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

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 cond...

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Main Authors: Juri Minxha, Clayton Mosher, Jeremiah K. Morrow, Adam N. Mamelak, Ralph Adolphs, Katalin M. Gothard, Ueli Rutishauser
Format: Article
Language:English
Published: Elsevier 2017-01-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124716318058
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spelling doaj-e419383393d0400589b97b77c77ab3312020-11-24T21:47:22ZengElsevierCell Reports2211-12472017-01-0118487889110.1016/j.celrep.2016.12.083Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque AmygdalaJuri Minxha0Clayton Mosher1Jeremiah K. Morrow2Adam N. Mamelak3Ralph Adolphs4Katalin M. Gothard5Ueli Rutishauser6Computation and Neural Systems Program, California Institute of Technology, Pasadena, CA 90025, USADepartment of Physiology, College of Medicine, University of Arizona, Tucson, AZ 85724, USADepartment of Physiology, College of Medicine, University of Arizona, Tucson, AZ 85724, USADepartment of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USAComputation and Neural Systems Program, California Institute of Technology, Pasadena, CA 90025, USADepartment of Physiology, College of Medicine, University of Arizona, Tucson, AZ 85724, USADepartment of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USANeurons 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.http://www.sciencedirect.com/science/article/pii/S2211124716318058amygdalahuman single neuronface cellsinterspecies comparisonvisual tuninglatencyattention
collection DOAJ
language English
format Article
sources DOAJ
author Juri Minxha
Clayton Mosher
Jeremiah K. Morrow
Adam N. Mamelak
Ralph Adolphs
Katalin M. Gothard
Ueli Rutishauser
spellingShingle Juri Minxha
Clayton Mosher
Jeremiah K. Morrow
Adam N. Mamelak
Ralph Adolphs
Katalin M. Gothard
Ueli Rutishauser
Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
Cell Reports
amygdala
human single neuron
face cells
interspecies comparison
visual tuning
latency
attention
author_facet Juri Minxha
Clayton Mosher
Jeremiah K. Morrow
Adam N. Mamelak
Ralph Adolphs
Katalin M. Gothard
Ueli Rutishauser
author_sort Juri Minxha
title Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
title_short Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
title_full Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
title_fullStr Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
title_full_unstemmed Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
title_sort fixations gate species-specific responses to free viewing of faces in the human and macaque amygdala
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2017-01-01
description 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.
topic amygdala
human single neuron
face cells
interspecies comparison
visual tuning
latency
attention
url http://www.sciencedirect.com/science/article/pii/S2211124716318058
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