Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills

Pascual‐Leone, Álvaro; Nguyet, D.; Cohen, Leonardo G.; Brasil‐Neto, Joaquim P.; Cammarota, Angel; Hallett, Mark

doi:10.1152/jn.1995.74.3.1037

Cited by 1,166 publications

(823 citation statements)

References 42 publications

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“…The finding of increased activation in M1 following sleep is supportive of our original hypothesis, and extends previous investigations of motor skill learning following continued practice but over much greater time periods (multiple days to weeks not concerning sleep) (Karni et al, 1995;Pascual-Leone et al, 1995;Penhune and Doyon, 2002). Based on these data, it seems reasonable to hypothesize that delayed/off-line motor skill learning is associated with increased functional activity and/or an expansion of the cortical representation in M1 (Ungerleider et al, 2002), and our findings indicate that sleep plays a fundamental role in the evolution of such plastic changes.…”

Section: Discussionsupporting

confidence: 88%

“…These reports have described increased activity or responsiveness in the primary motor cortex (M1), and to a lesser extent, the pre-motor cortex, basal ganglia and cerebellum (Karni et al, 1995;Pascual-Leone et al, 1995;Penhune and Doyon, 2002). Enhanced motor skill learning has also been associated with signal decreases throughout the parietal cortex, thought to reflect automaticity of performance as skill level improves (Seitz et al, 1990;Toni et al, 1998;Muller et al, 2002;Sakai et al, 2002).…”

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confidence: 99%

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Sleep-dependent motor memory plasticity in the human brain

et al. 2005

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Abstract-Growing evidence indicates a role for sleep in off-line memory processing, specifically in post-training consolidation. In humans, sleep has been shown to trigger overnight learning on a motor-sequence memory task, while equivalent waking periods produce no such improvement. But while the behavioral characteristics of sleep-dependent motor learning become increasingly well characterized, the underlying neural basis remains unknown. Here we present functional magnetic resonance imaging data demonstrating a change in the representation of a motor memory after a night of sleep. Subjects trained on a motor-skill memory and 12 hours later, after either sleep or wake, were retested during functional magnetic resonance imaging. Following sleep relative to wake, regions of increased activation were expressed in the right primary motor cortex, medial prefrontal lobe, hippocampus and left cerebellum; changes that can support faster motor output and more precise mapping of key-press movements. In contrast, signal decreases were identified in parietal cortices, the left insular cortex, temporal pole and fronto-polar region, reflecting a reduced need for conscious spatial monitoring and a decreased emotional task burden. This evidence of an overnight, systems- A large body of evidence, spanning a wide range of neuroscientific disciplines, now describes evidence of sleepdependent learning in both humans and animals , already complemented by cellular and molecular models of sleep-dependent plasticity (Graves et al., 2001;Tononi and Cirelli, 2001;Benington and Frank, 2003). In particular, sleep has been implicated in the ongoing process of consolidation, following initial memory acquisition.Within the procedural memory domain, sleep in humans has been shown to trigger significant overnight learning enhancements, whereby performance is selectively improved across sleeping intervals, while equivalent waking periods confer no such performance benefit (for reviews see Walker, in press). Demonstrations of overnight, sleep-dependent learning have now been reported across both sensory (Karni et al., 1994;Gais et al., 2000; Stickgold et al., 2000a,b;Fenn et al., 2003;Atienza et al., 2004;Gaab et al., 2004) Regarding motor-sequence learning, Walker et al. (2002, 2003a,b) have shown that a night of sleep can trigger significant improvements in both performance speed and accuracy on a finger-tapping task, while equivalent periods of time awake do not result in any such learning enhancements. Furthermore, these overnight learning gains correlated with the amount of stage two non-rapid eye movement (NREM) sleep, particularly late in the night (Walker et al., 2002). Adding to these findings, it also appears that there is no transfer of sleep-dependent procedural learning to either new motor sequences, or to performance of the same sequence using the opposite hand (Fischer et al., 2002;Korman et al., 2003), suggesting that the influence of sleep is highly specific. But while the behavioral characteristics of sleep-dependent motor...

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Section: Discussionsupporting

confidence: 88%

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confidence: 99%

Sleep-dependent motor memory plasticity in the human brain

et al. 2005

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“…Learning new motor skills (Pascual-Leone et al, 1995) and performing skilled motor activities result in an expansion of the representation of the muscles involved in the task. Complete long term sensorimotor deafferentation, as in the case of limb amputation (Chen et al, 1998;Cohen et al, 1991;Kew et al, 1994;Ridding and Rothwell, 1997;Wu and Kaas, 1999) and peripheral nerve lesions (Rijntjes et al, 1997;Tinazzi et al, 1998), as well as short term deafferentation secondary to ischemic nerve block (Brasil-Neto et al, 1993;Ridding and Rothwell, 1997;Ziemann et al, 1998a;Ziemann et al, 1998b), result in an expansion of the surrounding representations.…”

