Selective Suppression of Local Circuits during Movement Preparation in the Mouse Motor Cortex

Hasegawa, Masashi; Majima, Kei; Itokazu, Takahide; Maki, Takakuni; Albrecht, Urban Raphael; Castner, Nora; Izumo, Mariko; Sohya, Kazuhiro; Sato, Tatsuo K.; Kamitani, Yukiyasu; Satō, Takashi

doi:10.1016/j.celrep.2017.02.043

Cited by 36 publications

(38 citation statements)

References 37 publications

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“…That is, stronger levels of suppression were predictive of faster initiation times in the very same trials. This is coherent with the view that action preparation is an essential part of motor behavior, with relative changes in preparatory activity/suppression being a key determinant of the efficiency of ensuing action initiation (Hasegawa et al, 2017; Hannah et al, 2018). Notably though, we found such relationship when considering the non-selected prime-mover but not the selected one, possibly because MEPs in the latter effector reflect many overlapping inputs during response preparation (Duque and Ivry, 2009), an aspect that may have precluded us from observing a trial-by-trial link with behavior.…”

Section: Discussionsupporting

confidence: 86%

“…In conclusion, our data indicate that RTs depend on preparatory suppression in the non-selected prime-mover and that this link emerges mainly after a period of practice, at Training late . Interestingly, these results suggest that the dependency of RTs on preparatory activity reported in single-neuron studies (Churchland et al, 2006; Afshar et al, 2011; Michaels et al, 2015; Hasegawa et al, 2017) and more recently in TMS work (Hannah et al, 2018) may have been mainly shaped by data considered at a later training stage.…”

Section: Resultsmentioning

confidence: 78%

“…From this dynamical point of view, training may allow tuning the dynamics of preparatory activity, bringing it closer to an optimal state for action initiation (Vyas et al, 2018). In this line, strengthening of preparatory suppression would facilitate action initiation by allowing excitatory inputs targeting the selected motor representation to better stand out against a quiescent background, ultimately speeding up RTs (Hasbroucq et al, 1997; Greenhouse et al, 2015; Hasegawa et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…This view is supported by studies showing that the amount of preparatory suppression scales with the complexity of selection processes (Klein et al, 2014; Duque et al, 2016). Interestingly, another hypothesis in the field is that preparatory suppression could reflect a form of neural inhibition easing action initiation (Greenhouse et al, 2015; Hasegawa et al, 2017). This proposition was supported by the results of a study showing a dependence of RTs on the amount of preparatory suppression on a trial-by-trial basis: the stronger the preparatory suppression, the faster the initiation of the ensuing movement (Hannah et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Motor training strengthens corticospinal suppression during movement preparation

Vassiliadis

Derosière

Grandjean

et al. 2020

Preprint

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46Motor training improves the efficiency of trained movements and modifies neural activity 47 at rest and during motor execution. Training may also shape preparatory processes but the neural 48 correlates and the potential behavioral relevance of changes at the level of action preparation 49 remain unclear. In humans, transcranial magnetic stimulation (TMS) studies have shown that 50 movement preparation is accompanied by a suppression of corticospinal (CS) excitability relative 51 to a baseline measure; a phenomenon called preparatory suppression. Here, we trained participants 52 to initiate quick movements in an instructed-delay reaction time (RT) task and investigated resting 53 CS excitability as well as preparatory suppression over the practice blocks. We found that training 54 speeds up motor initiation, with no repercussion on error rates. Moreover, training increased 55 baseline CS excitability and deepened preparatory suppression. Importantly, training-related 56 changes in preparatory suppression were correlated to behavioral improvements: the subjects who 57 showed a stronger expansion of preparatory suppression were also those exhibiting larger gains in 58 RTs. Finally, in line with previous data, we observed a trial-by-trial relationship between the 59 amount of preparatory suppression and the subsequent RT: subjects responded faster on trials with 60 more preparatory suppression. Strikingly though, such a dependency of RTs on preparatory 61 suppression was tuned by the amount of training performed: while it was not evident early on, the 62 link emerged during the later practice blocks. Overall, our data indicate that training induces 63 changes in motor preparatory processes that are linked to an enhanced ability to initiate fast 64 movements. 65 66 67 3 Significance statement 68 69 Any movement is preceded by a period of preparation which involves significant changes 70 in the activity of the motor system, including a broad suppression of the corticospinal output 71 pathway, commonly referred to as preparatory suppression in human studies. Whether training can 72 alter such preparatory activity is unknown. Here, we show that motor training leads to a 73 strengthening of preparatory suppression in an instructed-delay reaction time (RT) task, and that 74 such change is related to a shortening of RTs. Moreover, at the single-trial level, we observed a 75 dependency of RTs on preparatory suppression which developed over training: the stronger the 76 preparatory suppression, the faster the RT. These results indicate that motor training can alter 77 motor preparatory activity in a behaviorally-relevant manner. 78 79 80 4 1. Introduction 81 82 Motor training generally improves the speed and/or accuracy at which movements are 83 selected, initiated and executed. A great deal of research has been devoted to unveiling the 84 functional changes at the basis of such improvements (Krakauer et al., 2019). At the neural level, 85 neuroimaging (e.g., Wiestler and Diedrichsen, 2013; Wenger et al., 2017; Yokoi and D...

