Dataset Information

Single-trial cross-area neural population dynamics during long-term skill learning.

ABSTRACT: Mammalian cortex has both local and cross-area connections, suggesting vital roles for both local and cross-area neural population dynamics in cortically-dependent tasks, like movement learning. Prior studies of movement learning have focused on how single-area population dynamics change during short-term adaptation. It is unclear how cross-area dynamics contribute to movement learning, particularly long-term learning and skill acquisition. Using simultaneous recordings of rodent motor (M1) and premotor (M2) cortex and computational methods, we show how cross-area activity patterns evolve during reach-to-grasp learning in rats. The emergence of reach-related modulation in cross-area activity correlates with skill acquisition, and single-trial modulation in cross-area activity predicts reaction time and reach duration. Local M2 neural activity precedes local M1 activity, supporting top-down hierarchy between the regions. M2 inactivation preferentially affects cross-area dynamics and behavior, with minimal disruption of local M1 dynamics. Together, these results indicate that cross-area population dynamics are necessary for learned motor skills.

SUBMITTER: Veuthey TL

PROVIDER: S-EPMC7426952 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Single-trial cross-area neural population dynamics during long-term skill learning.

Veuthey T L TL Derosier K K Kondapavulur S S Ganguly K K

Nature communications 20200813 1

Mammalian cortex has both local and cross-area connections, suggesting vital roles for both local and cross-area neural population dynamics in cortically-dependent tasks, like movement learning. Prior studies of movement learning have focused on how single-area population dynamics change during short-term adaptation. It is unclear how cross-area dynamics contribute to movement learning, particularly long-term learning and skill acquisition. Using simultaneous recordings of rodent motor (M1) and ...[more]

PMID: 32792523

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Project description:The dynamics of human brain function are increasingly well understood at the short timescale of seconds/minutes (for example, through studies of learning) and the long timescale of years/decades (for example, through studies of development andageing), but almost nothing is known about how the human brainfunction varies across the range of days to months. This is a critical gap, because major psychiatric disorders show large fluctuations in brain function over this timescale. However, the kind of dense longitudinal phenotyping that is necessary to understand this question is extremely challenging with healthy human volunteers,who are unlikely to be sufficiently motivated to sustain frequent participation in a study over a long period. For this reason, the participation of motivated experimenters can be uniquely useful for demanding longitudinal studies. We investigated the long-range dynamics of brain function andtheir relation to a broad set of psychological and biological variables in a single healthy human (author R.A.P.) over the course of 532 days (along with several follow-up visits), representing one of the most intensive biological characterizations of a single individual ever performed (referred to hereafter as the MyConnectomestudy). The study was designed to measure the broadest possible range of human phenotypes (the phenome’3,4) to allow the widespread assessment of relations between psychological, neural and metabolic function. The results of the present study demonstrate that healthy brain function shows rich dynamics over the course of 18 months, and that these dynamics are paralleled by ongoing fluctuations in psychological and physiological function as observed in behaviour,gene expression and metabolomic measurements. These findings provide a proof of concept for the dynamic longitudinal phenotyping of individuals, which we propose will be crucial togain a better understanding of the substantial fluctuations in psychological and neural function in individuals with major psychiatric disorders.

Project description:BACKGROUND:Since motor learning is a key component for stroke recovery, enhancing motor skill learning is a crucial challenge for neurorehabilitation. Transcranial direct current stimulation (tDCS) is a promising approach for improving motor learning. The aim of this trial was to test the hypothesis that dual-tDCS applied bilaterally over the primary motor cortices (M1) improves online motor skill learning with the paretic hand and its long-term retention. METHODS:Eighteen chronic stroke patients participated in a randomized, cross-over, placebo-controlled, double bind trial. During separate sessions, dual-tDCS or sham dual-tDCS was applied over 30?min while stroke patients learned a complex visuomotor skill with the paretic hand: using a computer mouse to move a pointer along a complex circuit as quickly and accurately as possible. A learning index involving the evolution of the speed/accuracy trade-off was calculated. Performance of the motor skill was measured at baseline, after intervention and 1?week later. RESULTS:After sham dual-tDCS, eight patients showed performance worsening. In contrast, dual-tDCS enhanced the amount and speed of online motor skill learning compared to sham (p?<?0.001) in all patients; this superiority was maintained throughout the hour following. The speed/accuracy trade-off was shifted more consistently after dual-tDCS (n?=?10) than after sham (n?=?3). More importantly, 1?week later, online enhancement under dual-tDCS had translated into superior long-term retention (+44%) compared to sham (+4%). The improvement generalized to a new untrained circuit and to digital dexterity. CONCLUSION:A single-session of dual-tDCS, applied while stroke patients trained with the paretic hand significantly enhanced online motor skill learning both quantitatively and qualitatively, leading to successful long-term retention and generalization. The combination of motor skill learning and dual-tDCS is promising for improving post-stroke neurorehabilitation.

Dataset Information

Single-trial cross-area neural population dynamics during long-term skill learning.

Publications

Single-trial cross-area neural population dynamics during long-term skill learning.

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