The Neuronal Basis of Long-Term Sensorimotor Learning

Mandelblat-Cerf, Yael; Novick, Itai; Paz, Rony; Link, Yuval; Freeman, Sharon; Vaadia, Eilon

doi:10.1523/jneurosci.4055-10.2011

Cited by 37 publications

(30 citation statements)

References 51 publications

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“…There is consistent evidence from animal and human studies that M1 plays a central role in the long-term retention of motor skills following multisession training (Mandelblat-Cerf et al, 2011;Matsuzaka, Picard, & Strick, 2007;Floyer-Lea & Matthews, 2005;Kleim et al, 2004;Penhune & Doyon, 2002;Karni et al, 1995Karni et al, , 1998Kleim, Barbay, & Nudo, 1998;Nudo, Milliken, Jenkins, & Merzenich, 1996). Moreover, it has been recently shown that extended practice of the motor skill stabilizes the M1 activity pattern (Huang et al, 2013) and is associated with reduced metabolic activity in M1 (Picard, Matsuzaka, & Strick, 2013).…”

Section: Discussionmentioning

confidence: 87%

Done That: Short-term Repetition Related Modulations of Motor Cortex Activity as a Stable Signature for Overnight Motor Memory Consolidation

Gabitov

Manor

Karni

2014

Journal of Cognitive Neuroscience

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An almost universally accepted tacit expectation is that learning and memory consolidation processes must be reflected in the average brain activity in brain areas relevant to task performance. Motor cortex (M1) plasticity has been implicated in motor skill acquisition and its consolidation. Nevertheless, no consistent pattern of changes in the average signal, related to motor learning or motor memory consolidation following a single session of training, has emerged from imaging studies. Here we show that the pattern and magnitude of short-term brain activity modulations in response to task repetition, in M1, may provide a robust signature for effective motor memory consolidation processes. We studied participants during the paced performance of a finger-to-thumb opposition sequence (FOS), intensively trained a day earlier, and a similarly constructed untrained FOS. In addition to within-session "on-line" gains, most participants expressed delayed, consolidation-phase gains in the performance of the trained FOS. The execution of the trained FOS induced repetition enhancements in the contralateral M1 and bilaterally in the medial-temporal lobes, offsetting novelty-related repetition suppression effects. Moreover, the M1 modulations were positively correlated with the magnitude of each participant's overnight delayed gains but not with absolute performance levels. Our results suggest that short-term enhancements of brain signals upon task repetition reflect the effectiveness of overnight motor memory consolidation. We propose that procedural memory consolidation processes may affect the excitation-inhibition balance within cortical representations of the trained movements; this new balance is better reflected in repetition effects than in the average level of evoked neural activity.

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Section: Discussionmentioning

confidence: 87%

Done That: Short-term Repetition Related Modulations of Motor Cortex Activity as a Stable Signature for Overnight Motor Memory Consolidation

Gabitov

Manor

Karni

2014

Journal of Cognitive Neuroscience

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“…Therefore, we also expressed M1 activity in terms of the dynamics of the “motor plan”, using an approach developed by Mandelblat-Cerf, et al (Mandelblat-Cerf et al 2011). Briefly, during the window between movement onset and peak speed, we used endpoint velocity to compute the underlying CF force, which we subtracted from the force recorded by the force transducer.…”

Section: Resultsmentioning

confidence: 99%

Altered tuning in primary motor cortex does not account for behavioral adaptation during force field learning

Perich¹,

Miller

2017

Exp Brain Res

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Although primary motor cortex (M1) is intimately involved in the dynamics of limb movement, its inputs may be more closely related to higher order aspects of movement and multi-modal sensory feedback. Motor learning is thought to result from the adaption of internal models that compute transformations between these representations. While the psychophysics of motor learning has been studied in many experiments, the particular role of M1 in the process remains the subject of debate. Studies of learning-related changes in the spatial tuning of M1 neurons have yielded conflicting results. To resolve the discrepancies, we recorded from M1 during curl field adaptation in a reaching task. Our results suggest that aside from the addition of the load itself, the relation of M1 to movement dynamics remains unchanged as monkeys adapt behaviorally. Accordingly, we implemented a musculoskeletal model to generate synthetic neural activity having a fixed dynamical relation to movement and showed that these simulated neurons reproduced the observed behavior of the recorded M1 neurons. The stable representation of movement dynamics in M1 suggests that behavioral changes are mediated through progressively altered recruitment of M1 neurons, while the output effect of those neurons remain largely unchanged.

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“…The Arce et al paradigm of one-direction force-field learning was recently used, in conjunction with chronic recording arrays, to study correlates of long-term adaptation across five daily sessions (Mandelblat-Cerf et al 2011). Although recordings of the same neurons across sessions were not specifically sought out or analyzed, the chronic ensemble results of Mandelblat-Cerf et al are certainly relevant to our study.…”

Section: Discussionmentioning

confidence: 99%

Activity of the same motor cortex neurons during repeated experience with perturbed movement dynamics

Richardson

Borghi

Bizzi

2012

Journal of Neurophysiology

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Neurons in the primary motor cortex (M1) have been shown to have persistent, memory-like activity following adaptation to altered movement dynamics. However, the techniques used to study these memory traces limited recordings to only single sessions lasting no more than a few hours. Here, chronically implanted microelectrode arrays were used to study the long-term neuronal responses to repeated experience with perturbing, velocity-dependent force fields. Force-field-related neuronal activity within each session was similar to that found previously. That is, the directional tuning curves of the M1 neurons shifted in a manner appropriate to compensate for the forces. Next, the across-session behavior was examined. Long-term learning was evident in the performance improvements across multiple force-field sessions. Correlated with this change, the neuronal population had smaller within-session spike rate changes as experience with the force field increased. The smaller within-session changes were a result of persistent across-session shifts in directional tuning. The results extend the observation of memory traces of newly learned dynamics and provide further evidence for the role of M1 in early motor memory formation.

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The Neuronal Basis of Long-Term Sensorimotor Learning

Cited by 37 publications

References 51 publications

Done That: Short-term Repetition Related Modulations of Motor Cortex Activity as a Stable Signature for Overnight Motor Memory Consolidation

Done That: Short-term Repetition Related Modulations of Motor Cortex Activity as a Stable Signature for Overnight Motor Memory Consolidation

Altered tuning in primary motor cortex does not account for behavioral adaptation during force field learning

Activity of the same motor cortex neurons during repeated experience with perturbed movement dynamics

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