Feeling fooled: Texture contaminates the neural code for tactile speed.

Motion is an essential component of everyday tactile experience: most manual interactions involve relative movement between the skin and objects. Much of the research on the neural basis of tactile motion perception has focused on how direction is encoded, but less is known about how speed is. Perce...

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Main Authors: Benoit P Delhaye, Molly K O'Donnell, Justin D Lieber, Kristine R McLellan, Sliman J Bensmaia
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-08-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000431
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author Benoit P Delhaye
Molly K O'Donnell
Justin D Lieber
Kristine R McLellan
Sliman J Bensmaia
author_facet Benoit P Delhaye
Molly K O'Donnell
Justin D Lieber
Kristine R McLellan
Sliman J Bensmaia
author_sort Benoit P Delhaye
collection DOAJ
description Motion is an essential component of everyday tactile experience: most manual interactions involve relative movement between the skin and objects. Much of the research on the neural basis of tactile motion perception has focused on how direction is encoded, but less is known about how speed is. Perceived speed has been shown to be dependent on surface texture, but previous studies used only coarse textures, which span a restricted range of tangible spatial scales and provide a limited window into tactile coding. To fill this gap, we measured the ability of human observers to report the speed of natural textures-which span the range of tactile experience and engage all the known mechanisms of texture coding-scanned across the skin. In parallel experiments, we recorded the responses of single units in the nerve and in the somatosensory cortex of primates to the same textures scanned at different speeds. We found that the perception of speed is heavily influenced by texture: some textures are systematically perceived as moving faster than are others, and some textures provide a more informative signal about speed than do others. Similarly, the responses of neurons in the nerve and in cortex are strongly dependent on texture. In the nerve, although all fibers exhibit speed-dependent responses, the responses of Pacinian corpuscle-associated (PC) fibers are most strongly modulated by speed and can best account for human judgments. In cortex, approximately half of the neurons exhibit speed-dependent responses, and this subpopulation receives strong input from PC fibers. However, speed judgments seem to reflect an integration of speed-dependent and speed-independent responses such that the latter help to partially compensate for the strong texture dependence of the former.
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spelling doaj.art-1a534443d58d47a8b28552887e9d87a32022-12-21T21:24:31ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-08-01178e300043110.1371/journal.pbio.3000431Feeling fooled: Texture contaminates the neural code for tactile speed.Benoit P DelhayeMolly K O'DonnellJustin D LieberKristine R McLellanSliman J BensmaiaMotion is an essential component of everyday tactile experience: most manual interactions involve relative movement between the skin and objects. Much of the research on the neural basis of tactile motion perception has focused on how direction is encoded, but less is known about how speed is. Perceived speed has been shown to be dependent on surface texture, but previous studies used only coarse textures, which span a restricted range of tangible spatial scales and provide a limited window into tactile coding. To fill this gap, we measured the ability of human observers to report the speed of natural textures-which span the range of tactile experience and engage all the known mechanisms of texture coding-scanned across the skin. In parallel experiments, we recorded the responses of single units in the nerve and in the somatosensory cortex of primates to the same textures scanned at different speeds. We found that the perception of speed is heavily influenced by texture: some textures are systematically perceived as moving faster than are others, and some textures provide a more informative signal about speed than do others. Similarly, the responses of neurons in the nerve and in cortex are strongly dependent on texture. In the nerve, although all fibers exhibit speed-dependent responses, the responses of Pacinian corpuscle-associated (PC) fibers are most strongly modulated by speed and can best account for human judgments. In cortex, approximately half of the neurons exhibit speed-dependent responses, and this subpopulation receives strong input from PC fibers. However, speed judgments seem to reflect an integration of speed-dependent and speed-independent responses such that the latter help to partially compensate for the strong texture dependence of the former.https://doi.org/10.1371/journal.pbio.3000431
spellingShingle Benoit P Delhaye
Molly K O'Donnell
Justin D Lieber
Kristine R McLellan
Sliman J Bensmaia
Feeling fooled: Texture contaminates the neural code for tactile speed.
PLoS Biology
title Feeling fooled: Texture contaminates the neural code for tactile speed.
title_full Feeling fooled: Texture contaminates the neural code for tactile speed.
title_fullStr Feeling fooled: Texture contaminates the neural code for tactile speed.
title_full_unstemmed Feeling fooled: Texture contaminates the neural code for tactile speed.
title_short Feeling fooled: Texture contaminates the neural code for tactile speed.
title_sort feeling fooled texture contaminates the neural code for tactile speed
url https://doi.org/10.1371/journal.pbio.3000431
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