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

2021 ◽  
Author(s):  
A. Giustiniani ◽  
V. Tarantino ◽  
M. Bracco ◽  
R. E. Bonaventura ◽  
M. Oliveri

AbstractAlthough 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.

2014 ◽  
Vol 111 (12) ◽  
pp. 2560-2569 ◽  
Author(s):  
Pranav Parikh ◽  
Marco Davare ◽  
Patrick McGurrin ◽  
Marco Santello

Control of digit forces for grasping relies on sensorimotor memory gained from prior experience with the same or similar objects and on online sensory feedback. However, little is known about neural mechanisms underlying digit force planning. We addressed this question by quantifying the temporal evolution of corticospinal excitability (CSE) using single-pulse transcranial magnetic stimulation (TMS) during two reach-to-grasp tasks. These tasks differed in terms of the magnitude of force exerted on the same points on the object to isolate digit force planning from reach and grasp planning. We also addressed the role of intracortical circuitry within primary motor cortex (M1) by quantifying the balance between short intracortical inhibition and facilitation using paired-pulse TMS on the same tasks. Eighteen right-handed subjects were visually cued to plan digit placement at predetermined locations on the object and subsequently to exert either negligible force (“low-force” task, LF) or 10% of their maximum pinch force (“high-force” task, HF) on the object. We found that the HF task elicited significantly smaller CSE than the LF task, but only when the TMS pulse coincided with the signal to initiate the reach. This force planning-related CSE modulation was specific to the muscles involved in the performance of both tasks. Interestingly, digit force planning did not result in modulation of M1 intracortical inhibitory and facilitatory circuitry. Our findings suggest that planning of digit forces reflected by CSE modulation starts well before object contact and appears to be driven by inputs from frontoparietal areas other than M1.


2010 ◽  
Vol 104 (5) ◽  
pp. 2603-2614 ◽  
Author(s):  
Michael A. Nitsche ◽  
Michaela Jakoubkova ◽  
Nivethida Thirugnanasambandam ◽  
Leonie Schmalfuss ◽  
Sandra Hullemann ◽  
...  

Motor learning and memory consolidation require the contribution of different cortices. For motor sequence learning, the primary motor cortex is involved primarily in its acquisition. Premotor areas might be important for consolidation. In accordance, modulation of cortical excitability via transcranial DC stimulation (tDCS) during learning affects performance when applied to the primary motor cortex, but not premotor cortex. We aimed to explore whether premotor tDCS influences task performance during motor memory consolidation. The impact of excitability-enhancing, -diminishing, or placebo premotor tDCS during rapid eye movement (REM) sleep on recall in the serial reaction time task (SRTT) was explored in healthy humans. The motor task was learned in the evening. Recall was performed immediately after tDCS or the following morning. In two separate control experiments, excitability-enhancing premotor tDCS was performed 4 h after task learning during daytime or immediately before conduction of a simple reaction time task. Excitability-enhancing tDCS performed during REM sleep increased recall of the learned movement sequences, when tested immediately after stimulation. REM density was enhanced by excitability-increasing tDCS and reduced by inhibitory tDCS, but did not correlate with task performance. In the control experiments, tDCS did not improve performance. We conclude that the premotor cortex is involved in motor memory consolidation during REM sleep.


PLoS ONE ◽  
2021 ◽  
Vol 16 (9) ◽  
pp. e0255815
Author(s):  
Lukas Schilberg ◽  
Sanne Ten Oever ◽  
Teresa Schuhmann ◽  
Alexander T. Sack

