Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity

We can easily and without sight bring our fingertip to our nose, or swat a mosquito on our arm. These actions rely on proprioception, also known as kinesthesia, which classically has been attributed to processing of sensory inflow by the CNS. However, internal model theories of sensorimotor neurosci...

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Main Authors: Warren G. Darling, Brian M. Wall, Chris R. Coffman, Charles Capaday
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-05-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fnhum.2018.00177/full
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author Warren G. Darling
Brian M. Wall
Chris R. Coffman
Charles Capaday
author_facet Warren G. Darling
Brian M. Wall
Chris R. Coffman
Charles Capaday
author_sort Warren G. Darling
collection DOAJ
description We can easily and without sight bring our fingertip to our nose, or swat a mosquito on our arm. These actions rely on proprioception, also known as kinesthesia, which classically has been attributed to processing of sensory inflow by the CNS. However, internal model theories of sensorimotor neuroscience propose that proprioceptive localization also involves a contribution from estimates of limb kinematics derived from motor commands. We tested this prediction in 19 subjects who moved the right index finger tip to touch the moving left index finger tip under three conditions: (1) vision allowed, active movement of the left hand (2) vision blocked, active movement of the left hand, and (3) vision blocked, passive movement of the left hand imposed by the experimenter. The target left index finger tip was moved in a wide range of directions by unrestricted movements of the arm. Mean errors in apposition of the right to the left index finger tips were small, averaging <2 cm between sensors fixed to the finger nails. Note that the average distance between the sensors was ~1.7 cm when the fingertips were brought together in “perfect” apposition under visual guidance. The 3D mean distance and variable distance errors were marginally lower by some 2 mm with eyes open compared to the eyes closed active condition. However, mean distance and variable distance errors did not differ between the active and passive conditions with eyes closed. Thus, proprioceptive localization of one's moving hand is very accurate, essentially as accurate as when vision is allowed. More importantly, our results demonstrate that hypothesized internal model derived estimates of arm kinematics do not contribute to localization accuracy beyond that provided by sensory signals, casting doubt on their existence.
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spelling doaj.art-32506e524d07464a9a25251710b2a9c32022-12-22T03:49:50ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-05-011210.3389/fnhum.2018.00177312566Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive AcuityWarren G. Darling0Brian M. Wall1Chris R. Coffman2Charles Capaday3Motor Control Laboratories, Department of Health and Human Physiology, University of Iowa, Iowa City, IA, United StatesMotor Control Laboratories, Department of Health and Human Physiology, University of Iowa, Iowa City, IA, United StatesMotor Control Laboratories, Department of Health and Human Physiology, University of Iowa, Iowa City, IA, United StatesBernstein Center for Computational Neuroscience, Bernstein Focus Neurotechnology Göttingen, Institute of Neurorehabilitation Engineering, Universitätsmedizin Göttingen, Georg-August-University, Göttingen, GermanyWe can easily and without sight bring our fingertip to our nose, or swat a mosquito on our arm. These actions rely on proprioception, also known as kinesthesia, which classically has been attributed to processing of sensory inflow by the CNS. However, internal model theories of sensorimotor neuroscience propose that proprioceptive localization also involves a contribution from estimates of limb kinematics derived from motor commands. We tested this prediction in 19 subjects who moved the right index finger tip to touch the moving left index finger tip under three conditions: (1) vision allowed, active movement of the left hand (2) vision blocked, active movement of the left hand, and (3) vision blocked, passive movement of the left hand imposed by the experimenter. The target left index finger tip was moved in a wide range of directions by unrestricted movements of the arm. Mean errors in apposition of the right to the left index finger tips were small, averaging <2 cm between sensors fixed to the finger nails. Note that the average distance between the sensors was ~1.7 cm when the fingertips were brought together in “perfect” apposition under visual guidance. The 3D mean distance and variable distance errors were marginally lower by some 2 mm with eyes open compared to the eyes closed active condition. However, mean distance and variable distance errors did not differ between the active and passive conditions with eyes closed. Thus, proprioceptive localization of one's moving hand is very accurate, essentially as accurate as when vision is allowed. More importantly, our results demonstrate that hypothesized internal model derived estimates of arm kinematics do not contribute to localization accuracy beyond that provided by sensory signals, casting doubt on their existence.http://journal.frontiersin.org/article/10.3389/fnhum.2018.00177/fullkinesthesiaproprioceptionhandkinematicsinternal model
spellingShingle Warren G. Darling
Brian M. Wall
Chris R. Coffman
Charles Capaday
Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
Frontiers in Human Neuroscience
kinesthesia
proprioception
hand
kinematics
internal model
title Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
title_full Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
title_fullStr Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
title_full_unstemmed Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
title_short Pointing to One's Moving Hand: Putative Internal Models Do Not Contribute to Proprioceptive Acuity
title_sort pointing to one s moving hand putative internal models do not contribute to proprioceptive acuity
topic kinesthesia
proprioception
hand
kinematics
internal model
url http://journal.frontiersin.org/article/10.3389/fnhum.2018.00177/full
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