Cerebellar transcranial alternating current stimulation in the gamma range applied during the acquisition of a novel motor skill

Wessel, Maximilian J.; Draaisma, Laurijn R.; Boer, Anne F. W. de; Park, Chang-Hyun; Maceira-Elvira, Pablo; Durand-Ruel, Manon; Koch, Philipp; Morishita, Takuya; Hummel, Friedhelm C.

doi:10.1038/s41598-020-68028-9

Cited by 37 publications

(37 citation statements)

References 65 publications

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“…Overall, the authors conclude that synchronizing the activity of cortical and cerebellar areas in the gamma frequency band affects explicit motor learning over a wide intervals of time (i.e., 1 day after learning). In a more recent study, 50 Hz left cerebellar tACS did not affect performance in an explicit motor learning task requiring the execution of a grip force to move a cursor [37]. The difference in montage and hand between this study (left cerebellum and non-dominant hand) and our study (right cerebellum and right hand) might account for the divergent results and suggests that the effects depend on the stimulated hemisphere.…”

Section: Discussioncontrasting

confidence: 85%

Functional Role of Cerebellar Gamma Frequency in Motor Sequences Learning: a tACS Study

et al. 2021

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Although the role of the cerebellum in motor sequences learning is widely established, the specific function of its gamma oscillatory activity still remains unclear. In the present study, gamma (50 Hz)—or delta (1 Hz)—transcranial alternating current stimulation (tACS) was applied to the right cerebellar cortex while participants performed an implicit serial reaction time task (SRTT) with their right hand. The task required the execution of motor sequences simultaneously with the presentation of a series of visual stimuli. The same sequence was repeated across multiple task blocks (from blocks 2 to 5 and from blocks 7 to 8), whereas in other blocks, new/pseudorandom sequences were reproduced (blocks 1 and 6). Task performance was examined before and during tACS. To test possible after-effects of cerebellar tACS on the contralateral primary motor cortex (M1), corticospinal excitability was assessed by examining the amplitude of motor potentials (MEP) evoked by single-pulse transcranial magnetic stimulation (TMS). Compared with delta stimulation, gamma-tACS applied during the SRTT impaired participants’ performance in blocks where the same motor sequence was repeated but not in blocks where the new pseudorandom sequences were presented. Noteworthy, the later assessed corticospinal excitability was not affected. These results suggest that cerebellar gamma oscillations mediate the implicit acquisition of motor sequences but do not affect task execution itself. Overall, this study provides evidence of a specific role of cerebellar gamma oscillatory activity in implicit motor learning.

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Section: Discussioncontrasting

confidence: 85%

Functional Role of Cerebellar Gamma Frequency in Motor Sequences Learning: a tACS Study

et al. 2021

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“…We suspect that the entrainment at this frequency neither alters the baseline firing rate of these neurons nor recruits further cerebellar neurons to respond to TMS. In support of this, recent work showed that 50Hz cerebellar tACS did not enhance motor skill learning or retention when compared to sham stimulation [63], thus it could be argued that this frequency is suboptimal for facilitating processes that are involved in motor skill learning. Contrary to this, Naro and colleagues found that 50 Hz tACS reduced CBI and improved the performance of a sequential tapping motor task [27].…”

Section: Discussionmentioning

confidence: 95%

Frequency-dependent modulation of cerebellar excitability during the application of non-invasive alternating current stimulation

et al. 2021

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Background: it is well-known that the cerebellum is critical for the integrity of motor and cognitive actions. Applying non-invasive brain stimulation techniques over this region results in neurophysiological and behavioural changes, which have been associated with the modulation of cerebellar-cerebral cortex connectivity. Here, we investigated whether online application of cerebellar transcranial alternating current stimulation (tACS) results in changes to this pathway. Methods: thirteen healthy individuals participated in two sessions of cerebellar tACS delivered at different frequencies (5Hz and 50Hz). We used transcranial magnetic stimulation to measure cerebellarmotor cortex (M1) inhibition (CBI), short-intracortical inhibition (SICI) and short-afferent inhibition (SAI) before, during and after the application of tACS. Results: we found that CBI was specifically strengthened during the application of 5Hz cerebellar tACS. No changes were detected immediately following the application of 5Hz stimulation, nor at any time point with 50Hz stimulation. We also found no changes to M1 intracortical circuits (i.e. SICI) or sensorimotor interaction (i.e. SAI), indicating that the effects of 5Hz tACS over the cerebellum are site-specific. Conclusions: cerebellar tACS can modulate cerebellar excitability in a time-and frequency-dependent manner. Additionally, cerebellar tACS does not appear to induce any long-lasting effects (i.e. plasticity), suggesting that stimulation enhances oscillations within the cerebellum only throughout the stimulation period. As such, cerebellar tACS may have significant implications for diseases manifesting with abnormal cerebellar oscillatory activity and also for future behavioural studies.

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“…However, no clear association with behaviour (training gain) was present. It is important to note, that when applying other tasks and stimulation paradigms no effect of training phase 58 or opposite tendencies 59 on SICI move modulation have been reported. In future work, it would be interesting to also study additional aspects of neurotransmission with TMS-based techniques for instance assessing long-interval intercortical inhibition (LICI—GABA B -ergic) or short-latency afferent inhibition (SAI—acetylcholinergic) to disentangle potential other underlying mechanisms of tDCS and motor learning 18 .…”

Section: Discussionmentioning

confidence: 91%

Multifocal stimulation of the cerebro-cerebellar loop during the acquisition of a novel motor skill

Wessel

Park

Beanato

et al. 2021

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Transcranial direct current stimulation (tDCS)-based interventions for augmenting motor learning are gaining interest in systems neuroscience and clinical research. Current approaches focus largely on monofocal motorcortical stimulation. Innovative stimulation protocols, accounting for motor learning related brain network interactions also, may further enhance effect sizes. Here, we tested different stimulation approaches targeting the cerebro-cerebellar loop. Forty young, healthy participants trained a fine motor skill with concurrent tDCS in four sessions over two days, testing the following conditions: (1) monofocal motorcortical, (2) sham, (3) monofocal cerebellar, or (4) sequential multifocal motorcortico-cerebellar stimulation in a double-blind, parallel design. Skill retention was assessed after circa 10 and 20 days. Furthermore, potential underlying mechanisms were studied, applying paired-pulse transcranial magnetic stimulation and multimodal magnetic resonance imaging-based techniques. Multisession motorcortical stimulation facilitated skill acquisition, when compared with sham. The data failed to reveal beneficial effects of monofocal cerebellar or additive effects of sequential multifocal motorcortico-cerebellar stimulation. Multimodal multiple linear regression modelling identified baseline task performance and structural integrity of the bilateral superior cerebellar peduncle as the most influential predictors for training success. Multisession application of motorcortical tDCS in several daily sessions may further boost motor training efficiency. This has potential implications for future rehabilitation trials.

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Cerebellar transcranial alternating current stimulation in the gamma range applied during the acquisition of a novel motor skill

Cited by 37 publications

References 65 publications

Functional Role of Cerebellar Gamma Frequency in Motor Sequences Learning: a tACS Study

Functional Role of Cerebellar Gamma Frequency in Motor Sequences Learning: a tACS Study

Frequency-dependent modulation of cerebellar excitability during the application of non-invasive alternating current stimulation

Multifocal stimulation of the cerebro-cerebellar loop during the acquisition of a novel motor skill

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