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Frontal cortex neuron types categorically encode single decision variables

Author

Listed:
  • Junya Hirokawa

    (Cold Spring Harbor Laboratory
    Doshisha University)

  • Alexander Vaughan

    (Cold Spring Harbor Laboratory)

  • Paul Masset

    (Cold Spring Harbor Laboratory
    Watson School of Biological Sciences
    Centre for Brain Science, Harvard University)

  • Torben Ott

    (Cold Spring Harbor Laboratory)

  • Adam Kepecs

    (Cold Spring Harbor Laboratory)

Abstract

Individual neurons in many cortical regions have been found to encode specific, identifiable features of the environment or body that pertain to the function of the region1–3. However, in frontal cortex, which is involved in cognition, neural responses display baffling complexity, carrying seemingly disordered mixtures of sensory, motor and other task-related variables4–13. This complexity has led to the suggestion that representations in individual frontal neurons are randomly mixed and can only be understood at the neural population level14,15. Here we show that neural activity in rat orbitofrontal cortex (OFC) is instead highly structured: single neuron activity co-varies with individual variables in computational models that explain choice behaviour. To characterize neural responses across a large behavioural space, we trained rats on a behavioural task that combines perceptual and value-guided decisions. An unbiased, model-free clustering analysis identified distinct groups of OFC neurons, each with a particular response profile in task-variable space. Applying a simple model of choice behaviour to these categorical response profiles revealed that each profile quantitatively corresponds to a specific decision variable, such as decision confidence. Additionally, we demonstrate that a connectivity-defined cell type, orbitofrontal neurons projecting to the striatum, carries a selective and temporally sustained representation of a single decision variable: integrated value. We propose that neurons in frontal cortex, as in other cortical regions, form a sparse and overcomplete representation of features relevant to the region’s function, and that they distribute this information selectively to downstream regions to support behaviour.

Suggested Citation

  • Junya Hirokawa & Alexander Vaughan & Paul Masset & Torben Ott & Adam Kepecs, 2019. "Frontal cortex neuron types categorically encode single decision variables," Nature, Nature, vol. 576(7787), pages 446-451, December.
  • Handle: RePEc:nat:nature:v:576:y:2019:i:7787:d:10.1038_s41586-019-1816-9
    DOI: 10.1038/s41586-019-1816-9
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    Citations

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    Cited by:

    1. Wenqi Chen & Jiejunyi Liang & Qiyun Wu & Yunyun Han, 2024. "Anterior cingulate cortex provides the neural substrates for feedback-driven iteration of decision and value representation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Nagaraj R. Mahajan & Shreesh P. Mysore, 2022. "Donut-like organization of inhibition underlies categorical neural responses in the midbrain," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Wei-Long Zheng & Zhongxuan Wu & Ali Hummos & Guangyu Robert Yang & Michael M. Halassa, 2024. "Rapid context inference in a thalamocortical model using recurrent neural networks," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Yihan Wang & Qian-Quan Sun, 2024. "A prefrontal motor circuit initiates persistent movement," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Kyuhyun Choi & Eugenio Piasini & Edgar Díaz-Hernández & Luigim Vargas Cifuentes & Nathan T. Henderson & Elizabeth N. Holly & Manivannan Subramaniyan & Charles R. Gerfen & Marc V. Fuccillo, 2023. "Distributed processing for value-based choice by prelimbic circuits targeting anterior-posterior dorsal striatal subregions in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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