Effects of low-gamma tACS on primary motor cortex in implicit motor learning

In the primary motor cortex (M1), rhythmic activity in the gamma frequency band has been found during movement planning, onset and execution. Although the role of high-gamma oscillatory activity in M1 is well established, the contribution of low-gamma activity is still unexplored. In this study, transcranial alternating current stimulation (tACS) was used with the aim to specifically modulate low-gamma frequency band in M1, during an implicit motor learning task. A 40 Hz-tACS was applied over the left M1 while participants performed a serial reaction time task (SRTT) using their right hand. The task required the repetitive execution of sequential movements in response to sequences of visual stimuli. Sequential blocks were interleaved by a random block, which served as interference to sequence learning. Sham and 1 Hz tACS were used as control. Task performance was examined before, during and after tACS (pre-, online- and post-phase, respectively). Furthermore, cortical reactivity of M1 was assessed in the pre- and post-tACS phases, by measuring motor-evoked potentials (MEPs) elicited by single-pulse transcranial magnetic stimulation (TMS). Compared to sham and pre-tACS, the 40 Hz stimulation applied during SRTT slowed down response times in blocks that required retrieving previously learned sequences, after performing the random block. In addition, M1 cortical reactivity was selectively inhibited following 40 Hz-tACS, as quantified by reduced MEP amplitude. These results show that low-gamma tACS delivered over M1 during motor learning enhanced susceptibility to interference generated by the random sequence (i.e., proactive interference effect). Importantly, only low-gamma stimulation produced long-lasting effects on M1 cortical reactivity.

[1]  S. Lisanby,et al.  Pulse width dependence of motor threshold and input–output curve characterized with controllable pulse parameter transcranial magnetic stimulation , 2013, Clinical Neurophysiology.

[2]  Martin Meyer,et al.  Transcranial Alternating Current Stimulation (tACS) differentially modulates speech perception in young and older adults , 2016, Brain Stimulation.

[3]  Martin Meyer,et al.  40Hz-Transcranial alternating current stimulation (tACS) selectively modulates speech perception. , 2016, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[5]  S. Yazawa,et al.  Modulation of Motor Learning Capacity by Transcranial Alternating Current Stimulation , 2018, Neuroscience.

[6]  Paul Ferrari,et al.  MEG studies of motor cortex gamma oscillations: evidence for a gamma “fingerprint” in the brain? , 2013, Front. Hum. Neurosci..

[7]  C. Capaday,et al.  Input-output properties and gain changes in the human corticospinal pathway , 1997, Experimental Brain Research.

[8]  Catharina Zich,et al.  Motor Cortical Gamma Oscillations: What Have We Learnt and Where Are We Headed? , 2018, Current Behavioral Neuroscience Reports.

[9]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[10]  F. Fröhlich,et al.  Transcranial Alternating Current Stimulation Modulates Large-Scale Cortical Network Activity by Network Resonance , 2013, The Journal of Neuroscience.

[11]  Per B. Brockhoff,et al.  lmerTest Package: Tests in Linear Mixed Effects Models , 2017 .

[12]  M. Oliveri,et al.  Relationship between physiological excitatory and inhibitory measures of excitability in the left vs. right human motor cortex and peripheral electrodermal activity , 2017, Neuroscience Letters.

[13]  Suresh D Muthukumaraswamy,et al.  Functional properties of human primary motor cortex gamma oscillations. , 2010, Journal of neurophysiology.

[14]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[15]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[16]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[17]  J. Krakauer,et al.  Are We Ready for a Natural History of Motor Learning? , 2011, Neuron.

[18]  G. Ojemann,et al.  Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks , 1999, Clinical Neurophysiology.

[19]  Rosalind J. Sadleir,et al.  Transcranial direct current stimulation (tDCS) in a realistic head model , 2010, NeuroImage.

[20]  Christa Neuper,et al.  40-Hz oscillations during motor behavior in man , 1993, Neuroscience Letters.

[21]  Tipu Z. Aziz,et al.  Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance , 2012, Current Biology.

[22]  P. Brown,et al.  Driving Human Motor Cortical Oscillations Leads to Behaviorally Relevant Changes in Local GABAA Inhibition: A tACS-TMS Study , 2017, Clinical Neurophysiology.

[23]  M. Hallett,et al.  Modulation of cortical motor output maps during development of implicit and explicit knowledge. , 1994, Science.

[24]  C. Herrmann,et al.  Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states , 2013, Front. Hum. Neurosci..

[25]  P. Matthews,et al.  Polarity and timing-dependent effects of transcranial direct current stimulation in explicit motor learning , 2011, Neuropsychologia.

[26]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[27]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[28]  G. Pfurtscheller,et al.  Simultaneous EEG 10 Hz desynchronization and 40 Hz synchronization during finger movements. , 1992, Neuroreport.

[29]  A. Antal,et al.  Investigating Neuroplastic Changes in the Human Brain Induced by Transcranial Direct (tDCS) and Alternating Current (tACS) Stimulation Methods , 2012, Clinical EEG and neuroscience.

[30]  A. Antal,et al.  Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans , 2008, Brain Stimulation.

[31]  J. Krakauer,et al.  Human sensorimotor learning: adaptation, skill, and beyond , 2011, Current Opinion in Neurobiology.

[32]  J. Rothwell,et al.  Transcranial magnetic stimulation: new insights into representational cortical plasticity , 2002, Experimental Brain Research.

[33]  Steven G. Luke,et al.  Evaluating significance in linear mixed-effects models in R , 2016, Behavior Research Methods.

[34]  György Buzsáki,et al.  What does gamma coherence tell us about inter-regional neural communication? , 2015, Nature Neuroscience.

[35]  Bettina Pollok,et al.  The effect of transcranial alternating current stimulation (tACS) at alpha and beta frequency on motor learning , 2015, Behavioural Brain Research.

[36]  L. Cohen,et al.  Mechanisms influencing stimulus-response properties of the human corticospinal system , 2001, Clinical Neurophysiology.

[37]  Gregor Thut,et al.  Lasting EEG/MEG Aftereffects of Rhythmic Transcranial Brain Stimulation: Level of Control Over Oscillatory Network Activity , 2015, Front. Cell. Neurosci..

[38]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[39]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[40]  J. Krakauer,et al.  The uses and interpretations of the motor-evoked potential for understanding behaviour , 2015, Experimental Brain Research.

[41]  M. Nitsche,et al.  Modulating parameters of excitability during and after transcranial direct current stimulation of the human motor cortex , 2005, Clinical Neurophysiology.

[42]  A. Schnitzler,et al.  Effects of 10Hz and 20Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability , 2013, Behavioural Brain Research.

[43]  Walter Paulus,et al.  Boosting brain excitability by transcranial high frequency stimulation in the ripple range , 2010, The Journal of physiology.

[44]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.