Humans and monkeys use eye movements to explore their world and identify, in their visual environment, the emotionally and socially important elements. The success of non-verbal social communication with facial expressions, gestures, and postures depends critically on the fast and correct evaluation of the signals displayed by others. The sequence of saccades and fixations executed by the eyes of monkeys and humans during the visual exploration of facial expressions (scanpaths) are influenced by two processes: bottom-up visual processes which allocate visual attention to salient elements of the image (e.g., the eyes), and top-down processes that reflect goals, expertise, and momentary emotional states. The majority of psychiatric disorders are accompanied by aberrant scanpaths, yet the source of the deficit is poorly understood. The observation that patients with amygdala damage fail to explore the eyes and show scanpath abnormalities similar to patients with autism, schizophrenia, social phobia, and affective disorders, suggests that the amygdala is involved in guiding visual attention during face exploration. The precise contribution of the amygdala to this process is unknown. The amygdala is a complex of two main nuclear groups with dissociable functions and we propose that different nuclear groups are involved in the bottom-up and top-down components of scanpath elaboration. The resources afforded by this application will be used to selectively inactivate the centromedial and basolateral nuclear groups of the monkey amygdala and determine the contribution of the each nuclear group to bottom-up and top-down processes of face exploration. The results are expected to clarify the contribution of the amygdala to the acquisition of socially and emotionally relevant information-a critical prerequisite in designing a more effective intervention in socio-emotional disorders.

Public Health Relevance

The goal of this application is to determine the role of the primate amygdala in allocating visual attention to visual targets of enhanced emotional and social significance. The proposal is centered on the hypothesis that the pattern of eye movements during the visual exploration of faces depends on both top-down and bottom-up processes and that these processes can be localized to different groups of amygdaloid nuclei. The centromedial group of nuclei, reciprocally connected to reflexive and autonomic centers in the brain-stem, are hypothesized for form a circuit that contributes to bottom-up control of eye movements. In contrast, the basolateral nuclear complex, functionally connected to high-level cortical visual areas, is expected to provide top-down control of eye movements. To test these hypotheses, we will use reversible inactivation to separately manipulate the two components of the amygdalar complex, and measure the alterations in visually-guided saccades and in the exploration of images of facial expressions. This project reflects a novel integrative approach using a combination of reversible inactivation with electrophysiology under electrophysiological control, which affords causal inference between neural activity and behavior, and scanpath monitoring, which reveals untrained behavioral responses to naturalistic stimuli. The outcome will dissociate the role of two amygdaloid components within the circuit that guides eye movements, clarifying two potentially clinically relevant functions of the amygdala.

National Institute of Health (NIH)
National Institute of Mental Health (NIMH)
Exploratory/Developmental Grants (R21)
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Cognitive Neuroscience Study Section (COG)
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Simmons, Janine M
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University of Arizona
Schools of Medicine
United States
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Minxha, Juri; Mosher, Clayton; Morrow, Jeremiah K et al. (2017) Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala. Cell Rep 18:878-891
Ballesta, S├ębastien; Mosher, Clayton P; Szep, Jeno et al. (2016) Social determinants of eyeblinks in adult male macaques. Sci Rep 6:38686
Mosher, Clayton P; Zimmerman, Prisca E; Gothard, Katalin M (2014) Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Curr Biol 24:2459-64