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Neurons in human pre-supplementary motor area encode key computations for value-based choice

Nature Human Behaviour volume 7, pages 970–985 (2023)Cite this article

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Abstract

Adaptive behaviour in real-world environments requires that choices integrate several variables, including the novelty of the options under consideration, their expected value and uncertainty in value estimation. Here, to probe how integration over decision variables occurs during decision-making, we recorded neurons from the human pre-supplementary motor area (preSMA), ventromedial prefrontal cortex and dorsal anterior cingulate. Unlike the other areas, preSMA neurons not only represented separate pre-decision variables for each choice option but also encoded an integrated utility signal for each choice option and, subsequently, the decision itself. Post-decision encoding of variables for the chosen option was more widely distributed and especially prominent in the ventromedial prefrontal cortex. Our findings position the human preSMA as central to the implementation of value-based decisions.

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Fig. 1: Electrode positions, exploration task and behaviour.
Fig. 2: Encoding of action utility components in the preSMA and vmPFC.
Fig. 3: Neurons in the preSMA encode integrated utility.
Fig. 4: The PreSMA encodes decisions.
Fig. 5: Encoding selected stimulus properties.

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Data availability

Behavioural and neural data have been deposited in the OSF platform: https://osf.io/34b9f/?view_only=be3c529466fa444d8b97a2bab8951435.

Code availability

The code for data analysis can be found at: https://github.com/43technetium/casino_task_analysis.

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Acknowledgements

We thank the members of the O’Doherty and Rutishauser laboratories for discussions and feedback. We thank all participants and their families for their participation, and nurses and medical staff for their work. This work was supported by National Institutes of Health grant nos. R01DA040011 and R01MH111425 (to J.P.O.), R01MH110831 and U01NS117839 (to U.R.) and P50MH094258 (to J.P.O. and U.R.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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  1. These authors jointly supervised this work: Ueli Rutishauser, John P. O’Doherty.

Authors and Affiliations

  1. Computation and Neural Systems, Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA

    Tomas G. Aquino, Ueli Rutishauser & John P. O’Doherty

  2. Department of Neurosurgery, Cedars-Sinai Medical Center, Los Angeles, CA, USA

    Tomas G. Aquino, Adam N. Mamelak & Ueli Rutishauser

  3. Division of Humanities and Social Sciences, California Institute of Technology, Pasadena, CA, USA

    Jeffrey Cockburn & John P. O’Doherty

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Contributions

T.G.A., J.C., U.R. and J.P.O. designed the study. T.G.A. performed the experiments. T.G.A. and J.C. analysed the data. T.G.A., J.C., A.N.M., U.R. and J.P.O. wrote the paper. A.N.M. performed the surgery and supervised the clinical work.

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Correspondence to Tomas G. Aquino.

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Aquino, T.G., Cockburn, J., Mamelak, A.N. et al. Neurons in human pre-supplementary motor area encode key computations for value-based choice. Nat Hum Behav 7, 970–985 (2023). https://doi.org/10.1038/s41562-023-01548-2

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