Abstract

While skin, joints and muscles receptors alone provide lower level information about individual variables (e.g., exerted limb force and limb displacement), the distance between limb endpoints (i.e., relative position) has to be extracted from high level integration of somatosensory and motor signals. In particular, estimation of fingertip relative position likely involves more complex sensorimotor transformations than those underlying hand or arm position sense: the brain has to estimate where each fingertip is relative to the hand and where fingertips are relative to each other. It has been demonstrated that during grasping, feedback of digit position drives rapid adjustments of fingers force control. However, it has been shown that estimation of fingertips' relative position can be biased by digit forces. These findings raise the question of how the brain combines concurrent tactile (i.e., cutaneous mechanoreceptors afferents induced by skin pressure and stretch) and non-tactile (i.e., both descending motor command and joint/muscle receptors signals associated to muscle contraction) digit force-related inputs for fingertip distance estimation. Here we addressed this question by quantifying the contribution of tactile and non-tactile force-related inputs for the estimation of fingertip relative position. We asked subjects to match fingertip vertical distance relying only on either tactile or non-tactile inputs from the thumb and index fingertip, and compared their performance with the condition where both types of inputs were combined. We found that (a) the bias in the estimation of fingertip distance persisted when tactile inputs and non-tactile force-related signals were presented in isolation; (b) tactile signals contributed the most to the estimation of fingertip distance; (c) linear summation of the matching errors relying only on either tactile or non-tactile inputs was comparable to the matching error when both inputs were simultaneously available. These findings reveal a greater role of tactile signals for sensing fingertip distance and suggest a linear integration mechanism with non-tactile inputs for the estimation of fingertip relative position.

Highlights

  • The central nervous system (CNS) has a remarkable ability to rapidly integrate sensory feedback of digit position with motor commands for force control (Fu et al, 2010, 2011)

  • Due to the lack of dedicated sensory receptors encoding distance between limb endpoints, in absence of vision, estimation of fingertip position requires processing of information conveyed by at least three different sensory or sensorimotor inputs: (a) tactile cues arising from mechanical deformation of the finger pads; (b) proprioceptive inputs triggered by changes in length and tension of the muscle-tendon complex, and joint angle; (c) and a copy of the motor command responsible for fingers placements and contact forces, i.e., efference copy

  • The role of motor commands for estimation of relative finger position has been explored in our previous work by asking subjects to perform a digit position matching task after exerting large normal and tangential forces against a contact surface, involving tactile input, proprioceptive input, and efference copy (Shibata et al, 2014)

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Summary

Introduction

The central nervous system (CNS) has a remarkable ability to rapidly integrate sensory feedback of digit position with motor commands for force control (Fu et al, 2010, 2011). Cutaneous receptors can provide information about the magnitude and direction of force acting on the finger pad (Birznieks et al, 2001; Jenmalm et al, 2003; Panarese and Edin, 2011; see Johansson and Flanagan, 2009 for a review) This ability to encode forcerelated inputs allows the CNS to gather exteroceptive cues necessary to estimate object features, e.g., object compliance, size, and hand configuration (Longo et al, 2010). The thumb was placed higher than the index fingertip when thumb and index finger tangential forces were directed upward and downward, respectively, and vice versa This suggests that the efference copy overrode the information provided by afferents signals about fingertips’ relative position. This result raised important questions regarding the CNS’ limited ability to integrate feedback from tactile and proprioceptive inputs with efference copy, and their relative contribution to the estimation of fingertip distance

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