Digit Position and Forces Covary during Anticipatory Control of Whole-Hand Manipulation

Theoretical perspectives on anticipatory planning of object manipulation have traditionally been informed by studies that have investigated kinematics (hand shaping and digit position) and kinetics (forces) in isolation. This poses limitations on our understanding of the integration of such domains, which have recently been shown to be strongly interdependent. Specifically, recent studies revealed strong covariation of digit position and load force during the loading phase of two-digit grasping. Here, we determined whether such digit force-position covariation is a general feature of grasping. We investigated the coordination of digit position and forces during five-digit whole-hand manipulation of an object with a variable mass distribution. Subjects were instructed to prevent object roll during the lift. As found in precision grasping, there was strong trial-to-trial covariation of digit position and force. This suggests that the natural variation of digit position that is compensated for by trial-to-trial variation in digit forces is a fundamental feature of grasp control, and not only specific to precision grasp. However, a main difference with precision grasping was that modulation of digit position to the object’s mass distribution was driven predominantly by the thumb, with little to no modulation of finger position. Modulation of thumb position rather than fingers is likely due to its greater range of motion and therefore adaptability to object properties. Our results underscore the flexibility of the central nervous system in implementing a range of solutions along the digit force-to-position continuum for dexterous manipulation.

[1]  M. Santello,et al.  Force synergies for multifingered grasping: effect of predictability in object center of mass and handedness , 2002, Experimental Brain Research.

[2]  Andrew M. Gordon,et al.  Initiation and development of fingertip forces during whole-hand grasping , 2001, Experimental Brain Research.

[3]  Gabriel Baud-Bovy,et al.  Neural bases of hand synergies , 2013, Front. Comput. Neurosci..

[4]  K. J. Cole,et al.  Coordination of three-joint digit movements for rapid finger-thumb grasp. , 1986, Journal of neurophysiology.

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

[6]  J. Flanagan,et al.  Sensorimotor memory of weight asymmetry in object manipulation , 2007, Experimental Brain Research.

[7]  Jae Kun Shim,et al.  Prehension synergies in three dimensions. , 2005, Journal of neurophysiology.

[8]  Fan Gao,et al.  Finger force vectors in multi-finger prehension. , 2003, Journal of biomechanics.

[9]  Marco Santello,et al.  Effects of Visual Cues of Object Density on Perception and Anticipatory Control of Dexterous Manipulation , 2013, PloS one.

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

[11]  Mark L Latash,et al.  Multifinger Prehension: An Overview , 2008, Journal of motor behavior.

[12]  R. Cohen,et al.  Where grasps are made reveals how grasps are planned: generation and recall of motor plans , 2004, Experimental Brain Research.

[13]  Marco Santello,et al.  Coordination between digit forces and positions: interactions between anticipatory and feedback control. , 2014, Journal of neurophysiology.

[14]  M. Jeannerod The timing of natural prehension movements. , 1984, Journal of motor behavior.

[15]  K. Lashley Basic Neural Mechanisms in Behavior , 2009 .

[16]  Umberto Castiello,et al.  Insights into the reach to grasp movement , 1994 .

[17]  J. F. Soechting,et al.  Force synergies for multifingered grasping , 2000, Experimental Brain Research.

[18]  R. Johansson,et al.  Visual size cues in the programming of manipulative forces during precision grip , 2004, Experimental Brain Research.

[19]  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.

[20]  M. Davare,et al.  Temporal Dissociation between Hand Shaping and Grip Force Scaling in the Anterior Intraparietal Area , 2007, The Journal of Neuroscience.

[21]  Marco Santello,et al.  Generalization of Dexterous Manipulation Is Sensitive to the Frame of Reference in Which It Is Learned , 2015, PloS one.

[22]  Mark Latash,et al.  Tangential load sharing among fingers during prehension , 2004, Ergonomics.

[23]  A. Gordon,et al.  Selective use of visual information signaling objects' center of mass for anticipatory control of manipulative fingertip forces , 2003, Experimental Brain Research.

[24]  J. F. Soechting,et al.  Gradual molding of the hand to object contours. , 1998, Journal of neurophysiology.

[25]  Marco Santello,et al.  Choice of Contact Points during Multidigit Grasping: Effect of Predictability of Object Center of Mass Location , 2007, The Journal of Neuroscience.

[26]  Marco Santello,et al.  Patterns of Hand Motion during Grasping and the Influence of Sensory Guidance , 2002, The Journal of Neuroscience.

[27]  A. Landi Human Hand Function , 2007 .

[28]  M. Santello,et al.  Anticipatory Planning and Control of Grasp Positions and Forces for Dexterous Two-Digit Manipulation , 2010, The Journal of Neuroscience.

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

[30]  M. Santello,et al.  Effects of end-goal on hand shaping. , 2006, Journal of neurophysiology.

[31]  R. Johansson,et al.  Responses in glabrous skin mechanoreceptors during precision grip in humans , 2004, Experimental Brain Research.

[32]  Marco Santello,et al.  Manipulation after object rotation reveals independent sensorimotor memory representations of digit positions and forces. , 2010, Journal of neurophysiology.

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

[34]  H. Forssberg,et al.  The integration of haptically acquired size information in the programming of precision grip , 2004, Experimental Brain Research.

[35]  U. Castiello,et al.  Differential cortical activity for precision and whole‐hand visually guided grasping in humans , 2007, The European journal of neuroscience.