Literature DB >> 28652360

Simulating tactile signals from the whole hand with millisecond precision.

Hannes P Saal1,2, Benoit P Delhaye1, Brandon C Rayhaun1, Sliman J Bensmaia3.   

Abstract

When we grasp and manipulate an object, populations of tactile nerve fibers become activated and convey information about the shape, size, and texture of the object and its motion across the skin. The response properties of tactile fibers have been extensively characterized in single-unit recordings, yielding important insights into how individual fibers encode tactile information. A recurring finding in this extensive body of work is that stimulus information is distributed over many fibers. However, our understanding of population-level representations remains primitive. To fill this gap, we have developed a model to simulate the responses of all tactile fibers innervating the glabrous skin of the hand to any spatiotemporal stimulus applied to the skin. The model first reconstructs the stresses experienced by mechanoreceptors when the skin is deformed and then simulates the spiking response that would be produced in the nerve fiber innervating that receptor. By simulating skin deformations across the palmar surface of the hand and tiling it with receptors at their known densities, we reconstruct the responses of entire populations of nerve fibers. We show that the simulated responses closely match their measured counterparts, down to the precise timing of the evoked spikes, across a wide variety of experimental conditions sampled from the literature. We then conduct three virtual experiments to illustrate how the simulation can provide powerful insights into population coding in touch. Finally, we discuss how the model provides a means to establish naturalistic artificial touch in bionic hands.

Entities:  

Keywords:  computational model; mechanoreceptor; skin mechanics; somatosensory periphery; tactile afferent

Mesh:

Year:  2017        PMID: 28652360      PMCID: PMC5514748          DOI: 10.1073/pnas.1704856114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  69 in total

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Authors:  J W Bisley; A W Goodwin; H E Wheat
Journal:  J Neurophysiol       Date:  2000-07       Impact factor: 2.714

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Authors:  M Knibestöl
Journal:  J Physiol       Date:  1975-02       Impact factor: 5.182

3.  A structural fingertip model for simulating of the biomechanics of tactile sensation.

Authors:  J Z Wu; R G Dong; S Rakheja; A W Schopper; W P Smutz
Journal:  Med Eng Phys       Date:  2004-03       Impact factor: 2.242

4.  Spatiotemporal receptive fields of peripheral afferents and cortical area 3b and 1 neurons in the primate somatosensory system.

Authors:  Arun P Sripati; Takashi Yoshioka; Peter Denchev; Steven S Hsiao; Kenneth O Johnson
Journal:  J Neurosci       Date:  2006-02-15       Impact factor: 6.167

5.  Properties of cutaneous mechanoreceptors in the human hand related to touch sensation.

Authors:  A B Vallbo; R S Johansson
Journal:  Hum Neurobiol       Date:  1984

6.  Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements.

Authors:  R S Johansson; U Landström; R Lundström
Journal:  Brain Res       Date:  1982-07-22       Impact factor: 3.252

7.  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

8.  Reconstruction of population response to a vibratory stimulus in quickly adapting mechanoreceptive afferent fiber population innervating glabrous skin of the monkey.

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Journal:  J Neurophysiol       Date:  1974-01       Impact factor: 2.714

9.  Texture perception through direct and indirect touch: an analysis of perceptual space for tactile textures in two modes of exploration.

Authors:  T Yoshioka; S J Bensmaïa; J C Craig; S S Hsiao
Journal:  Somatosens Mot Res       Date:  2007 Mar-Jun       Impact factor: 1.111

10.  Surface strain measurements of fingertip skin under shearing.

Authors:  Benoit Delhaye; Allan Barrea; Benoni B Edin; Philippe Lefèvre; Jean-Louis Thonnard
Journal:  J R Soc Interface       Date:  2016-02       Impact factor: 4.118

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  43 in total

1.  Human touch receptors are sensitive to spatial details on the scale of single fingerprint ridges.

Authors:  Ewa Jarocka; J Andrew Pruszynski; Roland S Johansson
Journal:  J Neurosci       Date:  2021-03-15       Impact factor: 6.167

2.  Rapid geometric feature signaling in the simulated spiking activity of a complete population of tactile nerve fibers.

Authors:  Benoit P Delhaye; Xinyue Xia; Sliman J Bensmaia
Journal:  J Neurophysiol       Date:  2019-04-03       Impact factor: 2.714

3.  Neural Coding of Contact Events in Somatosensory Cortex.

Authors:  Thierri Callier; Aneesha K Suresh; Sliman J Bensmaia
Journal:  Cereb Cortex       Date:  2019-12-17       Impact factor: 5.357

4.  Tactile perception of the roughness of 3D-printed textures.

Authors:  Chelsea Tymms; Denis Zorin; Esther P Gardner
Journal:  J Neurophysiol       Date:  2017-11-22       Impact factor: 2.714

5.  Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain.

Authors:  Luke E Osborn; Andrei Dragomir; Joseph L Betthauser; Christopher L Hunt; Harrison H Nguyen; Rahul R Kaliki; Nitish V Thakor
Journal:  Sci Robot       Date:  2018-06-20

6.  Biomimetic encoding model for restoring touch in bionic hands through a nerve interface.

Authors:  Elizaveta V Okorokova; Qinpu He; Sliman J Bensmaia
Journal:  J Neural Eng       Date:  2018-09-24       Impact factor: 5.379

7.  A dynamical model for generating synthetic data to quantify active tactile sensing behavior in the rat.

Authors:  Nadina O Zweifel; Nicholas E Bush; Ian Abraham; Todd D Murphey; Mitra J Z Hartmann
Journal:  Proc Natl Acad Sci U S A       Date:  2021-07-06       Impact factor: 11.205

Review 8.  Of mice and monkeys: Somatosensory processing in two prominent animal models.

Authors:  Daniel H O'Connor; Leah Krubitzer; Sliman Bensmaia
Journal:  Prog Neurobiol       Date:  2021-02-12       Impact factor: 11.685

9.  High-resolution imaging of skin deformation shows that afferents from human fingertips signal slip onset.

Authors:  Benoit P Delhaye; Ewa Jarocka; Allan Barrea; Jean-Louis Thonnard; Benoni Edin; Philippe Lefèvre
Journal:  Elife       Date:  2021-04-22       Impact factor: 8.140

10.  Temporal coherency of mechanical stimuli modulates tactile form perception.

Authors:  Masashi Nakatani; Yasuaki Kobayashi; Kota Ohno; Masaaki Uesaka; Sayako Mogami; Zixia Zhao; Takamichi Sushida; Hiroyuki Kitahata; Masaharu Nagayama
Journal:  Sci Rep       Date:  2021-06-03       Impact factor: 4.379

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