Literature DB >> 33326349

Information about contact force and surface texture is mixed in the firing rates of cutaneous afferent neurons.

Monica Liu1,2,3, Aaron Batista2,3, Sliman Bensmaia4, Douglas J Weber3,5,6.   

Abstract

Cutaneous mechanoreceptors in our hands gather information about the objects we handle. Tactile fibers encode mixed information about contact events and object properties. Neural coding in tactile afferents is typically studied by varying a single aspect of tactile stimuli, avoiding the confounds of real-world haptic interactions. We instead record responses of small populations of dorsal root ganglia (DRG) neurons to variable tactile stimuli and find that neurons primarily respond to force, though some texture information can be detected. Tactile nerve fibers convey information about many features of haptic interactions, including the force and speed of contact, as well as the texture and shape of the objects being handled. How we perceive these object features is relatively unaffected by the forces and movements we use when interacting with the object. Because signals related to contact events and object properties are mixed in the responses of tactile fibers, our ability to disentangle these different components of our tactile experience implies that they are demultiplexed as they propagate along the neuraxis. To understand how texture and contact mechanics are encoded together by tactile fibers, we studied the activity of multiple neurons recorded simultaneously in the cervical DRG of two anesthetized rhesus monkeys while textured surfaces were applied to the glabrous skin of the fingers and palm using a handheld probe. A transducer at the tip of the textured probe measured contact forces as tactile stimuli were applied at different locations on the finger-pads and palm. We examined how a sample population of DRG neurons encode force and texture and found that firing rates of individual neurons are modulated by both force and texture. In particular, slowly adapting (SA) neurons were more responsive to force than texture, and rapidly adapting (RA) neurons were more responsive to texture than force. Although force could be decoded accurately throughout the entire contact interval, texture signals were most salient during onset and offset phases of the contact interval.NEW & NOTEWORTHY Cutaneous mechanoreceptors in our hands gather information about the objects we handle. Tactile fibers encode mixed information about contact events and object properties. Neural coding in tactile afferents is typically studied by varying a single aspect of tactile stimuli, avoiding the confounds of real-world haptic interactions. We instead record responses of small populations of DRG neurons to variable tactile stimuli and find that neurons primarily respond to force, though some texture information can be detected.

Entities:  

Keywords:  cutaneous; dorsal root ganglia; mechanoreceptor; nonhuman primate; sensory

Mesh:

Year:  2020        PMID: 33326349      PMCID: PMC7948138          DOI: 10.1152/jn.00725.2019

Source DB:  PubMed          Journal:  J Neurophysiol        ISSN: 0022-3077            Impact factor:   2.714


  43 in total

1.  Neural coding of tactile texture: comparison of spatial and temporal mechanisms for roughness perception.

Authors:  C E Connor; K O Johnson
Journal:  J Neurosci       Date:  1992-09       Impact factor: 6.167

2.  Cutaneous afferents from the monkeys fingers: responses to tangential and normal forces.

Authors:  H E Wheat; L M Salo; A W Goodwin
Journal:  J Neurophysiol       Date:  2009-12-02       Impact factor: 2.714

3.  Monkey cutaneous SAI and RA responses to raised and depressed scanned patterns: effects of width, height, orientation, and a raised surround.

Authors:  D T Blake; K O Johnson; S S Hsiao
Journal:  J Neurophysiol       Date:  1997-11       Impact factor: 2.714

4.  Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand.

Authors:  R S Johansson; A B Vallbo
Journal:  J Physiol       Date:  1979-12       Impact factor: 5.182

5.  A model accounting for effects of vibratory amplitude on responses of cutaneous mechanoreceptors in macaque monkey.

Authors:  A W Freeman; K O Johnson
Journal:  J Physiol       Date:  1982-02       Impact factor: 5.182

6.  Neural mechanisms of spatial tactile discrimination: neural patterns evoked by braille-like dot patterns in the monkey.

Authors:  K O Johnson; G D Lamb
Journal:  J Physiol       Date:  1981-01       Impact factor: 5.182

7.  Importance of cutaneous feedback in maintaining a secure grip during manipulation of hand-held objects.

Authors:  Anne-Sophie Augurelle; Allan M Smith; Thierry Lejeune; Jean-Louis Thonnard
Journal:  J Neurophysiol       Date:  2003-02       Impact factor: 2.714

8.  The neural coding of stimulus intensity: linking the population response of mechanoreceptive afferents with psychophysical behavior.

Authors:  Michael A Muniak; Supratim Ray; Steven S Hsiao; J Frank Dammann; Sliman J Bensmaia
Journal:  J Neurosci       Date:  2007-10-24       Impact factor: 6.167

9.  Temporary Nerve Block at Selected Digits Revealed Hand Motor Deficits in Grasping Tasks.

Authors:  Aude Carteron; Kerry McPartlan; Christina Gioeli; Emily Reid; Matt Turturro; Barry Hahn; Cynthia Benson; Wei Zhang
Journal:  Front Hum Neurosci       Date:  2016-11-25       Impact factor: 3.169

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

Authors:  Benoit P Delhaye; Molly K O'Donnell; Justin D Lieber; Kristine R McLellan; Sliman J Bensmaia
Journal:  PLoS Biol       Date:  2019-08-27       Impact factor: 8.029

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