The role of the cross-sensory error signal in visuomotor adaptation

Reaching to targets with misaligned visual feedback of the hand leads to changes in proprioceptive estimates of hand position and reach aftereffects. In such tasks, subjects are able to make use of two error signals: the discrepancy between the desired and actual movement, known as the sensorimotor error signal, and the discrepancy between visual and proprioceptive estimates of hand position, which we refer to as the cross-sensory error signal. We have recently shown that mere exposure to a sensory discrepancy in the absence of goal-directed movement (i.e. no sensorimotor error signal) is sufficient to produce similar changes in felt hand position and reach aftereffects. Here, we sought to determine the extent that this cross-sensory error signal can contribute to proprioceptive recalibration and movement aftereffects by manipulating the magnitude of this signal in the absence of volitional aiming movements. Subjects pushed their hand out along a robot-generated linear path that was gradually rotated clockwise relative to the path of a cursor. On all trials, subjects viewed a cursor that headed directly towards a remembered target while their hand moved out synchronously. After exposure to a 30° rotated hand-cursor distortion, subjects recalibrated their sense of felt hand position and adapted their reaches. However, no additional increases in recalibration or aftereffects were observed following further increases in the cross-sensory error signal (e.g. up to 70°). This is in contrast to our previous study where subjects freely reached to targets with misaligned visual hand position feedback, hence experiencing both sensorimotor and cross-sensory errors, and the distortion magnitude systematically predicted increases in proprioceptive recalibration and reach aftereffects. Given these findings, we suggest that the cross-sensory error signal results in changes to felt hand position which drive partial reach aftereffects, while larger aftereffects that are produced after visuomotor adaptation (and that vary with the size of distortion) are related to the sensorimotor error signal.

[1]  C Ghez,et al.  Learning of Visuomotor Transformations for Vectorial Planning of Reaching Trajectories , 2000, The Journal of Neuroscience.

[2]  B. Treutwein Adaptive psychophysical procedures , 1995, Vision Research.

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

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

[5]  D. Henriques,et al.  Visuomotor adaptation and proprioceptive recalibration in older adults , 2010, Experimental Brain Research.

[6]  B Wallace,et al.  Prism Exposure Aftereffects and Direct Effects for Different Movement and Feedback Times , 2000, Journal of motor behavior.

[7]  Mark Shelhamer,et al.  Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes. , 2011, Journal of neurophysiology.

[8]  Erin K Cressman,et al.  Visuomotor Adaptation and Proprioceptive Recalibration , 2012, Journal of motor behavior.

[9]  D. Henriques,et al.  Proprioceptive recalibration in the right and left hands following abrupt visuomotor adaptation , 2011, Experimental Brain Research.

[10]  W. T. Thach,et al.  Throwing while looking through prisms , 2005 .

[11]  H. Pick,et al.  Visual and proprioceptive adaptation to optical displacement of the visual stimulus. , 1966, Journal of experimental psychology.

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

[13]  Stephan Riek,et al.  Real-time error detection but not error correction drives automatic visuomotor adaptation , 2010, Experimental Brain Research.

[14]  J. F. Soechting,et al.  Bias and sensitivity in the haptic perception of geometry , 2003, Experimental Brain Research.

[15]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[16]  G. M. Redding,et al.  Adaptive spatial alignment and strategic perceptual-motor control. , 1996, Journal of experimental psychology. Human perception and performance.

[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]  D. Henriques,et al.  Proprioceptive recalibration following prolonged training and increasing distortions in visuomotor adaptation , 2011, Neuropsychologia.

[19]  H. Kesten Accelerated Stochastic Approximation , 1958 .

[20]  Mollie K. Marko,et al.  Sensitivity to prediction error in reach adaptation. , 2012, Journal of neurophysiology.

[21]  Benjamin Wallace,et al.  First-Trial "Adaptation" to Prism Exposure: Artifact of Visual Capture , 2004, Journal of motor behavior.

[22]  Erin K. Cressman,et al.  Proprioceptive localization of the left and right hands , 2010, Experimental Brain Research.

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

[24]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

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

[26]  Konrad Paul Kording,et al.  Relevance of error: what drives motor adaptation? , 2009, Journal of neurophysiology.

[27]  C. S. Harris Adaptation to Displaced Vision: Visual, Motor, or Proprioceptive Change? , 1963, Science.

[28]  Katja Fiehler,et al.  Reach endpoint errors do not vary with movement path of the proprioceptive target. , 2012, Journal of neurophysiology.

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

[30]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[31]  O. Bock,et al.  Sensorimotor adaptation to rotated visual input: different mechanisms for small versus large rotations , 2001, Experimental Brain Research.

[32]  P. Thier,et al.  The Cerebellum Updates Predictions about the Visual Consequences of One's Behavior , 2008, Current Biology.

[33]  Hannah J. Block,et al.  Cerebellar involvement in motor but not sensory adaptation , 2012, Neuropsychologia.

[34]  Erin K Cressman,et al.  Reach adaptation and proprioceptive recalibration following exposure to misaligned sensory input. , 2010, Journal of neurophysiology.

[35]  D. Wolpert,et al.  When Feeling Is More Important Than Seeing in Sensorimotor Adaptation , 2002, Current Biology.

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

[37]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[38]  Philip N. Sabes,et al.  Visual-shift adaptation is composed of separable sensory and task-dependent effects. , 2007, Journal of neurophysiology.