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

Minxha, Juri and Mosher, Clayton and Morrow, Jeremiah K. and Mamelak, Adam N. and Adolphs, Ralph and Gothard, Katalin M. and Rutishauser, Ueli (2017) Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala. Cell Reports, 18 (4). pp. 878-891. ISSN 2211-1247. PMCID PMC5283067. https://resolver.caltech.edu/CaltechAUTHORS:20170126-154932370

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.celrep.2016.12.083DOIArticle
http://www.sciencedirect.com/science/article/pii/S2211124716318058PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5283067/PubMed CentralArticle
ORCID:
AuthorORCID
Mamelak, Adam N.0000-0002-4245-6431
Adolphs, Ralph0000-0002-8053-9692
Rutishauser, Ueli0000-0002-9207-7069
Additional Information:© 2016 The Author(s). This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Received 17 May 2016, Revised 5 October 2016, Accepted 22 December 2016, Available online 24 January 2017. We thank J. Kaminski, S. Sullivan, S. Wang, and P.E. Zimmerman for discussion, and the staff and physicians of the Epilepsy Monitoring Unit at Cedars-Sinai Medical Center for assistance. This work was supported by the National Science Foundation (1554105 to U.R.), the National Institute of Mental Health (P50 MH094258 to R.A., R21 MH086065 to K.M.G., P50 MH100023 to K.M.G., and R01 MH110831 to U.R.), the McKnight Endowment Fund for Neuroscience (to U.R.), and a NARSAD Young Investigator grant from the Brain & Behavior Research Foundation (23502 to U.R.). Author Contributions: Conceptualization, U.R., R.A., and K.M.G.; Investigation, J.M., C.M., J.K.M., U.R., A.N.M., and K.M.G.; Formal Analysis, J.M. and U.R.; Writing – Original Draft, U.R. and R.A.; Writing – Reviewing & Editing, J.M., U.R., R.A., K.M.G., and A.N.M., Supervision, R.A., K.M.G., and U.R.; Funding Acquisition, R.A., K.M.G., and U.R.
Funders:
Funding AgencyGrant Number
NSFBCS-1554105
NIHP50 MH094258
NIHR21 MH086065
NIHP50 MH100023
NIHR01 MH110831
McKnight Endowment Fund for NeuroscienceUNSPECIFIED
Brain and Behavior Research Foundation23502
National Institute of Mental Health (NIMH)UNSPECIFIED
Subject Keywords:amygdala; human single neuron; face cells; interspecies comparison; visual tuning; latency; attention
Issue or Number:4
PubMed Central ID:PMC5283067
Record Number:CaltechAUTHORS:20170126-154932370
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20170126-154932370
Official Citation: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, Volume 18, Issue 4, 24 January 2017, Pages 878-891, ISSN 2211-1247, http://dx.doi.org/10.1016/j.celrep.2016.12.083. (//www.sciencedirect.com/science/article/pii/S2211124716318058)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:73762
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:27 Jan 2017 00:01
Last Modified:03 Oct 2019 16:31

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