Stable task information from an unstable neural population

Over days and weeks, neural activity representing an animal’s position and movement in sensorimotor cortex has been found to continually reconfigure or ‘drift’ during repeated trials of learned tasks, with no obvious change in behavior. This challenges classical theories, which assume stable engrams...

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Main Authors: Michael E Rule, Adrianna R Loback, Dhruva V Raman, Laura N Driscoll, Christopher D Harvey, Timothy O'Leary
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/51121
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author Michael E Rule
Adrianna R Loback
Dhruva V Raman
Laura N Driscoll
Christopher D Harvey
Timothy O'Leary
author_facet Michael E Rule
Adrianna R Loback
Dhruva V Raman
Laura N Driscoll
Christopher D Harvey
Timothy O'Leary
author_sort Michael E Rule
collection DOAJ
description Over days and weeks, neural activity representing an animal’s position and movement in sensorimotor cortex has been found to continually reconfigure or ‘drift’ during repeated trials of learned tasks, with no obvious change in behavior. This challenges classical theories, which assume stable engrams underlie stable behavior. However, it is not known whether this drift occurs systematically, allowing downstream circuits to extract consistent information. Analyzing long-term calcium imaging recordings from posterior parietal cortex in mice (Mus musculus), we show that drift is systematically constrained far above chance, facilitating a linear weighted readout of behavioral variables. However, a significant component of drift continually degrades a fixed readout, implying that drift is not confined to a null coding space. We calculate the amount of plasticity required to compensate drift independently of any learning rule, and find that this is within physiologically achievable bounds. We demonstrate that a simple, biologically plausible local learning rule can achieve these bounds, accurately decoding behavior over many days.
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spelling doaj.art-20628c39d67f481c81e9437b30663da72022-12-22T03:52:09ZengeLife Sciences Publications LtdeLife2050-084X2020-07-01910.7554/eLife.51121Stable task information from an unstable neural populationMichael E Rule0https://orcid.org/0000-0002-4196-774XAdrianna R Loback1Dhruva V Raman2Laura N Driscoll3Christopher D Harvey4Timothy O'Leary5https://orcid.org/0000-0002-1029-0158Department of Engineering, University of Cambridge, Cambridge, United KingdomDepartment of Engineering, University of Cambridge, Cambridge, United KingdomDepartment of Engineering, University of Cambridge, Cambridge, United KingdomDepartment of Electrical Engineering, Stanford University, Stanford, United StatesDepartment of Neurobiology, Harvard Medical School, Boston, United StatesDepartment of Engineering, University of Cambridge, Cambridge, United KingdomOver days and weeks, neural activity representing an animal’s position and movement in sensorimotor cortex has been found to continually reconfigure or ‘drift’ during repeated trials of learned tasks, with no obvious change in behavior. This challenges classical theories, which assume stable engrams underlie stable behavior. However, it is not known whether this drift occurs systematically, allowing downstream circuits to extract consistent information. Analyzing long-term calcium imaging recordings from posterior parietal cortex in mice (Mus musculus), we show that drift is systematically constrained far above chance, facilitating a linear weighted readout of behavioral variables. However, a significant component of drift continually degrades a fixed readout, implying that drift is not confined to a null coding space. We calculate the amount of plasticity required to compensate drift independently of any learning rule, and find that this is within physiologically achievable bounds. We demonstrate that a simple, biologically plausible local learning rule can achieve these bounds, accurately decoding behavior over many days.https://elifesciences.org/articles/51121spatial navigationlearning and memoryneural codingcomputational neuroscienceplasticitysystems modeling
spellingShingle Michael E Rule
Adrianna R Loback
Dhruva V Raman
Laura N Driscoll
Christopher D Harvey
Timothy O'Leary
Stable task information from an unstable neural population
eLife
spatial navigation
learning and memory
neural coding
computational neuroscience
plasticity
systems modeling
title Stable task information from an unstable neural population
title_full Stable task information from an unstable neural population
title_fullStr Stable task information from an unstable neural population
title_full_unstemmed Stable task information from an unstable neural population
title_short Stable task information from an unstable neural population
title_sort stable task information from an unstable neural population
topic spatial navigation
learning and memory
neural coding
computational neuroscience
plasticity
systems modeling
url https://elifesciences.org/articles/51121
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AT adriannarloback stabletaskinformationfromanunstableneuralpopulation
AT dhruvavraman stabletaskinformationfromanunstableneuralpopulation
AT laurandriscoll stabletaskinformationfromanunstableneuralpopulation
AT christopherdharvey stabletaskinformationfromanunstableneuralpopulation
AT timothyoleary stabletaskinformationfromanunstableneuralpopulation