Distinct Sources of Deterministic and Stochastic Components of Action Timing Decisions in Rodent Frontal Cortex

Masayoshi Murakami; Hanan Shteingart; Yonatan Loewenstein; Zachary F. Mainen

doi:10.1016/j.neuron.2017.04.040

Distinct Sources of Deterministic and Stochastic Components of Action Timing Decisions in Rodent Frontal Cortex

Masayoshi Murakami^*, Hanan Shteingart, Yonatan Loewenstein, Zachary F. Mainen

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

The selection and timing of actions are subject to determinate influences such as sensory cues and internal state as well as to effectively stochastic variability. Although stochastic choice mechanisms are assumed by many theoretical models, their origin and mechanisms remain poorly understood. Here we investigated this issue by studying how neural circuits in the frontal cortex determine action timing in rats performing a waiting task. Electrophysiological recordings from two regions necessary for this behavior, medial prefrontal cortex (mPFC) and secondary motor cortex (M2), revealed an unexpected functional dissociation. Both areas encoded deterministic biases in action timing, but only M2 neurons reflected stochastic trial-by-trial fluctuations. This differential coding was reflected in distinct timescales of neural dynamics in the two frontal cortical areas. These results suggest a two-stage model in which stochastic components of action timing decisions are injected by circuits downstream of those carrying deterministic bias signals.

Original language	American English
Pages (from-to)	908-919.e7
Journal	Neuron
Volume	94
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2017.04.040
State	Published - 17 May 2017

Bibliographical note

Funding Information:
We thank Maria Inês Vicente, Gil M. Costa, and Mark Terrelonge for help in behavioral training and electrophysiology, Nicole Horst and Mark Laubach for advice on muscimol inactivation procedures, Dmitry Kobak and Pietro Vertechi for advice on demixed principal component analysis, Barry Burbach and Mauricia Vinhas for technical assistance, and Fanny Cazettes, Luca Mazzucato, Gautam Agarwal, Eran Lottem, Cindy Poo, and Bassam Atallah for helpful comments on the manuscript. This work was supported by European Research Council (250334 and 671251, Z.F.M.), Simons Foundation (325057, Z.F.M.), Champalimaud Foundation (Z.F.M.), the Israel Science Foundation (757/16, Y.L.), the Gatsby Charitable Foundation (Y.L.), Fundaçao para a Ciência e a Tecnologia (SFRH/BPD/46314/2008, M.M.), the Uehara Memorial Foundation (M.M.), and Fundaçao Bial (127/08, M.M.).

Publisher Copyright:
© 2017 Elsevier Inc.

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10.1016/j.neuron.2017.04.040

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title = "Distinct Sources of Deterministic and Stochastic Components of Action Timing Decisions in Rodent Frontal Cortex",

abstract = "The selection and timing of actions are subject to determinate influences such as sensory cues and internal state as well as to effectively stochastic variability. Although stochastic choice mechanisms are assumed by many theoretical models, their origin and mechanisms remain poorly understood. Here we investigated this issue by studying how neural circuits in the frontal cortex determine action timing in rats performing a waiting task. Electrophysiological recordings from two regions necessary for this behavior, medial prefrontal cortex (mPFC) and secondary motor cortex (M2), revealed an unexpected functional dissociation. Both areas encoded deterministic biases in action timing, but only M2 neurons reflected stochastic trial-by-trial fluctuations. This differential coding was reflected in distinct timescales of neural dynamics in the two frontal cortical areas. These results suggest a two-stage model in which stochastic components of action timing decisions are injected by circuits downstream of those carrying deterministic bias signals.",

author = "Masayoshi Murakami and Hanan Shteingart and Yonatan Loewenstein and Mainen, {Zachary F.}",

note = "Funding Information: We thank Maria In{\^e}s Vicente, Gil M. Costa, and Mark Terrelonge for help in behavioral training and electrophysiology, Nicole Horst and Mark Laubach for advice on muscimol inactivation procedures, Dmitry Kobak and Pietro Vertechi for advice on demixed principal component analysis, Barry Burbach and Mauricia Vinhas for technical assistance, and Fanny Cazettes, Luca Mazzucato, Gautam Agarwal, Eran Lottem, Cindy Poo, and Bassam Atallah for helpful comments on the manuscript. This work was supported by European Research Council (250334 and 671251, Z.F.M.), Simons Foundation (325057, Z.F.M.), Champalimaud Foundation (Z.F.M.), the Israel Science Foundation (757/16, Y.L.), the Gatsby Charitable Foundation (Y.L.), Funda{\c c}ao para a Ci{\^e}ncia e a Tecnologia (SFRH/BPD/46314/2008, M.M.), the Uehara Memorial Foundation (M.M.), and Funda{\c c}ao Bial (127/08, M.M.). Publisher Copyright: {\textcopyright} 2017 Elsevier Inc.",

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Distinct Sources of Deterministic and Stochastic Components of Action Timing Decisions in Rodent Frontal Cortex

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