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A neuronal social trait space for first impressions in the human amygdala and hippocampus

Molecular Psychiatry volume 27, pages 3501–3509 (2022)Cite this article

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Abstract

People instantaneously evaluate faces with significant agreement on evaluations of social traits. However, the neural basis for such rapid spontaneous face evaluation remains largely unknown. Here, we recorded from 490 neurons in the human amygdala and hippocampus and found that the neuronal activity was associated with the geometry of a social trait space. We further investigated the temporal evolution and modulation on the social trait representation, and we employed encoding and decoding models to reveal the critical social traits for the trait space. We also recorded from another 938 neurons and replicated our findings using different social traits. Together, our results suggest that there exists a neuronal population code for a comprehensive social trait space in the human amygdala and hippocampus that underlies spontaneous first impressions. Changes in such neuronal social trait space may have implications for the abnormal processing of social information observed in some neurological and psychiatric disorders.

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Fig. 1: A neuronal social trait space.
Fig. 2: Encoding and decoding models.
Fig. 3: Replication of the neuronal social trait space using the FaceGen stimuli and a different set of social traits.
Fig. 4: People with ASD demonstrate atypical social trait representations.

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Data availability

All data are publicly available on OSF (https://osf.io/a4jn3/).

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Acknowledgements

We thank all patients for their participation, staff from WVU Ruby Memorial Hospital for support with patient testing, and Paula Webster for valuable comments. This research was supported by AFOSR Young Investigator Program Award (FA9550-21-1-0088), NSF Grants (BCS-1945230, IIS-2114644), Dana Foundation Clinical Neuroscience Award, and ORAU Ralph E. Powe Junior Faculty Enhancement Award. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Authors and Affiliations

  1. Lane Department of Computer Science and Electrical Engineering, West Virginia University, Morgantown, WV, 26506, USA

    Runnan Cao, Xin Li & Shuo Wang

  2. Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH, 03755, USA

    Chujun Lin

  3. Department of Neurosurgery, West Virginia University, Morgantown, WV, 26506, USA

    Johnie Hodge & Nicholas J. Brandmeir

  4. Booth School of Business, University of Chicago, Chicago, IL, 60637, USA

    Alexander Todorov

  5. Rockefeller Neuroscience Institute, West Virginia University, Morgantown, WV, 26506, USA

    Nicholas J. Brandmeir & Shuo Wang

  6. Department of Radiology, Washington University in St. Louis, St. Louis, MO, 63110, USA

    Shuo Wang

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Contributions

RC, CL, XL, and SW designed research. RC and SW performed experiments. NJB performed surgery. RC, CL, JH, and SW analyzed data. RC, CL, XL, AT, and SW wrote the paper. All authors discussed the results and contributed toward the manuscript.

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Correspondence to Runnan Cao or Shuo Wang.

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Cao, R., Lin, C., Hodge, J. et al. A neuronal social trait space for first impressions in the human amygdala and hippocampus. Mol Psychiatry 27, 3501–3509 (2022). https://doi.org/10.1038/s41380-022-01583-x

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