Continuous Reports of Sensed Hand Position During Sensorimotor Adaptation

Sensorimotor learning entails multiple learning processes, some volitional and explicit, and others automatic and implicit. A new method to isolate implicit adaptation involves the use of a “clamped” visual perturbation in which, during a reaching movement, visual feedback is limited to a cursor that follows an invariant trajectory, offset from the target by a fixed angle. Despite full awareness that the cursor movement is not contingent on their behavior, as well as explicit instructions to ignore the cursor, systematic changes in motor behavior are observed, and these changes have the signatures of implicit adaptation observed in studies using classic visuomotor perturbations. While it is clear that the response to clamped feedback occurs automatically, it remains unknown if the adjustments in behavior remain outside the participant’s awareness. To address this question, we used the clamp method and directly probed awareness by asking participants to report their hand position after each reach. As expected, we observed robust deviations in hand angle away from the target (average of ∼18°). The hand reports also showed systematic deviations over the course of adaptation, initially attracted towards the visual feedback and then in the opposite direction, paralleling the shift in hand position. However, these effects were subtle (∼2° at asymptote), with the hand reports dominated by a feedforward signal associated with the motor intent yet modulated in a limited way by feedback sources. These results confirm that adaptation in response to a visual perturbation is not only automatic, but also largely implicit. NEWS AND NOTEWORTHY Sensorimotor adaptation operates in an obligatory manner. Qualitatively, subjective reports obtained after adaptation demonstrate that, in many conditions, participants are unaware of significant changes in behavior. In the present study, we quantified participants’ awareness of adaptation by obtaining reports of hand position on a trial-by-trial basis. The results confirm that participants are largely unaware of adaptation, but also reveal the subtle influence of feedback on their subjective experience.

[1]  Richard B. Ivry,et al.  Flexible Cognitive Strategies during Motor Learning , 2011, PLoS Comput. Biol..

[2]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[3]  Krista M Bond,et al.  Flexible explicit but rigid implicit learning in a visuomotor adaptation task. , 2015, Journal of neurophysiology.

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

[5]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[6]  Darius E. Parvin,et al.  Credit Assignment in a Motor Decision Making Task Is Influenced by Agency and Not Sensory Prediction Errors , 2018, The Journal of Neuroscience.

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

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

[9]  E. Erdfelder,et al.  Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses , 2009, Behavior research methods.

[10]  Hermann von Helmholtz,et al.  Treatise on Physiological Optics , 1962 .

[11]  Gordon M. Redding,et al.  Applications of prism adaptation: a tutorial in theory and method , 2005, Neuroscience & Biobehavioral Reviews.

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

[13]  Jennifer E. Ruttle,et al.  Time Course of Reach Adaptation and Proprioceptive Recalibration during Visuomotor Learning , 2016, PloS one.

[14]  Jennifer E. Ruttle,et al.  Implicit motor learning within three trials , 2020, Scientific Reports.

[15]  J. Krakauer,et al.  An Implicit Plan Overrides an Explicit Strategy during Visuomotor Adaptation , 2006, The Journal of Neuroscience.

[16]  P. Thier,et al.  Misattributions of agency in schizophrenia are based on imprecise predictions about the sensory consequences of one's actions. , 2010, Brain : a journal of neurology.

[17]  Reza Moazzezi,et al.  Invariant errors reveal limitations in motor correction rather than constraints on error sensitivity , 2017, Communications Biology.

[18]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[19]  Allison M. Okamura,et al.  Cerebellar damage reduces the stability of motor memories , 2014 .

[20]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[21]  C. Jedynak,et al.  [Disorders of interhemispheric transfer (callosal disonnection). 3 cases of tumor of the corpus callosum. The strange hand sign]. , 1972, Revue neurologique.

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

[23]  A. G. Feldman New insights into action–perception coupling , 2009, Experimental Brain Research.

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

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

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

[27]  Raymond J. Delnicki,et al.  Overcoming Motor “Forgetting” Through Reinforcement Of Learned Actions , 2012, The Journal of Neuroscience.

[28]  D Curran-Everett,et al.  Multiple comparisons: philosophies and illustrations. , 2000, American journal of physiology. Regulatory, integrative and comparative physiology.

[29]  Reza Shadmehr,et al.  Learning from Sensory and Reward Prediction Errors during Motor Adaptation , 2011, PLoS Comput. Biol..

[30]  Richard B. Ivry,et al.  Characteristics of Implicit Sensorimotor Adaptation Revealed by Task-irrelevant Clamped Feedback , 2017, Journal of Cognitive Neuroscience.

[31]  O. Donchin,et al.  Awareness of Sensorimotor Adaptation to Visual Rotations of Different Size , 2015, PloS one.

[32]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[33]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[34]  Richard B Ivry,et al.  The influence of task outcome on implicit motor learning , 2018, eLife.

[35]  J. Krakauer,et al.  Explicit and Implicit Contributions to Learning in a Sensorimotor Adaptation Task , 2014, The Journal of Neuroscience.