The evaluation of transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs) promises valuable information about fundamental brain related mechanisms and may serve as a diagnostic tool for clinical monitoring of therapeutic progress or surgery procedures. However, reports about spontaneous fluctuations of MEP amplitudes causing high intra-individual variability have led to increased concerns about the reliability of this measure. One possible cause for high variability of MEPs could be neuronal oscillatory activity, which reflects fluctuations of membrane potentials that systematically increase and decrease the excitability of neuronal networks. Here, we investigate the dependence of MEP amplitude on oscillation power and phase by combining the application of single pulse TMS over the primary motor cortex with concurrent recordings of electromyography and electroencephalography. Our results show that MEP amplitude is correlated to alpha phase, alpha power as well as beta phase. These findings may help explain corticospinal excitability fluctuations by highlighting the modulatory effect of alpha and beta phase on MEPs. In the future, controlling for such a causal relationship may allow for the development of new protocols, improve this method as a (diagnostic) tool and increase the specificity and efficacy of general TMS applications.


2021 ◽  
Author(s):  
Daniel Ramirez-Gordillo ◽  
Andrew A. Parra ◽  
K. Ulrich Bayer ◽  
Diego Restrepo

Learning and memory requires coordinated activity between different regions of the brain. Here we studied the interaction between medial prefrontal cortex (mPFC) and hippocampal dorsal CA1 during associative odorant discrimination learning in the mouse. We found that as the animal learns to discriminate odorants in a go-no go task the coupling of high frequency neural oscillations to the phase of theta oscillations (phase-amplitude coupling or PAC) changes in a manner that results in divergence between rewarded and unrewarded odorant-elicited changes in the theta-phase referenced power (tPRP) for beta and gamma oscillations. In addition, in the proficient animal there was a decrease in the coordinated oscillatory activity between CA1 and mPFC in the presence of the unrewarded odorant. Furthermore, the changes in PAC resulted in a marked increase in the accuracy for decoding odorant identity from tPRP when the animal became proficient. Finally, we studied the role of Ca2+/calmodulin-dependent protein kinase II α (CaMKIIα), a protein involved in learning and memory, in oscillatory neural processing in this task. We find that the accuracy for decoding the odorant identity from tPRP decreases in CaMKIIα knockout mice and that this accuracy correlates with behavioral performance. These results implicate a role for PAC and CaMKIIα in olfactory go-no go associative learning in the hippocampal-prefrontal circuit.


1998 ◽  
Vol 79 (2) ◽  
pp. 1070-1080 ◽  
Author(s):  
H. Boecker ◽  
A. Dagher ◽  
A. O. Ceballos-Baumann ◽  
R. E. Passingham ◽  
M. Samuel ◽  
...  

Boecker, H., A. Dagher, A. O. Ceballos-Baumann, R. E. Passingham, M. Samuel, K. J. Friston, J.-B. Poline, C. Dettmers, B. Conrad, and D. J. Brooks. Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. J. Neurophysiol. 79: 1070–1080, 1998. The aim of this study was to investigate the functional anatomy of distributed cortical and subcortical motor areas in the human brain that participate in the central control of overlearned complex sequential unimanual finger movements. On the basis of previous research in nonhuman primates, a principal involvement of basal ganglia (medial premotor loops) was predicted for central control of finger sequences performed automatically. In pertinent areas, a correlation of activation levels with the complexity of a motor sequence was hypothesized. H2 15O positron emission tomography (PET) was used in a group of seven healthy male volunteers [mean age 32.0 ± 10.4 yr] to determine brain regions where levels of regional cerebral blood flow (rCBF) correlated with graded complexity levels of five different key-press sequences. All sequences were overlearned before PET and involved key-presses of fingers II–V of the right hand. Movements of individual fingers were kept constant throughout all five conditions by external pacing at 1-Hz intervals. Positive correlations of rCBF with increasing sequence complexity were identified in the contralateral rostral supplementary motor area (pre-SMA) and the associated pallido-thalamic loop, as well as in right parietal area 7 and ipsilateral primary motor cortex (M1). In contrast, while rCBF in contralateral M1 and and extensive parts of caudal SMA was increased compared with rest during task performance, significant correlated increases of rCBF with sequence complexity were not observed. Inverse correlations of rCBF with increasing sequence complexity were identified in mesial prefrontal-, medial temporal-, and anterior cingulate areas. The findings provide further evidence in humans supporting the notion of a segregation of SMA into functionally distinct subcomponents: although pre-SMA was differentially activated depending on the complexity of a sequence of learned finger movements, such modulation was not detectable in caudal SMA (except the most antero-superior part), implicating a motor executive role. Our observations of complexity-correlated rCBF increases in anterior globus palllidus suggest a specific role for the basal ganglia in the process of sequence facilitation and control. They may act to filter and focus input from motor cortical areas as patterns of action become increasingly complex.


