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Neural population dynamics in dorsal premotor cortex underlying a reach decision

View ORCID ProfilePierre O Boucher, Tian Wang, Laura Carceroni, View ORCID ProfileGary Kane, View ORCID ProfileKrishna V Shenoy, View ORCID ProfileChandramouli Chandrasekaran
doi: https://doi.org/10.1101/2022.06.30.497070
Pierre O Boucher
aDepartment of Biomedical Engineering, Boston University, Boston, 02115, MA, USA
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Tian Wang
aDepartment of Biomedical Engineering, Boston University, Boston, 02115, MA, USA
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Laura Carceroni
jDepartment of Psychological and Brain Sciences, Boston University, Boston, 02115, MA, USA
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Gary Kane
jDepartment of Psychological and Brain Sciences, Boston University, Boston, 02115, MA, USA
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Krishna V Shenoy
bDepartment of Electrical Engineering, Stanford University, Stanford, 94305, CA, USA
cDepartment of Neurobiology, Stanford University, Stanford, 94305, CA, USA
dHoward Hughes Medical Institute, HHMI, Chevy Chase, 20815-6789, MD, USA
eDepartment of Bioengineering, Stanford University, Stanford, 94305, CA, USA
fStanford Neurosciences Institute, Stanford University, Stanford, 94305, CA, USA
gBio-X Program, Stanford University, Stanford, 94305, CA, USA
hDepartment of Neurosurgery, Stanford University, Stanford, 94305, CA, USA
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Chandramouli Chandrasekaran
aDepartment of Biomedical Engineering, Boston University, Boston, 02115, MA, USA
iCenter for Systems Neuroscience, Boston University, Boston, 02115, MA, USA
jDepartment of Psychological and Brain Sciences, Boston University, Boston, 02115, MA, USA
kDepartment of Anatomy & Neurobiology, Boston University, Boston, 02118, MA, USA
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  • For correspondence: cchandr1@bu.edu
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Abstract

We investigated if a dynamical systems approach could help understand the link between decision-related neural activity and decision-making behavior, a fundamentally unresolved problem. The dynamical systems approach posits that neural dynamics can be parameterized by a state equation that has different initial conditions and evolves in time by combining at each time step, recurrent dynamics and inputs. For decisions, the two key predictions of the dynamical systems approach are that 1) initial conditions substantially predict subsequent dynamics and behavior and 2) inputs should combine with initial conditions to lead to different choice-related dynamics. We tested these predictions by investigating neural population dynamics in the dorsal premotor cortex (PMd) of monkeys performing a red-green reaction time (RT) checkerboard discrimination task where we varied the sensory evidence (i.e., the inputs). Prestimulus neural state, a proxy for the initial condition, predicted poststimulus neural trajectories and showed organized covariation with RT. Furthermore, faster RTs were associated with faster pre- and poststimulus dynamics as compared to slower RTs, with these effects observed within a stimulus difficulty. Poststimulus dynamics depended on both the sensory evidence and initial condition, with easier stimuli and “fast” initial conditions leading to the fastest choice-related dynamics whereas harder stimuli and “slow” initial conditions led to the slowest dynamics. Finally, changes in initial condition were related to the outcome of the previous trial, with slower pre- and poststimulus population dynamics and RTs on trials following an error as compared to trials following a correct response. Together these results suggest that decision-related activity in PMd is well described by a dynamical system where inputs combine with initial conditions that covary with eventual RT and previous outcome, to induce decision-related dynamics.

Competing Interest Statement

K.V.S. consults for Neuralink Corp. and CTRL-Labs Inc. (part of Facebook Reality Labs) and is on the scientific advisory boards of MIND-X Inc., Inscopix Inc., and Heal Inc. All other authors have no competing interests. These companies provided no funding and had no role in study design, data collection, and interpretation or the decision to submit the work for publication.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted July 04, 2022.
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Neural population dynamics in dorsal premotor cortex underlying a reach decision
Pierre O Boucher, Tian Wang, Laura Carceroni, Gary Kane, Krishna V Shenoy, Chandramouli Chandrasekaran
bioRxiv 2022.06.30.497070; doi: https://doi.org/10.1101/2022.06.30.497070
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Neural population dynamics in dorsal premotor cortex underlying a reach decision
Pierre O Boucher, Tian Wang, Laura Carceroni, Gary Kane, Krishna V Shenoy, Chandramouli Chandrasekaran
bioRxiv 2022.06.30.497070; doi: https://doi.org/10.1101/2022.06.30.497070

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