It’s too quick to blame myself—the effects of fast and slow rates of change on credit assignment during object lifting

Although there have been substantial research efforts examining the effect of various rates of change in reaching movements, there has been little to no research devoted to this issue during object manipulation tasks. In force-field and visuomotor adaptation studies, two parallel processes have been identified: first, a fast process that adapts and de-adapts quickly is thought to enable the actor to deal with potentially transient perturbations. Second, a slower, but longer lasting process adapts if these initial perturbations persist over time. In a largely separate body of research, the role of credit assignment has been examined in terms of allotting the cause of errors to changes in the body vs. changes in the outside world. Of course, these two processes are usually linked within the real world, with short lasting perturbations most often being linked to external causes and longer lasting perturbations being linked to internal causes. Here, we demonstrate that the increases in load forces associated with a gradual increase in object weight during a natural object lifting task are transferred when lifting a novel object, whereas a sudden increase in object weight is not. We speculate that gradual rates of change in the weight of the object being lifted are attributed to the self, whereas fast rates of change are more likely to be attributed to the external environment. This study extends our knowledge of the multiple timescales involved in motor learning to a more natural object manipulation scenario, while concurrently providing support for the hypothesis that the multiple time scales involved in motor learning are tuned for different learning contexts.

[1]  Jonathan S. Cant,et al.  Living in a material world: how visual cues to material properties affect the way that we lift objects and perceive their weight. , 2009, Journal of neurophysiology.

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

[3]  D. Nowak,et al.  Preserved and impaired aspects of predictive grip force control in cerebellar patients , 2005, Clinical Neurophysiology.

[4]  J. Noth,et al.  Precision grip deficits in cerebellar disorders in man , 2001, Clinical Neurophysiology.

[5]  R. Johansson,et al.  Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip , 2004, Experimental Brain Research.

[6]  N. Schweighofer,et al.  Dual Adaptation Supports a Parallel Architecture of Motor Memory , 2009, The Journal of Neuroscience.

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

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

[9]  Lee A Baugh,et al.  Material evidence: interaction of well-learned priors and sensorimotor memory when lifting objects. , 2012, Journal of neurophysiology.

[10]  K. J. Cole,et al.  Memory representations underlying motor commands used during manipulation of common and novel objects. , 1993, Journal of neurophysiology.

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

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

[13]  J. Dichgans,et al.  Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions , 2004, Experimental Brain Research.

[14]  Miles C. Bowman,et al.  Control strategies in object manipulation tasks , 2006, Current Opinion in Neurobiology.

[15]  Reza Shadmehr,et al.  Dissociable effects of the implicit and explicit memory systems on learning control of reaching , 2006, Experimental Brain Research.

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

[17]  J. Flanagan,et al.  Independence of perceptual and sensorimotor predictions in the size–weight illusion , 2000, Nature Neuroscience.

[18]  R. Johansson,et al.  Development of human precision grip , 2004, Experimental Brain Research.

[19]  D. Westwood,et al.  Opposite perceptual and sensorimotor responses to a size-weight illusion. , 2006, Journal of neurophysiology.

[20]  R. S. Johansson,et al.  Roles of glabrous skin receptors and sensorimotor memory in automatic control of precision grip when lifting rougher or more slippery objects , 2004, Experimental Brain Research.

[21]  L. Jones,et al.  Perception of force and weight: theory and research. , 1986, Psychological bulletin.

[22]  D. Wolpert,et al.  The cerebellum is involved in predicting the sensory consequences of action , 1999, Neuroreport.

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

[24]  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.

[25]  Hans Forssberg,et al.  Brain activity during predictable and unpredictable weight changes when lifting objects. , 2005, Journal of neurophysiology.

[26]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  R. Johansson,et al.  Integration of sensory information during the programming of precision grip: comments on the contributions of size cues , 2004, Experimental Brain Research.

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

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

[30]  N. Durlach,et al.  Manual discrimination of force using active finger motion , 1991, Perception & psychophysics.

[31]  M. Wiesendanger,et al.  Role of the Cerebellum in Tuning Anticipatory and Reactive Grip Force Responses , 1999, Journal of Cognitive Neuroscience.

[32]  Reza Shadmehr,et al.  Learning of action through adaptive combination of motor primitives , 2000, Nature.

[33]  J R Flanagan,et al.  The Role of Internal Models in Motion Planning and Control: Evidence from Grip Force Adjustments during Movements of Hand-Held Loads , 1997, The Journal of Neuroscience.

[34]  R. Johansson,et al.  Factors influencing the force control during precision grip , 2004, Experimental Brain Research.

[35]  Hiroshi Kinoshita,et al.  Functional brain areas used for the lifting of objects using a precision grip: a PET study , 2000, Brain Research.

[36]  J. Randall Flanagan,et al.  Coding and use of tactile signals from the fingertips in object manipulation tasks , 2009, Nature Reviews Neuroscience.

[37]  H. Ross,et al.  Sensorimotor mechanisms in weight discrimination , 1984, Perception & psychophysics.

[38]  D. Pélisson,et al.  Sensorimotor adaptation of saccadic eye movements , 2010, Neuroscience & Biobehavioral Reviews.

[39]  D. Wolpert,et al.  Motor prediction , 2001, Current Biology.

[40]  I Salimi,et al.  Specificity of internal representations underlying grasping. , 2000, Journal of neurophysiology.

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

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

[43]  M. Kawato,et al.  Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. , 2003, Progress in brain research.

[44]  S. M. Morton,et al.  Prism adaptation during walking generalizes to reaching and requires the cerebellum. , 2004, Journal of neurophysiology.

[45]  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.

[46]  Hans Forssberg,et al.  Formation and lateralization of internal representations underlying motor commands during precision grip , 1994, Neuropsychologia.

[47]  K. Newell Motor skill acquisition. , 1991, Annual review of psychology.

[48]  R. Johansson,et al.  Development of human precision grip , 2004, Experimental Brain Research.

[49]  R A Scheidt,et al.  Persistence of motor adaptation during constrained, multi-joint, arm movements. , 2000, Journal of neurophysiology.

[50]  R. Johansson,et al.  Experience Can Change Distinct Size-Weight Priors Engaged in Lifting Objects and Judging their Weights , 2008, Current Biology.

[51]  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.

[52]  R. Shadmehr,et al.  A Shared Resource between Declarative Memory and Motor Memory , 2010, The Journal of Neuroscience.

[53]  Yves Rossetti,et al.  Enhancing Visuomotor Adaptation by Reducing Error Signals: Single-step (Aware) versus Multiple-step (Unaware) Exposure to Wedge Prisms , 2007, Journal of Cognitive Neuroscience.

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

[55]  Rachael D. Seidler,et al.  Contributions of Spatial Working Memory to Visuomotor Learning , 2010, Journal of Cognitive Neuroscience.

[56]  A. Wing,et al.  Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration , 1999, Experimental Brain Research.

[57]  K. J. Cole,et al.  Sensory-motor coordination during grasping and manipulative actions , 1992, Current Biology.

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

[59]  M. Mon-Williams,et al.  The size of the visual size cue used for programming manipulative forces during precision grip , 2000, Experimental Brain Research.