2013 ◽  
Vol 25 (10) ◽  
pp. 1634-1648 ◽  
Author(s):  
Julie Duque ◽  
Etienne Olivier ◽  
Matthew Rushworth

Top–down control is critical to select goal-directed actions in changeable environments, particularly when several conflicting options compete for selection. In humans, this control system is thought to involve an inhibitory mechanism that suppresses the motor representation of unwanted responses to favor selection of the most appropriate action. Here, we aimed to evaluate the role of a region of the medial frontal cortex, the pre-SMA, in this form of inhibition by using a double coil TMS protocol combining repetitive TMS (rTMS) over the pre-SMA and a single-pulse TMS over the primary motor cortex (M1) during a visuomotor task that required participants to choose between a left or right button press according to an imperative cue. M1 stimulation allowed us to assess changes in motor excitability related to selected and nonselected (unwanted) actions, and rTMS was used to produce transient disruption of pre-SMA functioning. We found that when rTMS was applied over pre-SMA, inhibition of the nonselected movement representation was reduced. Importantly, this effect was only observed when the imperative cue produced a substantial amount of competition between the response alternatives. These results are consistent with previous studies pointing to a role of pre-SMA in competition resolution. In addition, our findings indicate that this function of pre-SMA involves the control of inhibitory influences directed at unwanted action representations.


Author(s):  
Sebastian H. Bitzenhofer ◽  
Jastyn A. Pöpplau ◽  
Ileana L. Hanganu-Opatz

AbstractGamma oscillations are a prominent activity pattern in the cerebral cortex. While gamma rhythms have been extensively studied in the adult prefrontal cortex in the context of cognitive (dys)functions, little is known about their development. We addressed this issue by using extracellular recordings and optogenetic stimulations in mice across postnatal development. We show that fast rhythmic activity in the prefrontal cortex becomes prominent during the second postnatal week. While initially at about 15 Hz, fast oscillatory activity progressively accelerates with age and stabilizes within gamma frequency range (30-80 Hz) during the fourth postnatal week. Activation of layer 2/3 pyramidal neurons drives fast oscillations throughout development, yet the acceleration of their frequency follows similar temporal dynamics as the maturation of fast-spiking interneurons. These findings uncover the development of prefrontal gamma activity and provide a framework to examine the origin of abnormal gamma activity in neurodevelopmental disorders.


Neurosurgery ◽  
2019 ◽  
Vol 66 (Supplement_1) ◽  
Author(s):  
Doris D Wang ◽  
Coralie de Hemptinne ◽  
Svjetlana Miocinovic ◽  
Witney Chen ◽  
Jill L Ostrem ◽  
...  