Section: Introductionmentioning

confidence: 99%

Modulation of motor cortex excitability after upper limb immobilization

Zanette

Manganotti

Fiaschi

et al. 2004

Clinical Neurophysiology

102

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Objective: To examine the mechanisms of disuse-induced plasticity following long-term limb immobilization. Methods: We studied 9 subjects, who underwent left upper limb immobilization for unilateral wrist fractures. All subjects were examined immediately after splint removal. Cortical motor maps, resting motor threshold (RMT), motor evoked potential (MEP) latency and MEP recruitment curves were studied from abductor pollicis brevis (APB) and flexor carpi radialis (FCR) muscles with single pulse transcranial magnetic stimulation (TMS). Paired pulse TMS was used to study intracortical inhibition and facilitation. Compound muscle action potentials (CMAPs) and F waves were obtained after median nerve stimulation. In 4/9 subjects the recording was repeated after 35 -41 days.Results: CMAP amplitude and RMT were reduced in APB muscle on the immobilized sides in comparison to the non-immobilized sides and controls after splint removal. CMAP amplitude and RMT were unchanged in FCR muscle. MEP latency and F waves were unchanged. MEP recruitment was significantly greater on the immobilized side at rest, but the asymmetry disappeared during voluntary muscle contraction. Paired pulse TMS showed an imbalance between inhibitory and excitatory networks, with a prevalence of excitation on the immobilized sides. A slight, non-significant change in the strength of corticospinal projections to the non-immobilized sides was found. TMS parameters were not correlated with hand dexterity. These abnormalities were largely normalized at the time of retesting in the four patients who were followed-up.Conclusions: Hyperexcitability occurs within the representation of single muscles, associated with changes in RMT and with an imbalance between intracortical inhibition and facilitation. These findings may be related to changes in the sensory input from the immobilized upper limb and/or in the discharge properties of the motor units.Significance: Different mechanisms may contribute to the reversible neuroplastic changes, which occur in response to long-term immobilization of the upper-limbs.

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“…At the level of cortical physiology, motor learning induces an enlargement of the motor-cortical representation (motor maps) of the body-parts that became trained. This phenomenon can be observed in rodents, primates, and humans (Kleim, Barbay, and Nudo, 1998;Nudo, Milliken, Jenkins, and Merzenich, 1996;Pascual-Leone, Nguyet, Cohen, Brasil-Neto, Cammarota, and Hallett, 1995). This enlargement is learning specific as it does not occur in response to mere motor activation and its magnitude is proportional to learning success (Kleim, Hogg, VandenBerg, Cooper, Bruneau, and Remple, 2004;Molina-Luna, Hertler, Buitrago, and Luft, 2008).…”

Section: Introductionmentioning

confidence: 88%

Temporal course of gene expression during motor memory formation in primary motor cortex of rats

Hertler

Buitrago

Luft

et al. 2016

Neurobiology of Learning and Memory

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Motor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that depends on changes in gene expression. Here, we investigate the temporal profile of these changes during motor memory formation in response to a skilled reaching task in rats. mRNA-levels were measured 1h, 7h and 24h after the end of a training session using microarray technique. To assure learning specificity, trained animals were compared to a control group. In response to motor learning, genes are sequentially regulated with high time-point specificity and a shift from initial suppression to later activation. The majority of regulated genes can be linked to learning-related plasticity. In the gene-expression cascade following motor learning, three different steps can be defined: (1) an initial suppression of genes influencing gene transcription. (2) Expression of genes that support translation of mRNA in defined compartments. (3) Expression of genes that immediately mediates plastic changes. Gene expression peaks after 24h -this is a much slower time-course when compared to hippocampusdependent learning, where peaks of gene-expression can be observed 6-12h after training ended. AbstractMotor learning is associated with plastic reorganization of neural networks in primary motor cortex (M1) that depends on changes in gene expression. Here, we investigate the temporal profile of these changes during motor memory formation in response to a skilled reaching task in rats. mRNA-levels were measured 1h, 7h and 24h after the end of a training session using microarray technique. To assure learning specificity, trained animals were compared to a control group. In response to motor learning, genes are sequentially regulated with high time-point specificity and a shift from initial suppression to later activation. The majority of regulated genes can be linked to learning-related plasticity. In the gene-expression cascade following motor learning, three different steps can be defined: 1) an initial suppression of genes influencing gene transcription. 2) Expression of genes that support translation of mRNA in defined compartments. 3) Expression of genes that immediately mediates plastic changes. Gene expression peaks after 24 hours -this is a much slower time-course when compared to hippocampus-dependent learning, where peaks of geneexpression can be observed 6 to 12 hours after training ended.3

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Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills

Cited by 1,166 publications

References 42 publications

Sleep-dependent motor memory plasticity in the human brain

Sleep-dependent motor memory plasticity in the human brain

Modulation of motor cortex excitability after upper limb immobilization

Temporal course of gene expression during motor memory formation in primary motor cortex of rats

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