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Value dynamics affect choice preparation during decision-making

Nature Neuroscience volume 26, pages 1575–1583 (2023)Cite this article

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Abstract

During decision-making, neurons in the orbitofrontal cortex (OFC) sequentially represent the value of each option in turn, but it is unclear how these dynamics are translated into a choice response. One brain region that may be implicated in this process is the anterior cingulate cortex (ACC), which strongly connects with OFC and contains many neurons that encode the choice response. We investigated how OFC value signals interacted with ACC neurons encoding the choice response by performing simultaneous high-channel count recordings from the two areas in nonhuman primates. ACC neurons encoding the choice response steadily increased their firing rate throughout the decision-making process, peaking shortly before the time of the choice response. Furthermore, the value dynamics in OFC affected ACC ramping—when OFC represented the more valuable option, ACC ramping accelerated. Because OFC tended to represent the more valuable option more frequently and for a longer duration, this interaction could explain how ACC selects the more valuable response.

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Fig. 1: Task and behavior.
Fig. 2: Single-neuron encoding of choice and value during the 500-ms preceding choice.
Fig. 3: ACC ramping activity around the time of the choice response.
Fig. 4: Value decoding in OFC and ACC.
Fig. 5: OFC value integration.
Fig. 6: Effects of OFC value states on ACC direction-selective neurons.

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Data availability

The dataset supporting the current work is available from the corresponding author upon request.

Code availability

The analysis code supporting the current work is available on T.W.E.’s GitHub: https://github.com/t-elston/OFCvalue-to-ACCresponse.

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Acknowledgements

We thank C. Ford, E. Hu, W. Liberti, L. Meckler and N. Munet for useful feedback on the manuscript. This work was funded by NIMH (R01-MH117763 and R01-MH121448 to J.D.W.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Author notes

  1. These authors contributed equally: Zuzanna Z. Balewski, Thomas W. Elston.

Authors and Affiliations

  1. Helen Wills Neuroscience Institute, University of California at Berkeley, Berkeley, CA, USA

    Zuzanna Z. Balewski, Thomas W. Elston, Eric B. Knudsen & Joni D. Wallis

  2. Department of Psychology, University of California at Berkeley, Berkeley, CA, USA

    Joni D. Wallis

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  1. Zuzanna Z. Balewski
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Contributions

Z.Z.B. and J.D.W. designed the experiments. Z.Z.B. and E.B.K. collected the data. T.W.E. and Z.Z.B. analyzed the data. Z.Z.B., T.W.E. and J.D.W. wrote the manuscript. E.B.K. and T.W.E. edited the manuscript. J.D.W. supervised the project.

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Correspondence to Joni D. Wallis.

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Nature Neuroscience thanks R Becket Ebitz, Camillo Padoa-Schioppa and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Choice biases as a function of reward probability.

(a) Probability of subject C selecting a given choice option as a function of the probability of reward predicted by the option, as compared to the optimal choice as given by equation 1. N = 12508 trials. Error bars denote the standard error of the mean. (b) Same data as for subject G. N = 4902 trials. Error bars denote the standard error of the mean. (c) Difference of subjects’ choices from choice optimality as a function of the probability of reward. Asterisks indicate significant differences from zero (p < 0.001, one-sample t-test corrected for multiple comparisons). Error bars denote the standard error of the mean.

Extended Data Fig. 2 Subjects’ saccade times.

Distribution of first and second saccade times.

Extended Data Fig. 3 Recording locations.

Reconstruction of (a) ACC and (b) OFC recording sites on coronal slices. Circle sizes represent the number of neurons.

Extended Data Fig. 4 Relationship between single neural activity and population-level decoding.

(a) More neurons significantly encoded the value of the same option that was currently reported by the decoder (color) than significantly encoded the value of the alternate option (gray). Significant encoding was determined by regressing the neuron’s firing rate (synced to the onset of the decoder state) against either the value of the option reported by the decoder or the value of the alternate option (assessed at p < 0.01). Horizontal gray bars indicate significant differences between the proportion of neurons encoding the current versus alternate option (χ2 test, p < 0.01). (b) Each data point is the beta coefficient from each neuron’s standardized firing rate during the first 100 ms immediately after state onset regressed against the parameters shown on the x- and y- axes. In both regions and both subjects there was a strong correlation between a neuron’s encoding of value for the left or right option when either was currently being reported by the decoder.

Supplementary information

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Supplementary Tables 1 and 2.

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Balewski, Z.Z., Elston, T.W., Knudsen, E.B. et al. Value dynamics affect choice preparation during decision-making. Nat Neurosci 26, 1575–1583 (2023). https://doi.org/10.1038/s41593-023-01407-3

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