Domain-specific representation of social inference by neurons in the human amygdala and hippocampus
Abstract
Inferring the intentions and emotions of others from behavior is crucial for social cognition. While neuroimaging studies have identified brain regions involved in social inference, it remains unknown whether performing social inference is an abstract computation that generalizes across different stimulus categories or is specific to certain stimulus domain. We recorded single-neuron activity from the medial temporal lobe (MTL) and the medial frontal cortex (MFC) in neurosurgical patients performing different types of inferences from images of faces, hands, and natural scenes. Our findings indicate distinct neuron populations in both regions encoding inference type for social (faces, hands) and nonsocial (scenes) stimuli, while stimulus category was itself represented in a task-general manner. Uniquely in the MTL, social inference type was represented by separate subsets of neurons for faces and hands, suggesting a domain-specific representation. These results reveal evidence for specialized social inference processes in the MTL, in which inference representations were entangled with stimulus type as expected from a domain-specific process.
Copyright and License
© 2024 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).
Acknowledgement
We thank all patients for their participation, staff from Cedars-Sinai Medical Center for support with patient testing, and H. Courellis for discussion.
Funding
This research was supported by the McDonnell Center for Systems Neuroscience, AFOSR (FA9550-21-1-0088), NSF (BCS-1945230 and IIS-2114644), and NIH (K99EY036650 to R.C., R01MH129426 to S.W., P50MH094258 to R.A., U01NS117839 to U.R., and R01MH134990 to U.R. and R.A.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Contributions
J.D., R.A., and U.R. designed the research. J.D. and U.R. performed the experiments. A.N.M. performed the surgery. R.C., S.W., and U.R. analyzed the data. R.C., R.A., S.W., and U.R. wrote the paper. All authors discussed the results and contributed toward the manuscript.
Data Availability
All data needed to evaluate the conclusions in this paper are present in the paper and/or the Supplementary Materials. The raw data (single-neuron activity and behavior) is available at https://osf.io/qx92s/.
Supplemental Material
This PDF file includes:
Supplementary Text
Tables S1 to S3
Figs. S1 to S5
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Additional details
- National Institutes of Health
- R01MH129426
- National Institutes of Health
- P50MH094258
- National Institutes of Health
- U01NS117839
- National Institutes of Health
- K99EY036650
- United States Air Force Office of Scientific Research
- FA9550-21-1-0088
- National Science Foundation
- BCS-1945230
- National Science Foundation
- IIS-2114644
- Accepted
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2024-11-01Accepted
- Caltech groups
- Division of Biology and Biological Engineering
- Publication Status
- Published