Abstract
Motor skills are acquired and refined across alternating phases of practice (online) and subsequent consolidation in the absence of further skill execution (offline). Both stages of learning are sustained by dynamic interactions within a widespread motor learning network including the premotor and primary motor cortices. Here, we aimed to investigate the role of the dorsal premotor cortex (dPMC) and its interaction with the primary motor cortex (M1) during motor memory consolidation. Forty-eight healthy human participants (age 22.1 ± 3.1 years) were assigned to three different groups corresponding to either low-frequency (1 Hz) repetitive transcranial magnetic stimulation (rTMS) of left dPMC, rTMS of left M1, or sham rTMS. rTMS was applied immediately after explicit motor sequence training with the right hand. Motor evoked potentials were recorded before training and after rTMS to assess potential stimulation-induced changes in corticospinal excitability (CSE). Participants were retested on motor sequence performance after eight hours to assess consolidation. While rTMS of dPMC significantly increased CSE and rTMS of M1 significantly decreased CSE, no CSE modulation was induced by sham rTMS. However, all groups demonstrated similar significant offline learning indicating that consolidation was not modulated by the post-training low-frequency rTMS intervention despite evidence of an interaction of dPMC and M1 at the level of CSE. Motor memory consolidation ensuing explicit motor sequence training seems to be a rather robust process that is not affected by low-frequency rTMS-induced perturbations of dPMC or M1. Findings further indicate that consolidation of explicitly acquired motor skills is neither mediated nor reflected by post-training CSE.
Highlights
The acquisition of a new motor skill is a multi-staged process that evolves both “online”, concurrent with repeated skill execution, and “offline”, between training sessions[1,2]
Subsequent repeated measures analyses of variance (rmANOVA) showed that the significant interaction of Time x Group was driven by a significant decrease of the average MEPpost amplitude compared to the average MEPpre amplitude in the M1 repetitive transcranial magnetic stimulation (rTMS) group (− 0.337 mV, CI − 0.566 to − 0.109, Time: F(1,15) = 9.886, p = 0.007), while there was a significant motor evoked potentials (MEPs) amplitude increase in the dorsal premotor cortex (dPMC) rTMS group (+ 0.868 mV, CI 0.202–1.535; Time: F(1,15) = 7.706, p = 0.014), and no relevant change of corticospinal excitability (CSE) in the SHAM group (− 0.037 mV, CI − 0.486–0.412; Time: F(1,15) = 0.031, p = 0.863; Fig. 2)
As expected, post-training 1 Hz M1 rTMS significantly decreased the size of the MEP amplitudes, post-training 1 Hz rTMS of the dPMC significantly increased CSE compared to the pre-training assessment
Summary
The acquisition of a new motor skill is a multi-staged process that evolves both “online”, concurrent with repeated skill execution, and “offline”, between training sessions[1,2]. A large body of evidence shows that sequential motor skill acquisition is sustained by specific and temporally dynamic interactions between multiple nodes of a widespread neural network that—in addition to M1—encompasses secondary motor cortical areas, parietal areas, as well as basal ganglia, hippocampus, the cerebellum, and the spinal cord[9,10,11,12,13,14,15] Within this network, recent research has identified the dorsal premotor cortex (dPMC) as a region that (i) has been shown to modulate excitability and plasticity in M1 by interconnections[16,17,18,19], (ii) plays an important role in the process of online motor memory. If malleability of motor memory consolidation by offline NIBS of the dPMC and M1 proves to be a robust finding, it would be conceivable to explore its potential as a therapeutic tool to target and modulate motor memory consolidation in the future
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