Cortical Observation by Synchronous Multifocal Optical Sampling Reveals Widespread Population Encoding of Actions

Isaac V Kauvar; Timothy A Machado; Elle Yuen; John Kochalka; Minseung Choi; William E Allen; Gordon Wetzstein; Karl Deisseroth

doi:10.1016/j.neuron.2020.04.023

Cortical Observation by Synchronous Multifocal Optical Sampling Reveals Widespread Population Encoding of Actions

Neuron. 2020 Jul 22;107(2):351-367.e19. doi: 10.1016/j.neuron.2020.04.023. Epub 2020 May 19.

Authors

Isaac V Kauvar¹, Timothy A Machado², Elle Yuen², John Kochalka³, Minseung Choi³, William E Allen⁴, Gordon Wetzstein⁵, Karl Deisseroth⁶

Affiliations

¹ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA; Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.
² Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.
³ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA; Neuroscience Graduate Program, Stanford University, Stanford, CA 94305, USA.
⁴ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA; Neuroscience Graduate Program, Stanford University, Stanford, CA 94305, USA; Department of Biology, Stanford University, Stanford, CA 94305, USA.
⁵ Department of Electrical Engineering, Stanford University, Stanford, CA 94305, USA.
⁶ Department of Bioengineering, Stanford University, Stanford, CA 94305, USA; Department of Psychiatry and Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305, USA. Electronic address: deissero@stanford.edu.

Abstract

To advance the measurement of distributed neuronal population representations of targeted motor actions on single trials, we developed an optical method (COSMOS) for tracking neural activity in a largely uncharacterized spatiotemporal regime. COSMOS allowed simultaneous recording of neural dynamics at ∼30 Hz from over a thousand near-cellular resolution neuronal sources spread across the entire dorsal neocortex of awake, behaving mice during a three-option lick-to-target task. We identified spatially distributed neuronal population representations spanning the dorsal cortex that precisely encoded ongoing motor actions on single trials. Neuronal correlations measured at video rate using unaveraged, whole-session data had localized spatial structure, whereas trial-averaged data exhibited widespread correlations. Separable modes of neural activity encoded history-guided motor plans, with similar population dynamics in individual areas throughout cortex. These initial experiments illustrate how COSMOS enables investigation of large-scale cortical dynamics and that information about motor actions is widely shared between areas, potentially underlying distributed computations.

Keywords: COSMOS; calcium imaging; cortex; licking; motor planning; multifocal; neural decoding; neural dynamics; population dynamics; synchronous; widefield.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Algorithms
Animals
Behavior, Animal / physiology
Brain Mapping
Cerebral Cortex / physiology*
Conditioning, Operant
Craniotomy
Mice
Neocortex / cytology
Neocortex / physiology
Neuroimaging / instrumentation*
Neuroimaging / methods*
Neurons
Observation / methods*
Optogenetics / methods
Psychomotor Performance
Robotic Surgical Procedures / instrumentation
Robotic Surgical Procedures / methods
Signal-To-Noise Ratio

Abstract

Publication types

MeSH terms

Grants and funding