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Section: Discussionsupporting

confidence: 86%

Section: Resultsmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Motor training strengthens corticospinal suppression during movement preparation

Vassiliadis

Derosière

Grandjean

et al. 2020

Preprint

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show abstract

“…To calculate the trial-to-trial correlation of the population activity, traces of z -scored inferred spike events of movement-related neurons during the movement-related period were realigned to a matrix with dimensions of cells × time × trials. We used z -scored activity of each neuron to avoid the effect of possible outliers, such as neurons with exceptionally high activity rate 41,43,64,65 . The time dimension of this array was then averaged to generate a trial-to-trial population activity matrix and used to calculate a trial-to-trial population activity correlation coefficient (population activity CC).…”

Section: Methodsmentioning

confidence: 99%

Super-wide-field two-photon imaging with a micro-optical device moving in post-objective space

et al. 2018

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Wide-field imaging of neural activity at a cellular resolution is a current challenge in neuroscience. To address this issue, wide-field two-photon microscopy has been developed; however, the field size is limited by the objective size. Here, we develop a micro-opto-mechanical device that rotates within the post-objective space between the objective and brain tissue. Two-photon microscopy with this device enables sub-second sequential calcium imaging of left and right mouse sensory forelimb areas 6 mm apart. When imaging the rostral and caudal motor forelimb areas (RFA and CFA) 2 mm apart, we found high pairwise correlations in spontaneous activity between RFA and CFA neurons and between an RFA neuron and its putative axons in CFA. While mice performed a sound-triggered forelimb-movement task, the population activity between RFA and CFA covaried across trials, although the field-averaged activity was similar across trials. The micro-opto-mechanical device in the post-objective space provides a novel and flexible design to clarify the correlation structure between distant brain areas at subcellular and population levels.

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Corticospinal Suppression Underlying Intact Movement Preparation Fades in Parkinson's Disease

et al. 2022

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Background In Parkinson's disease (PD), neurophysiological abnormalities within the primary motor cortex (M1) have been shown to contribute to bradykinesia, but exact modalities are still uncertain. We propose that such motor slowness could involve alterations in mechanisms underlying movement preparation, especially the suppression of corticospinal excitability—called “preparatory suppression”—which is considered to propel movement execution by increasing motor neural gain in healthy individuals. Methods On two consecutive days, 29 PD patients (on and off medication) and 29 matched healthy controls (HCs) underwent transcranial magnetic stimulation over M1, eliciting motor‐evoked potentials (MEPs) in targeted hand muscles, while they were either at rest or preparing a left‐ or right‐hand response in an instructed‐delay choice reaction time task. Preparatory suppression was assessed by expressing MEP amplitudes during movement preparation relative to rest. Results Contrary to HCs, PD patients showed a lack of preparatory suppression when the side of the responding hand was analyzed, especially when the latter was the most affected one. This deficit, which did not depend on dopamine medication, increased with disease duration and also tended to correlate with motor impairment, as measured by the Movement Disorder Society Unified Parkinson's Disease Rating Scale, Part III (both total and bradykinesia scores). Conclusions Our novel findings indicate that preparatory suppression fades in PD, in parallel with worsening motor symptoms, including bradykinesia. Such results suggest that an alteration in this marker of intact movement preparation could indeed cause motor slowness and support its use in future studies on the relation between M1 alterations and motor impairment in PD. © 2022 International Parkinson and Movement Disorder Society.

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Selective Suppression of Local Circuits during Movement Preparation in the Mouse Motor Cortex

Cited by 36 publications

References 37 publications

Motor training strengthens corticospinal suppression during movement preparation

Motor training strengthens corticospinal suppression during movement preparation

Super-wide-field two-photon imaging with a micro-optical device moving in post-objective space

Corticospinal Suppression Underlying Intact Movement Preparation Fades in Parkinson's Disease

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