Encoding of tangential torque in responses of tactile afferent fibres innervating the fingerpad of the monkey

Torsional loads are ubiquitous during everyday dextrous manipulations. We examined how information about torque is provided to the sensorimotor control system by populations of tactile afferents. Torsional loads of different magnitudes were applied in clockwise and anticlockwise directions to a standard central site on the fingertip. Three different background levels of contact (grip) force were used. The median nerve was exposed in anaesthetized monkeys and single unit responses recorded from 66 slowly adapting type‐I (SA‐I) and 31 fast adapting type‐I (FA‐I) afferents innervating the distal segments of the fingertips. Most afferents were excited by torque but some were suppressed. Responses of the majority of both afferent types were scaled by torque magnitude applied in one or other direction, with the majority of FA‐I afferent responses and about half of SA‐I afferent responses scaled in both directions. Torque direction affected responses in both afferent types, but more so for the SA‐I afferents. Latencies of the first spike in FA‐I afferent responses depended on the parameters of the torque. We used a Parzen window classifier to assess the capacity of the SA‐I and FA‐I afferent populations to discriminate, concurrently and in real‐time, the three stimulus parameters, namely background normal force, torque magnitude and direction. Despite the potentially confounding interactions between stimulus parameters, both the SA‐I and the FA‐I populations could extract torque magnitude accurately. The FA‐I afferents signalled torque magnitude earlier than did the SA‐I afferents, but torque direction was extracted more rapidly and more accurately by the SA‐I afferent population.

[1]  R. Johansson,et al.  First spikes in ensembles of human tactile afferents code complex spatial fingertip events , 2004, Nature Neuroscience.

[2]  G. Honderd,et al.  Shear force measurement using a rubber based tactile matrix sensor , 1997, 1997 8th International Conference on Advanced Robotics. Proceedings. ICAR'97.

[3]  Arnaud Delorme,et al.  Spike-based strategies for rapid processing , 2001, Neural Networks.

[4]  R. Johansson,et al.  Control of grasp stability in humans under different frictional conditions during multidigit manipulation. , 1999, Journal of neurophysiology.

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

[6]  Thomas Elbert,et al.  Semantic Categorization in the Human Brain , 2003, Psychological science.

[7]  R. Johansson,et al.  Encoding of Direction of Fingertip Forces by Human Tactile Afferents , 2001, The Journal of Neuroscience.

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

[9]  R. Johansson,et al.  Control of grasp stability during pronation and supination movements , 1999, Experimental Brain Research.

[10]  K. O. Johnson,et al.  Tactile spatial resolution. II. Neural representation of Bars, edges, and gratings in monkey primary afferents. , 1981, Journal of neurophysiology.

[11]  G. Drummond Reporting ethical matters in The Journal of Physiology: standards and advice , 2009, The Journal of physiology.

[12]  Allan M Smith,et al.  The effects of digital anesthesia on force control using a precision grip. , 2003, Journal of neurophysiology.

[13]  C. Carr,et al.  Evolution and development of time coding systems , 2001, Current Opinion in Neurobiology.

[14]  K. O. Johnson,et al.  Reconstruction of population response to a vibratory stimulus in quickly adapting mechanoreceptive afferent fiber population innervating glabrous skin of the monkey. , 1974, Journal of neurophysiology.

[15]  J Gautrais,et al.  Rate coding versus temporal order coding: a theoretical approach. , 1998, Bio Systems.

[16]  R. Johansson,et al.  Tangential torque effects on the control of grip forces when holding objects with a precision grip. , 1997, Journal of neurophysiology.

[17]  R. Johansson,et al.  Control of Grip Force When Tilting Objects: Effect of Curvature of Grasped Surfaces and Applied Tangential Torque , 1998, The Journal of Neuroscience.

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

[19]  R S Johansson,et al.  Grasp stability during manipulative actions. , 1994, Canadian journal of physiology and pharmacology.

[20]  M. Srinivasan,et al.  Tactile discrimination of shape: responses of slowly and rapidly adapting mechanoreceptive afferents to a step indented into the monkey fingerpad , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  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.

