Cerebellar motor learning: are environment dynamics more important than error size?

Cerebellar damage impairs the control of complex dynamics during reaching movements. It also impairs learning of predictable dynamic perturbations through an error-based process. Prior work suggests that there are distinct neural mechanisms involved in error-based learning that depend on the size of error experienced. This is based, in part, on the observation that people with cerebellar degeneration may have an intact ability to learn from small errors. Here we studied the relative effect of specific dynamic perturbations and error size on motor learning of a reaching movement in patients with cerebellar damage. We also studied generalization of learning within different coordinate systems (hand vs. joint space). Contrary to our expectation, we found that error size did not alter cerebellar patients' ability to learn the force field. Instead, the direction of the force field affected patients' ability to learn, regardless of whether the force perturbations were introduced gradually (small error) or abruptly (large error). Patients performed best in fields that helped them compensate for movement dynamics associated with reaching. However, they showed much more limited generalization patterns than control subjects, indicating that patients rely on a different learning mechanism. We suggest that patients typically use a compensatory strategy to counteract movement dynamics. They may learn to relax this compensatory strategy when the external perturbation is favorable to counteracting their movement dynamics, and improve reaching performance. Altogether, these findings show that dynamics affect learning in cerebellar patients more than error size.

[1]  Sarah E. Criscimagna-Hemminger,et al.  Size of error affects cerebellar contributions to motor learning. , 2010, Journal of neurophysiology.

[2]  John E. Schlerf,et al.  Individuals with cerebellar degeneration show similar adaptation deficits with large and small visuomotor errors. , 2013, Journal of neurophysiology.

[3]  T. Kalenscher,et al.  Adaptive Motor Behavior of Cerebellar Patients During Exposure to Unfamiliar External Forces , 2004, Journal of motor behavior.

[4]  Andrew A G Mattar,et al.  Effects of human arm impedance on dynamics learning and generalization. , 2009, Journal of neurophysiology.

[5]  W. T. Thach,et al.  Cerebellar ataxia: abnormal control of interaction torques across multiple joints. , 1996, Journal of neurophysiology.

[6]  G. Torres-Oviedo,et al.  Natural error patterns enable transfer of motor learning to novel contexts. , 2012, Journal of neurophysiology.

[7]  P. Thier,et al.  Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease , 2007, The European journal of neuroscience.

[8]  M. Arbib,et al.  Role of the cerebellum in reaching movements in humans. I. Distributed inverse dynamics control , 1998, The European journal of neuroscience.

[9]  W. T. Thach,et al.  Cerebellar ataxia: torque deficiency or torque mismatch between joints? , 2000, Journal of neurophysiology.

[10]  J. Flanagan,et al.  Learning and recall of incremental kinematic and dynamic sensorimotor transformations , 2005, Experimental Brain Research.

[11]  M. Hallett,et al.  International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome , 1997, Journal of the Neurological Sciences.

[12]  M. Kawato,et al.  Formation and control of optimal trajectory in human multijoint arm movement , 1989, Biological Cybernetics.

[13]  Aaron L. Wong,et al.  Saccade adaptation improves in response to a gradually introduced stimulus perturbation , 2011, Neuroscience Letters.

[14]  Konrad Paul Kording,et al.  Estimating the sources of motor errors for adaptation and generalization , 2008, Nature Neuroscience.

[15]  R. Ivry,et al.  An Explicit Strategy Prevails When the Cerebellum Fails to Compute Movement Errors , 2010, The Cerebellum.

[16]  T. Ebner,et al.  Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. , 2004, Journal of neurophysiology.

[17]  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.

[18]  J. Allum,et al.  Postural responses to multidirectional stance perturbations in cerebellar ataxia , 2006, Experimental Neurology.

[19]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[20]  R. Shadmehr Generalization as a behavioral window to the neural mechanisms of learning internal models. , 2004, Human movement science.

[21]  A. Bahill,et al.  Determining ideal baseball bat weights using muscle force-velocity relationships , 1989, Biological Cybernetics.

[22]  S. M. Morton,et al.  Cerebellar Contributions to Locomotor Adaptations during Splitbelt Treadmill Walking , 2006, The Journal of Neuroscience.

[23]  Reza Shadmehr,et al.  Motor Adaptation as a Process of Reoptimization , 2008, The Journal of Neuroscience.

[24]  Y. Rossetti,et al.  Two waves of a long-lasting aftereffect of prism adaptation measured over 7 days , 2006, Experimental Brain Research.

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

[26]  P. Gribble,et al.  Persistence of inter-joint coupling during single-joint elbow flexions after shoulder fixation , 2005, Experimental Brain Research.

[27]  R. Miall,et al.  Visuomotor adaptation during inactivation of the dentate nucleus. , 1999, Neuroreport.

[28]  Sarah E. Criscimagna-Hemminger,et al.  Cerebellar Contributions to Reach Adaptation and Learning Sensory Consequences of Action , 2012, The Journal of Neuroscience.

[29]  Jörn Diedrichsen,et al.  Reach adaptation: what determines whether we learn an internal model of the tool or adapt the model of our arm? , 2008, Journal of neurophysiology.

[30]  J. Konczak,et al.  Coordination of multi-joint arm movements in cerebellar ataxia: Analysis of hand and angular kinematics , 1998, Experimental Brain Research.

[31]  E. Boyden,et al.  Selective Engagement of Plasticity Mechanisms for Motor Memory Storage , 2006, Neuron.

[32]  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.

[33]  L. Nashner,et al.  Properties of postural adjustments associated with rapid arm movements. , 1982, Journal of neurophysiology.

[34]  Vincent S. Huang,et al.  Persistence of motor memories reflects statistics of the learning event. , 2009, Journal of neurophysiology.

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