Abstract INTRODUCTION In Parkinson's disease, the emergence of motor dysfunction is thought to be related to an imbalance between antikinetic and prokinetic patterns of oscillatory activity in the motor network. Invasive recordings from the basal ganglia and cortex in surgical patients have suggested that levodopa and therapeutic deep brain stimulation can suppress antikinetic beta band (13-30 Hz) rhythms while promoting prokinetic gamma band (60-90 Hz) rhythms. Surgical ablation of the globus pallidus internus is one of the oldest effective therapies for Parkinson's disease and gives a remarkable immediate relief from rigidity and bradykinesia, but its effects on oscillatory activity in the motor network have not been studied. We characterize the effects of pallidotomy on cortical oscillatory activity in Parkinson's disease patients. METHODS Using a temporary 6-contact lead placed over the sensorimotor cortex in the subdural space, we recorded acute changes in cortical oscillatory activities in 3 Parkinson's disease patients undergoing pallidotomy and compared the results to that of 3 essential tremor patients undergoing thalamotomy. RESULTS In all 3 Parkinson's disease patients, we observed the emergence of an approximately 70 to 80 Hz narrow-band oscillation with effective thermolesion of the pallidum. This gamma oscillatory activity was spatially localized over the primary motor cortex, was minimally affected by voluntary movements, and was not found in the motor cortex of essential tremor patients undergoing thalamotomy. CONCLUSION Our finding suggests that acute lesioning of the pallidum promotes cortical gamma band oscillations. This may represent an important mechanism for alleviating bradykinesia in Parkinson's disease.


2009 ◽  
Vol 101 (2) ◽  
pp. 789-802 ◽  
Author(s):  
M. Weinberger ◽  
W. D. Hutchison ◽  
A. M. Lozano ◽  
M. Hodaie ◽  
J. O. Dostrovsky

Rest tremor is one of the main symptoms in Parkinson's disease (PD), although in contrast to rigidity and akinesia, the severity of the tremor does not correlate well with the degree of dopamine deficiency or the progression of the disease. Studies suggest that akinesia in PD patients is related to abnormal increased beta (15–30 Hz) and decreased gamma (35–80 Hz) synchronous oscillatory activity in the basal ganglia. Here we investigated the dynamics of oscillatory activity in the subthalamic nucleus (STN) during tremor. We used two adjacent microelectrodes to simultaneously record neuronal firing and local field potential (LFP) activity in nine PD patients who exhibited resting tremor during functional neurosurgery. We found that neurons exhibiting oscillatory activity at tremor frequency are located in the dorsal region of STN, where neurons with beta oscillatory activity are observed, and that their activity is coherent with LFP oscillations in the beta frequency range. Interestingly, in 85% of the 58 sites examined, the LFP exhibited increased oscillatory activity in the low gamma frequency range (35–55 Hz) during periods with stronger tremor. Furthermore, in 17 of 26 cases where two LFPs were recorded simultaneously, their coherence in the gamma range increased with increased tremor. When averaged across subjects, the ratio of the beta to gamma coherence was significantly lower in periods with stronger tremor compared with periods of no or weak tremor. These results suggest that resting tremor in PD is associated with an altered balance between beta and gamma oscillations in the motor circuits of STN.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Yasuyuki Takamatsu ◽  
Satoko Koganemaru ◽  
Tatsunori Watanabe ◽  
Sumiya Shibata ◽  
Yoshihiro Yukawa ◽  
...  

AbstractTranscranial static magnetic stimulation (tSMS) has been focused as a new non-invasive brain stimulation, which can suppress the human cortical excitability just below the magnet. However, the non-regional effects of tSMS via brain network have been rarely studied so far. We investigated whether tSMS over the left primary motor cortex (M1) can facilitate the right M1 in healthy subjects, based on the hypothesis that the functional suppression of M1 can cause the paradoxical functional facilitation of the contralateral M1 via the reduction of interhemispheric inhibition (IHI) between the bilateral M1. This study was double-blind crossover trial. We measured the corticospinal excitability in both M1 and IHI from the left to right M1 by recording motor evoked potentials from first dorsal interosseous muscles using single-pulse and paired-pulse transcranial magnetic stimulation before and after the tSMS intervention for 30 min. We found that the corticospinal excitability of the left M1 decreased, while that of the right M1 increased after tSMS. Moreover, the evaluation of IHI revealed the reduced inhibition from the left to the right M1. Our findings provide new insights on the mechanistic understanding of neuromodulatory effects of tSMS in human.


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