Grip force control of predictable external loads

The grip force used to grasp and hold an object is modulated synchronously and precisely with a self-produced load indicating predictive feedforward control. It is unclear whether an externally produced load can be anticipated with similar feedforward-timing and precision if it can be predicted, e.g., because it has a periodic time course. In the present study we tested eight healthy subjects during the compensation of an externally produced sinusoidal load with cycle duration 1.5 s and more than 700 repetitions during two successive sessions. Performance parameters characterizing the timing and precision of the grip force–load coupling were analyzed across the sessions and compared with a retention measurement on the following day and with an experimental condition when the same loads were self-produced. The time lag between the grip force and the load decreased from values greater than zero to values close to zero during the practice sessions indicating a change from a more reactive to a predictive response. In contrast, the precision and economy of the coupling showed no improvement. Performance on the second day was similar to initial performance, only some retention of feedforward timing was obvious. Precision and economy of grip force control during self-produced loading was clearly superior to external loading even after extended practice. Our findings confirm that periodic external loads are controlled by predictive feedforward mechanism after sufficient experience. However, performance was not stable and did not reach the level of self-generated loading. These results are interpreted as reflecting the significance of an efferent copy of the motor command in sensorimotor processing that may be associated with a distinct neuronal representation.

[1]  Joachim Hermsdörfer,et al.  Evaluation of precision grip using pneumatically controlled loads , 1992, Journal of Neuroscience Methods.

[2]  D M Wolpert,et al.  Predicting the Consequences of Our Own Actions: The Role of Sensorimotor Context Estimation , 1998, The Journal of Neuroscience.

[3]  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.

[4]  D. L. Weeks,et al.  Precision-grip force changes in the anatomical and prosthetic limb during predictable load increases , 2000, Experimental Brain Research.

[5]  A. G. Witney,et al.  Learning and decay of prediction in object manipulation. , 2000, Journal of neurophysiology.

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

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

[8]  Alan M. Wing,et al.  Internal models of the motor system that explain predictive grip force control , 2004 .

[9]  Joachim Hermsdörfer,et al.  Predictability influences finger force control when catching a free-falling object , 2004, Experimental Brain Research.

[10]  R. Johansson,et al.  Prediction Precedes Control in Motor Learning , 2003, Current Biology.

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

[12]  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.

[13]  A. Lee,et al.  The representation of predictive force control and internal forward models: evidence from lesion studies and brain imaging , 2005, Cognitive Processing.

[14]  R. Johansson,et al.  Somatosensory control of precision grip during unpredictable pulling loads , 1992, Experimental Brain Research.

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

[16]  Dennis A Nowak,et al.  Different modes of grip force control: voluntary and externally guided arm movements with a hand-held load , 2004, Clinical Neurophysiology.

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

[18]  Joël Monzée,et al.  Responses of cerebellar interpositus neurons to predictable perturbations applied to an object held in a precision grip. , 2004, Journal of neurophysiology.

[19]  Joachim Hermsdörfer,et al.  Predictive and reactive control of grasping forces: on the role of the basal ganglia and sensory feedback , 2006, Experimental Brain Research.

[20]  Slobodan Jaric,et al.  Coordination of hand grip and load forces in uni- and bidirectional static force production tasks , 2005, Neuroscience Letters.

[21]  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.

[22]  R. Johansson,et al.  Programmed and triggered actions to rapid load changes during precision grip , 2004, Experimental Brain Research.

[23]  Joachim Hermsdörfer,et al.  Predictive and reactive finger force control during catching in cerebellar degeneration , 2008, The Cerebellum.

[24]  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.

[25]  Jean-Louis Thonnard,et al.  The cutaneous contribution to adaptive precision grip , 2004, Trends in Neurosciences.

[26]  J. Flanagan,et al.  The stability of precision grip forces during cyclic arm movements with a hand-held load , 1990, Experimental Brain Research.

[27]  A. M. Wing,et al.  Grip force dynamics in the approach to a collision , 1999, Experimental Brain Research.

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

[29]  K. Lashley.  Basic neural mechanisms in behavior. , 1930 .

[30]  R. Johansson,et al.  Somatosensory control of precision grip during unpredictable pulling loads , 2004, Experimental Brain Research.

[31]  R. Johansson,et al.  Hand Movements , 2001 .

[32]  Alan M. Wing,et al.  Time-based prediction in motor control: evidence from grip force response to external load perturbations , 2006, Experimental Brain Research.

[33]  A M Wing,et al.  Efficiency of Grip Force Adjustments for Impulsive Loading during Imposed and Actively Produced Collisions , 2003, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[34]  Daniel M. Wolpert,et al.  The effect of externally generated loading on predictive grip force modulation , 2007, Neuroscience Letters.

[35]  R. Ivry,et al.  Anticipatory adjustments in the unloading task: Is an efference copy necessary for learning? , 2002, Experimental Brain Research.

[36]  Alan M. Wing,et al.  Anticipatory Control of Grip Force in Rapid Arm Movement , 1996 .

[37]  J. Flanagan,et al.  Modulation of grip force with load force during point-to-point arm movements , 2004, Experimental Brain Research.

[38]  V. Ramachandran,et al.  Encyclopedia of the Human Brain , 2002 .

[39]  S Glasauer,et al.  The effects of digital anaesthesia on predictive grip force adjustments during vertical movements of a grasped object , 2001, The European journal of neuroscience.

[40]  Stefan Glasauer,et al.  Moving objects in a rotating environment: rapid prediction of Coriolis and centrifugal force perturbations , 2004, Experimental Brain Research.

[41]  Roland S Johansson,et al.  Predictions Specify Reactive Control of Individual Digits in Manipulation , 2002, The Journal of Neuroscience.

[42]  Yukari Ohki,et al.  Dependence of reactive responses in human bimanual finger movements on sensory feedback and auditory cues. , 2004, Journal of neurophysiology.

[43]  A. G. Witney,et al.  Predictive motor learning of temporal delays. , 1999, Journal of neurophysiology.

[44]  T. Lejeune,et al.  Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects. , 2003, Journal of neurophysiology.