Stimulating the Cerebellum Affects Visuomotor Adaptation but not Intermanual Transfer of Learning

When systematic movement errors occur, the brain responds with a systematic change in motor behavior. This type of adaptive motor learning can transfer intermanually; adaptation of movements of the right hand in response to training with a perturbed visual signal (visuomotor adaptation) may carry over to the left hand. While visuomotor adaptation has been studied extensively, it is unclear whether the cerebellum, a structure involved in adaptation, is important for intermanual transfer as well. We addressed this question with three experiments in which subjects reached with their right hands as a 30° visuomotor rotation was introduced. Subjects received anodal or sham transcranial direct current stimulation on the trained (experiment 1) or untrained (experiment 2) hemisphere of the cerebellum, or, for comparison, motor cortex (M1). After the training period, subjects reached with their left hand, without visual feedback, to assess intermanual transfer of learning aftereffects. Stimulation of the right cerebellum caused faster adaptation, but none of the stimulation sites affected transfer. To ascertain whether cerebellar stimulation would increase transfer if subjects learned faster as well as a larger amount, in experiment 3 anodal and sham cerebellar groups experienced a shortened training block such that the anodal group learned more than sham. Despite the difference in adaptation magnitude, transfer was similar across these groups, although smaller than in experiment 1. Our results suggest that intermanual transfer of visuomotor learning does not depend on cerebellar activity and that the number of movements performed at plateau is an important predictor of transfer.

[1]  Joaquin A. Anguera,et al.  Neural correlates associated with intermanual transfer of sensorimotor adaptation , 2007, Brain Research.

[2]  R B Welch,et al.  Variables affecting the intermanual transfer and decay of prism adaptation. , 1974, Journal of experimental psychology.

[3]  Sarah E. Criscimagna-Hemminger,et al.  Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. , 2011, Cerebral cortex.

[4]  W. T. Thach,et al.  Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. , 1996, Brain : a journal of neurology.

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

[6]  Mukta N. Joshi,et al.  The extent of interlimb transfer following adaptation to a novel visuomotor condition does not depend on awareness of the condition. , 2011, Journal of neurophysiology.

[7]  Robert L. Sainburg,et al.  The symmetry of interlimb transfer depends on workspace locations , 2006, Experimental Brain Research.

[8]  R. Shadmehr,et al.  Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degeneration. , 2005, Journal of neurophysiology.

[9]  R. Ivry,et al.  visuomotor adaptation Trial-by-trial analysis of intermanual transfer during , 2011 .

[10]  J. Krakauer,et al.  Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. , 2004, Journal of neurophysiology.

[11]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[12]  Sergio P. Rigonatti,et al.  Transcranial direct current stimulation of the unaffected hemisphere in stroke patients , 2005, Neuroreport.

[13]  M. Hallett,et al.  Adaptation to lateral displacement of vision in patients with lesions of the central nervous system , 1983, Neurology.

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

[15]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[16]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[17]  E. Vaadia,et al.  Expressions of Multiple Neuronal Dynamics during Sensorimotor Learning in the Motor Cortex of Behaving Monkeys , 2011, PloS one.

[18]  Robert L. Sainburg,et al.  Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position , 2007, Experimental Brain Research.

[19]  Amy J. Bastian,et al.  Inter- and intra-limb generalization of adaptation during catching , 2001, Experimental Brain Research.

[20]  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.

[21]  E. Vaadia,et al.  Preparatory activity in motor cortex reflects learning of local visuomotor skills , 2003, Nature Neuroscience.

[22]  H. Imamizu,et al.  The locus of visual-motor learning at the task or manipulator level: implications from intermanual transfer. , 1995, Journal of experimental psychology. Human perception and performance.

[23]  J. Lackner,et al.  Motor control and learning in altered dynamic environments , 2005, Current Opinion in Neurobiology.

[24]  Otmar Bock,et al.  The effect of cerebellar cortical degeneration on adaptive plasticity and movement control , 2009, Experimental Brain Research.

[25]  L. Cohen,et al.  Mechanisms controlling motor output to a transfer hand after learning a sequential pinch force skill with the opposite hand , 2009, Clinical Neurophysiology.

[26]  Maurice Ouaknine,et al.  Orientation of the body response to galvanic stimulation as a function of the inter-vestibular imbalance , 2000, Experimental Brain Research.

[27]  K M Heilman,et al.  Left-hemisphere motor dominance in righthanders. , 1980, Cortex; a journal devoted to the study of the nervous system and behavior.

[28]  Mathias Hegele,et al.  Constraints on visuo-motor adaptation depend on the type of visual feedback during practice , 2008, Experimental Brain Research.

