Cited by 103Memory and Neural MechanismsPrimate Behavior and EcologyNeural and Behavioral Psychology Studies

Primate amygdala neurons simulate decision processes of social partners

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Grabenhorst, Fabian, Báez-Mendoza, Raymundo, Genest, Wilfried, Deco, Gustavo, Schultz, Wolfram·2019·Cell

Abstract

By observing their social partners, primates learn about reward values of objects. Here, we show that monkeys' amygdala neurons derive object values from observation and use these values to simulate a partner monkey's decision process. While monkeys alternated making reward-based choices, amygdala neurons encoded object-specific values learned from observation. Dynamic activities converted these values to representations of the recorded monkey's own choices. Surprisingly, the same activity patterns unfolded spontaneously before partner's choices in separate neurons, as if these neurons simulated the partner's decision-making. These "simulation neurons" encoded signatures of mutual-inhibitory decision computation, including value comparisons and value-to-choice conversions, resulting in accurate predictions of partner's choices. Population decoding identified differential contributions of amygdala subnuclei. Biophysical modeling of amygdala circuits showed that simulation neurons emerge naturally from convergence between object-value neurons and self-other neurons. By simulating decision computations during observation, these neurons could allow primates to reconstruct their social partners' mental states.

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  • Macaque amygdala neurons are involved in social, observational learning in a reversal-learning task.

    “In addition, it has been shown in the macaque that amygdala neurons are involved in social, observational learning in a reversal-learning task, and that some neurons even predicted the choices of the partner monkey (Grabenhorst et al., 2019).”

    From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Grabenhorst et al., 2019

  • Some macaque amygdala neurons predicted the choices of the partner monkey.

    “In addition, it has been shown in the macaque that amygdala neurons are involved in social, observational learning in a reversal-learning task, and that some neurons even predicted the choices of the partner monkey (Grabenhorst et al., 2019).”

    From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Grabenhorst et al., 2019

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Authors
Grabenhorst, F., Báez-Mendoza, R., Genest, W., Deco, G., & Schultz, W.
Affiliations
  • University of Cambridge (GB)
  • Institució Catalana de Recerca i Estudis Avançats (ES)
Venue
Cell
Publisher
Elsevier BV
Published
2019-05
Volume
177
Issue
4
Pages
986-998.e15
ISSN
0092-8674 (ISSN-L)
OpenAlex
W2936454282
Cited by
103
References
65
Citations by year
2026: 9 · 2025: 15 · 2024: 10 · 2023: 12 · 2022: 14 · 2021: 17 · 2020: 19 · 2019: 7
FWCI
8.29
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo (cc-by)
Funders
  • Wellcome Trust
  • Principal Research Fellowship and Programme Grant (095495)
  • Sir Henry Dale Fellowship (206207/Z/17/Z)
  • European Research Council
  • ERC Advanced Grant (293549)
  • NIH Caltech Conte Center (P50MH094258)
  • MGH ECOR Fund for Medical Discovery
  • NARSAD Young Investigator Grant
  • Brain & Behavior Research Foundation
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
amygdala, social decision-making, observational learning, reciprocal inhibition, self and other representations, social cognition, primate social behavior, population decoding, amygdala subnuclei, biophysical model
MeSH terms
Amygdala, Animals, Behavior, Animal, Choice Behavior, Decision Making, Interpersonal Relations, Learning, Macaca mulatta, Male, Neurons, Reward

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