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Cell Rep. 2017 Jan 24;18(4):878-891. doi: 10.1016/j.celrep.2016.12.083.

Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala.

Author information

1
Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA 90025, USA.
2
Department of Physiology, College of Medicine, University of Arizona, Tucson, AZ 85724, USA.
3
Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.
4
Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA 90025, USA; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 90025, USA; Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA 90025, USA.
5
Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 90025, USA; Department of Neurology, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA. Electronic address: ueli.rutishauser@cshs.org.

Abstract

Neurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing.

KEYWORDS:

amygdala; attention; face cells; human single neuron; interspecies comparison; latency; visual tuning

PMID:
28122239
PMCID:
PMC5283067
DOI:
10.1016/j.celrep.2016.12.083
[Indexed for MEDLINE]
Free PMC Article

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