[22]  A. Wing,et al.  Anticipating load torques produced by voluntary movements. , 1998, Journal of experimental psychology. Human perception and performance.

[23]  R. Johansson,et al.  Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. , 1984, Human neurobiology.

[24]  M. Srinivasan,et al.  Encoding of shape and orientation of objects indented into the monkey fingerpad by populations of slowly and rapidly adapting mechanoreceptors. , 1998, Journal of neurophysiology.

[25]  Vladimir M. Zatsiorsky,et al.  Adjustments of prehension synergies in response to self-triggered and experimenter-triggered load and torque perturbations , 2006, Experimental Brain Research.

[26]  D V Buonomano,et al.  Decoding Temporal Information: A Model Based on Short-Term Synaptic Plasticity , 2000, The Journal of Neuroscience.

[27]  A. Goodwin,et al.  Peripheral Neural Mechanisms Determining the Orientation of Cylinders Grasped by the Digits , 1998, The Journal of Neuroscience.

[28]  A. Goodwin,et al.  Slowly adapting type I afferents from the sides and end of the finger respond to stimuli on the center of the fingerpad. , 2000, Journal of neurophysiology.

[29]  R S Johansson,et al.  Control of fingertip forces in multidigit manipulation. , 1999, Journal of neurophysiology.

[30]  Vincent Hayward,et al.  Experimental Evidence of Lateral Skin Strain During Tactile Exploration , 2003 .

[31]  David G. Stork,et al.  Pattern classification, 2nd Edition , 2000 .

[32]  R Van Rullen,et al.  Face processing using one spike per neurone. , 1998, Bio Systems.

[33]  Ingvars Birznieks,et al.  Influence of object shape on responses of human tactile afferents under conditions characteristic of manipulation , 2003, The European journal of neuroscience.

[34]  Ryan M Carey,et al.  Rapid Encoding and Perception of Novel Odors in the Rat , 2008, PLoS biology.

[35]  M. Latash,et al.  Effects of friction at the digit-object interface on the digit forces in multi-finger prehension , 2006, Experimental Brain Research.

[36]  T. Lejeune,et al.  Paradoxical effect of digital anaesthesia on force and corticospinal excitability , 2005, Neuroreport.

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

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

[39]  M. Diamond,et al.  Population coding in somatosensory cortex , 2002, Current Opinion in Neurobiology.

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

[41]  R. Johansson,et al.  Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip , 2004, Experimental Brain Research.

[42]  Rufin van Rullen,et al.  Rate Coding Versus Temporal Order Coding: What the Retinal Ganglion Cells Tell the Visual Cortex , 2001, Neural Computation.

[43]  A. Goodwin,et al.  Representation of curved surfaces in responses of mechanoreceptive afferent fibers innervating the monkey's fingerpad , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  S. Gepshtein,et al.  The combination of vision and touch depends on spatial proximity. , 2005, Journal of vision.

[45]  R. Johansson,et al.  Slowly Adapting Mechanoreceptors in the Borders of the Human Fingernail Encode Fingertip Forces , 2009, The Journal of Neuroscience.

[46]  J. Thonnard,et al.  A continuous measure of fingertip friction during precision grip , 2009, Journal of Neuroscience Methods.

[47]  Jae Kun Shim,et al.  Rotational equilibrium during multi-digit pressing and prehension. , 2004, Motor control.

[48]  D. Nowak,et al.  Grip force efficiency in long-term deprivation of somatosensory feedback , 2003, Neuroreport.

[49]  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.

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

[51]  Imin Kao,et al.  The sliding of robot fingers under combined torsion and shear loading , 1988, Proceedings. 1988 IEEE International Conference on Robotics and Automation.

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

[53]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[54]  N. Wittenburg,et al.  Transformation from temporal to rate coding in a somatosensory thalamocortical pathway , 2022 .

[55]  K. O. Johnson,et al.  SA1 and RA receptive fields, response variability, and population responses mapped with a probe array. , 1999, Journal of neurophysiology.