[29]  P. Celnik,et al.  Modulation of Cerebellar Excitability by Polarity-Specific Noninvasive Direct Current Stimulation , 2009, The Journal of Neuroscience.

[30]  S. Wise,et al.  Changes in motor cortical activity during visuomotor adaptation , 1998, Experimental Brain Research.

[31]  Erin V. L. Vasudevan,et al.  Younger Is Not Always Better: Development of Locomotor Adaptation from Childhood to Adulthood , 2011, The Journal of Neuroscience.

[32]  R. Sainburg,et al.  Interlimb transfer of visuomotor rotations: independence of direction and final position information , 2002, Experimental Brain Research.

[33]  Jinsung Wang,et al.  Interlimb transfer of novel inertial dynamics is asymmetrical. , 2004, Journal of neurophysiology.

[34]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[35]  Scott T. Grafton,et al.  Abstract and Effector-Specific Representations of Motor Sequences Identified with PET , 1998, The Journal of Neuroscience.

[36]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

[37]  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.

[38]  Mark L. Latash,et al.  Mirror Writing: Learning, Transfer, and Implications for Internal Inverse Models. , 1999, Journal of motor behavior.

[39]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

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

[41]  P J Bairstow,et al.  Bilateral transfer in tapping skill in the absence of peripheral information. , 1970, Journal of motor behavior.

[42]  Jason B. Mattingley,et al.  Neural mechanisms underlying spatial realignment during adaptation to optical wedge prisms , 2010, Neuropsychologia.

[43]  M. Ghilardi,et al.  Patterns of regional brain activation associated with different forms of motor learning , 2000, Brain Research.

[44]  P. van Donkelaar,et al.  The Human Dorsal Premotor Cortex Generates On-Line Error Corrections during Sensorimotor Adaptation , 2006, The Journal of Neuroscience.

[45]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

[46]  Reza Shadmehr,et al.  Learned dynamics of reaching movements generalize from dominant to nondominant arm. , 2003, Journal of neurophysiology.

[47]  S. Sato,et al.  Safety and cognitive effect of frontal DC brain polarization in healthy individuals , 2005, Neurology.

[48]  Sara Marceglia,et al.  Cerebellar Transcranial Direct Current Stimulation Impairs the Practice-dependent Proficiency Increase in Working Memory , 2008, Journal of Cognitive Neuroscience.

[49]  Denise Y. P. Henriques,et al.  Visuomotor adaptation and intermanual transfer under different viewing conditions , 2010, Experimental Brain Research.

[50]  R. Ivry,et al.  Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. , 2005, Journal of neurophysiology.

[51]  Marcel Kinsbourne,et al.  Asymmetrical transfer of training between hands: Implications for interhemispheric communication in normal brain , 1989, Brain and Cognition.

[52]  Erin V. L. Vasudevan,et al.  Modulating locomotor adaptation with cerebellar stimulation. , 2012, Journal of neurophysiology.

[53]  R B Welch,et al.  Multiple concurrent visual-motor mappings: implications for models of adaptation. , 1994, Journal of experimental psychology. Human perception and performance.

[54]  Adam Possner,et al.  Cerebellum , 2012, Neurology.

[55]  Kenneth M. Heilman,et al.  Left-Hemisphere Motor Dominance in Righthandersi , 1980, Cortex.

[56]  E. Bizzi,et al.  Neural basis of motor control and its cognitive implications , 1998, Trends in Cognitive Sciences.

[57]  A. Bastian,et al.  Thinking about walking: effects of conscious correction versus distraction on locomotor adaptation. , 2010, Journal of neurophysiology.

[58]  Reza Shadmehr,et al.  Impairment of Retention But Not Acquisition of a Visuomotor Skill Through Time-Dependent Disruption of Primary Motor Cortex , 2007, The Journal of Neuroscience.

[59]  J. Krakauer,et al.  Adaptation to Visuomotor Transformations: Consolidation, Interference, and Forgetting , 2005, The Journal of Neuroscience.

[60]  A. Patla,et al.  Postural responses and spatial orientation to neck proprioceptive and vestibular inputs during locomotion in young and older adults , 2005, Experimental Brain Research.

[61]  Jose L Contreras-Vidal,et al.  Learning multiple visuomotor transformations: adaptation and context-dependent recall. , 2004, Motor control.

[62]  Jinsung Wang A dissociation between visual and motor workspace inhibits generalization of visuomotor adaptation across the limbs , 2008, Experimental Brain Research.

[63]  S. P. Swinnen,et al.  Interlimb coordination in patients with Parkinson’s disease: motor learning deficits and the importance of augmented information feedback , 1997, Experimental Brain Research.

[64]  Rachael Seidler,et al.  Degree of handedness affects intermanual transfer of skill learning , 2008, Experimental Brain Research.