Learning in the Rodent Motor Cortex

Peters, Amy; Liu, Haixin; Komiyama, Takaki

doi:10.1146/annurev-neuro-072116-031407

Cited by 123 publications

(101 citation statements)

References 147 publications

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“…Once animals learn the stereotyped motor sequences required for our task, they are expressed in largely unaltered form over long periods of time 35 , suggesting the formation of stable memories. While prior studies have suggested that motor memories are stored in motor cortex [85][86][87][88][89][90][91][92][93][94][95] and/or at synapses between motor cortex and striatum 23,27,31,32,34 , neither of these neural substrates are required for executing the behaviors we train 11,35 . The crucial involvement of the DLS in both motor sequence learning ( Fig.…”

Section: Reversal Of Long-term Synaptic Plasticity In Dls Disrupts Pementioning

confidence: 88%

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Wolff

Ölveczky

2019

Preprint

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The acquisition and execution of learned motor sequences are mediated by a distributed motor network, spanning cortical and subcortical brain areas. The sensorimotor striatum is an important cog in this network, yet how its two main inputs, from motor cortex and thalamus respectively, contribute to its role in motor learning and execution remains largely unknown. To address this, we trained rats in a task that produces highly stereotyped and idiosyncratic motor sequences. We found that motor cortical input to the sensorimotor striatum is critical for the learning process, but after the behaviors were consolidated, this corticostriatal pathway became dispensable. Functional silencing of striatal-projecting thalamic neurons, however, disrupted the execution of the learned motor sequences, causing rats to revert to behaviors produced early in learning and preventing them from re-learning the task. These results show that the sensorimotor striatum is a conduit through which motor cortical inputs can drive experiencedependent changes in subcortical motor circuits, likely at thalamostriatal synapses.

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Section: Reversal Of Long-term Synaptic Plasticity In Dls Disrupts Pementioning

confidence: 88%

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Wolff

Ölveczky

2019

Preprint

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“…There is a strong body of evidence to suggest that a reduction in cortical inhibitory tone is critical for the induction of M1 plasticity (Bachtiar & Stagg, ; Peters et al . ). Specifically, a reduction in GABAergic signalling appears crucial to the induction of long‐term potentiation (LTP)‐like plasticity in M1 (Castro‐Alamancos et al .…”

Section: Introductionmentioning

confidence: 97%

The dynamics of cortical GABA in human motor learning

Kolasinski

Hinson

Zand

et al. 2018

The Journal of Physiology

137

120

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Key points The ability to learn new motor skills is supported by plasticity in the structural and functional organisation of the primary motor cortex in the human brain.Changes inhibitory to signalling by GABA are thought to be crucial in inducing motor cortex plasticity.This study used magnetic resonance spectroscopy (MRS) to quantify the concentration of GABA in human motor cortex during a period of motor learning, as well as during a period of movement and a period at rest.We report evidence for a reduction in the MRS‐measured concentration of GABA specific to learning. Further, the GABA concentration early in the learning task was strongly correlated with the magnitude of subsequent learning: higher GABA concentrations were associated with poorer learning.The results provide initial insight into the neurochemical correlates of cortical plasticity associated with motor learning, specifically relevant in therapeutic efforts to induce cortical plasticity during recovery from stroke. AbstractThe ability to learn novel motor skills is a central part of our daily lives and can provide a model for rehabilitation after a stroke. However, there are still fundamental gaps in our understanding of the physiological mechanisms that underpin human motor plasticity. The acquisition of new motor skills is dependent on changes in local circuitry within the primary motor cortex (M1). This reorganisation has been hypothesised to be facilitated by a decrease in local inhibition via modulation of the neurotransmitter GABA, but this link has not been conclusively demonstrated in humans. Here, we used 7 T magnetic resonance spectroscopy to investigate the dynamics of GABA concentrations in human M1 during the learning of an explicit, serial reaction time task. We observed a significant reduction in GABA concentration during motor learning that was not seen in an equivalent motor task lacking a learnable sequence, nor during a passive resting task of the same duration. No change in glutamate was observed in any group. Furthermore, M1 GABA measured early in task performance was strongly correlated with the degree of subsequent learning, such that greater inhibition was associated with poorer subsequent learning. This result suggests that higher levels of cortical inhibition may present a barrier that must be surmounted in order to achieve an increase in M1 excitability, and hence encoding of a new motor skill. These results provide strong support for the mechanistic role of GABAergic inhibition in motor plasticity, raising questions regarding the link between population variability in motor learning and GABA metabolism in the brain.

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“…Circuits within supragranular layers appear crucial for processing task‐relevant sensory information (Thura & Cisek, , ) and for learning (Peters et al . , ; Chen et al . ).…”

Section: Introductionmentioning

confidence: 99%

“…In the primary motor cortex (M1), circuits located in different layers appear to play different roles, reflecting their distinct anatomical connections. Circuits within supragranular layers appear crucial for processing task-relevant sensory information (Thura & Cisek, 2014, 2016 and for learning (Peters et al 2014(Peters et al , 2017bChen et al 2015). By contrast, activity in infragranular layer 5 is correlated with the prevention and production of movement (Ebbesen & Brecht, 2017;Peters et al 2017a;Soteropoulos, 2018).…”

Section: Introductionmentioning

confidence: 99%

Non‐invasive assessment of superficial and deep layer circuits in human motor cortex

Kurz

Wiegel

et al. 2019

The Journal of Physiology

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Key points The first indirect (I) corticospinal volley from stimulation of the motor cortex consists of two parts: one that originates from infragranular layer 5 and a subsequent part with a delay of 0.6 ms to which supragranular layers contribute. Non‐invasive probing of these two parts was performed in humans using a refined electrophysiological method involving transcranial magnetic stimulation and peripheral nerve stimulation. Activity modulation of these two parts during a sensorimotor discrimination task was consistent with previous results in monkeys obtained with laminar recordings. Abstract Circuits in superficial and deep layers play distinct roles in cortical computation, but current methods to study them in humans are limited. Here, we developed a novel approach for non‐invasive assessment of layer‐specific activity in the human motor cortex. We first conducted brain slice and in vivo experiments on monkey motor cortex to investigate the output timing from layer 5 (including corticospinal neurons) following extracellular stimulation. Neuron responses contained cyclical waves. The first wave was composed of two parts: the earliest part originated only from stimulation of layer 5; after 0.6 ms, stimuli to superficial layers 2/3 could also contribute. In healthy humans we then assessed different parts of the first corticospinal volley elicited by transcranial magnetic stimulation (TMS), by interacting TMS with stimulation of the median nerve generating an H‐reflex. By adjusting the delay between stimuli, we could assess the earliest volley evoked by TMS, and the part 0.6 ms later. Measurements were made while subjects performed a visuo‐motor discrimination task, which has been previously shown in monkey to modulate superficial motor cortical cells selectively depending on task difficulty. We showed a similar selective modulation of the later part of the TMS volley, as expected if this part of the volley is sensitive to superficial cortical excitability. We conclude that it is possible to segregate different cortical circuits which may refer to different motor cortex layers in humans, by exploiting small time differences in the corticospinal volleys evoked by non‐invasive stimulation.

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Learning in the Rodent Motor Cortex

Cited by 123 publications

References 147 publications

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

Distinct roles for motor cortical and thalamic inputs to striatum during motor learning and execution

The dynamics of cortical GABA in human motor learning

Non‐invasive assessment of superficial and deep layer circuits in human motor cortex

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