IT) cortex in humans can result in the syndrome termed prosopagnosia, an inability to recognize familiar faces. Single-cell recordings from IT cortex of monkeys have revealed the existence of neurons that are selectively activated by visual images of faces. Additionally, functional magnetic resonance imaging (fMRI) of both human and monkey brains has demonstrated face-selective regions, in which the fMRI signal evoked by faces is greater compared to that evoked by non-face objects. Together, these studies point to specialized neural machinery in the primate brain for processing faces. Thus far, our group and others have shown that the neural circuitry for face processing consists of a network of brain regions in the temporal and prefrontal cortex as well as in the amygdala. During the past year, we have made a number of important discoveries regarding the neural mechanisms mediating face processing: 1. Electrical stimulation of the amygdala led to stronger fMRI activation in face- than object-selective regions in the monkey temporal lobe, indicating that cortical face processing is strongly modulated by feedback from the amygdala, which likely conveys the emotion signaled by anothers expression and focuses the viewers attention on diagnostic facial features. 2. The pattern of eye movements in monkeys revealed that, like humans, they experience face pareidolia, the experience of perceiving faces on inanimate objects, indicating that this illusion is driven by a broadly-tuned face detection mechanism that we share with other species. 3. Monkeys with bilateral amygdala lesions, unlike normal monkeys, showed no preference for viewing faces or illusory faces, indicating that the amygdala is critical for our earliest specialized response to faces, a behavior thought to be a precursor for efficient social communication. 4. Thetaburst transcranial magnetic stimulation (TBS), which temporarily disrupts neural activity, delivered over the posterior superior temporal sulcus (STS) reduced the neural response to dynamic faces (but not to bodies or objects) in the posterior STS, anterior STS and amygdala, compared to TBS delivered over the vertex, indicating a cortico-amygdala pathway via the STS for dynamic face perception in humans. 5. Intranasal administration of oxytocin, a neuropeptide and potential treatment for autism, selectively altered fMRI responses to emotional expressions in monkeys, significantly reducing responses to both fearful and aggressive faces in face-responsive regions while leaving responses to appeasing and neutral faces unchanged, thereby explaining the beneficial effects of oxytocin on social cognition. 6. TBS applied on dorsal locationprocessing regions in humansreduced fMRI activity within ventral stream face-processing regions during configural but not featural face processing, indicating that ventral stream face-processing regions receive visuospatial information from dorsal stream location-processing regions during configural face processing. 7. Patients with Moebius syndrome (MoS), a rare genetic neurological disorder characterized by facial paralysis, showed an impairment in their ability to recognize emotional expressions in others, indicating that the perception of emotional expressions depends on the ability to produce those expressions oneself. 8. Resting-state fMRI showed reduced posterior STS-amygdala connectivity relative to fusiform face area-amygdala connectivity in MoS compared to healthy controls, suggesting that the neurocircuitry underlying emotion processing may be altered in MoS. 9. Several curvature-selective regions of the posterior cerebral cortex were identified in humans that overlapped face-selective regions, suggesting that face selectivity might arise from curvature selectivity.

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10
Fiscal Year
2018
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U.S. National Institute of Mental Health
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