Functional Anatomy of Face Processing in the Primate Brain

National Institute Of Mental Health

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Abstract

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. Multi-voxel pattern analysis of fMRI signals together with machine learning methods revealed that the classification of emotional facial expression and facial identity occurs in different neural substrates of the human brain: the amygdala and posterior superior temporal sulcus (STS) for the former and the fusiform face area and anterior inferior temporal cortex for the latter. 3. Thetaburst transcranial magnetic stimulation (TBS), which temporarily disrupts neural activity, delivered over the posterior 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. 4. 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. 5. Pharmacological inactivation combined with fMRI in monkeys demonstrated that the functional network among the face-processing regions is hierarchically organized: activation of the amygdala by faces depends on inputs from the anterior temporal lobe face regions, whereas activation of these anterior regions depends on inputs from more posterior temporal lobe face regions. 6. Detection of configural face differences by humans led to stronger activation relative to featural face differences in the posterior parietal cortex (PPC), and transcranial magnetic stimulation centered on PPC impaired their performance on configural but not featural difference detections, indicating that spatial mechanisms within the PPC are necessary for configural face processing and, more broadly, for veridical face perception. 7. Patients with Moebius syndrome, 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. The pattern of eye movements in monkeys reveals 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.