Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala
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.
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.Attached Files
Published - 1-s2.0-S2211124716318058-main.pdf
Supplemental Material - mmc1.pdf
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Additional details
- PMCID
- PMC5283067
- Eprint ID
- 73762
- Resolver ID
- CaltechAUTHORS:20170126-154932370
- NSF
- BCS-1554105
- NIH
- P50 MH094258
- NIH
- R21 MH086065
- NIH
- P50 MH100023
- NIH
- R01 MH110831
- McKnight Endowment Fund for Neuroscience
- Brain and Behavior Research Foundation
- 23502
- National Institute of Mental Health (NIMH)
- Created
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2017-01-27Created from EPrint's datestamp field
- Updated
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2021-11-11Created from EPrint's last_modified field