Pre-movement changes in sensorimotor beta oscillations predict motor adaptation drive

Beta frequency oscillations in scalp electroencephalography (EEG) recordings over the primary motor cortex have been associated with the preparation and execution of voluntary movements. Here, we test whether changes in beta frequency are related to the preparation of adapted movements in human, and whether such effects generalise to other species (cat). Eleven healthy adult humans performed a joystick visuomotor adaptation task. Beta (15-25Hz) scalp EEG signals recorded over the motor cortex during a pre-movement preparatory phase were, on average, significantly reduced in amplitude during early adaptation trials compared to baseline or late adaptation trials (p=0.01). The changes in beta were not related to measurements of reaction time or duration of the reach. We also recorded LFP activity within the primary motor cortex of three cats during a prism visuomotor adaptation task. Analysis of these signals revealed similar reductions in motor cortical LFP beta frequencies during early adaptation. This effect was also present when controlling for any influence of the reaction time and reaching duration. Overall, the results are consistent with a reduction in pre-movement beta oscillations predicting an increase in adaptive drive in upcoming task performance when motor errors are largest in magnitude and the rate of adaptation is greatest.

[1]  Hannah J. Block,et al.  Increase in weighting of vision vs. proprioception associated with force field adaptation , 2019, Scientific Reports.

[2]  Flavie Torrecillos,et al.  Distinct Modulations in Sensorimotor Postmovement and Foreperiod β-Band Activities Related to Error Salience Processing and Sensorimotor Adaptation , 2015, The Journal of Neuroscience.

[3]  Peter Brown,et al.  Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans , 2009, Current Biology.

[4]  Gonçalo Lopes,et al.  Bonsai: an event-based framework for processing and controlling data streams , 2014, bioRxiv.

[5]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[6]  Emilio Bizzi,et al.  Disruption of Primary Motor Cortex before Learning Impairs Memory of Movement Dynamics , 2006, The Journal of Neuroscience.

[7]  E. Olivier,et al.  Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation , 1997, The Journal of physiology.

[8]  Reza Shadmehr,et al.  Internal models of limb dynamics and the encoding of limb state , 2005, Journal of neural engineering.

[9]  E. Fetz,et al.  Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  D Timmann,et al.  Adaptation to visuomotor rotation and force field perturbation is correlated to different brain areas in patients with cerebellar degeneration. , 2009, Journal of neurophysiology.

[11]  Marco Bimbi,et al.  Simultaneous scalp recorded EEG and local field potentials from monkey ventral premotor cortex during action observation and execution reveals the contribution of mirror and motor neurons to the mu-rhythm , 2018, NeuroImage.

[12]  Dorothy V. M. Bishop,et al.  Journal of Neuroscience Methods , 2015 .

[13]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[14]  Claude Prablanc,et al.  Visuomotor adaptation needs a validation of prediction error by feedback error , 2014, Front. Hum. Neurosci..

[15]  M. Masson,et al.  Using confidence intervals in within-subject designs , 1994, Psychonomic bulletin & review.

[16]  Begoña Garcia-Zapirain,et al.  EEG artifact removal—state-of-the-art and guidelines , 2015, Journal of neural engineering.

[17]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[18]  Ned Jenkinson,et al.  Dynamic Neural Correlates of Motor Error Monitoring and Adaptation during Trial-to-Trial Learning , 2014, The Journal of Neuroscience.

[19]  Andreea Ioana Sburlea,et al.  EEG neural correlates of goal-directed movement intention , 2017, NeuroImage.

[20]  D. Wolpert,et al.  Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation , 2002, The Journal of physiology.

[21]  Thomas Brochier,et al.  Modulations of EEG Beta Power during Planning and Execution of Grasping Movements , 2013, PloS one.

[22]  M. Garwicz,et al.  Gating of cutaneous input to cerebellar climbing fibres during a reaching task in the cat , 1997, The Journal of physiology.

[23]  R. Miall,et al.  The effect of rTMS over the cerebellum in normal human volunteers on peg-board movement performance , 2004, Neuroscience Letters.

[24]  Flavie Torrecillos,et al.  Error-related modulations of the sensorimotor post-movement and foreperiod beta-band activities arise from distinct neural substrates and do not reflect efferent signal processing , 2019, NeuroImage.

[25]  P. Celnik,et al.  Dissociating the roles of the cerebellum and motor cortex during adaptive learning: the motor cortex retains what the cerebellum learns. , 2011, Cerebral cortex.

[26]  Bijan Pesaran,et al.  Uncovering the Mysterious Origins of Local Field Potentials , 2009, Neuron.

[27]  W. T. Thach,et al.  Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. , 1996, Brain : a journal of neurology.

[28]  Jose M Carmena,et al.  Beta band oscillations in motor cortex reflect neural population signals that delay movement onset , 2017, eLife.

[29]  D. Vaillancourt,et al.  Beta-band oscillations in the supplementary motor cortex are modulated by levodopa and associated with functional activity in the basal ganglia , 2018, NeuroImage: Clinical.

[30]  David J. Nutt,et al.  The effects of elevated endogenous GABA levels on movement-related network oscillations , 2013, NeuroImage.

[31]  M. Magnin,et al.  Stereotactic functional mapping of the cat motor cortex , 2011, Behavioural Brain Research.

[32]  Mikko Pohja,et al.  On the human sensorimotor-cortex beta rhythm: Sources and modeling , 2005, NeuroImage.

[33]  D. Henriques,et al.  Sensory recalibration of hand position following visuomotor adaptation. , 2009, Journal of neurophysiology.

[34]  M. Hallett,et al.  Adaptation motor learning of arm movements in patients with cerebellar disease. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[35]  Ross Cunnington,et al.  Neural Oscillations and the Initiation of Voluntary Movement , 2018, Front. Psychol..

[36]  M. Masson.  Using confidence intervals for graphically based data interpretation. , 2003, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[37]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[38]  J. Donoghue,et al.  Oscillations in local field potentials of the primate motor cortex during voluntary movement. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Christopher C. Pack,et al.  Pattern Motion Selectivity of Spiking Outputs and Local Field Potentials in Macaque Visual Cortex , 2009, The Journal of Neuroscience.

[40]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[41]  Sotaro Shimada,et al.  Simultaneous measurement of electroencephalography and near-infrared spectroscopy during voluntary motor preparation , 2015, Scientific Reports.

[42]  A. Riehle,et al.  The ups and downs of beta oscillations in sensorimotor cortex , 2013, Experimental Neurology.

[43]  J. Baizer,et al.  Cerebellar lesions and prism adaptation in macaque monkeys. , 1999, Journal of neurophysiology.

[44]  W. Mackay,et al.  EEG rhythms of the sensorimotor region during hand movements. , 1994, Electroencephalography and clinical neurophysiology.

[45]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

[46]  Ian M Franks,et al.  Updating of an internal model without proprioception: a deafferentation study , 2006, Neuroreport.

[47]  J. Galea,et al.  Neural changes associated with cerebellar tDCS studied using MR spectroscopy , 2018, Experimental Brain Research.

[48]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[49]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.