Literature DB >> 33722975

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

Ewa Jarocka1, J Andrew Pruszynski2,3, Roland S Johansson2.   

Abstract

Fast-adapting type 1 (FA-1) and slowly-adapting type 1 (SA-1) first-order tactile neurons provide detailed spatiotemporal tactile information when we touch objects with fingertips. The distal axon of these neuron types branches in the skin and innervates many receptor organs associated with fingerprint ridges (Meissner corpuscles and Merkel cell neurite complexes, respectively), resulting in heterogeneous receptive fields whose sensitivity topography includes many highly sensitive zones or 'subfields'. In experiments on humans of both sexes, using raised dots that tangentially scanned the receptive field we examined the spatial acuity of the subfields of FA-1 and SA-1 neurons and its constancy across scanning speed and direction. We report that the sensitivity of the subfield arrangement for both neuron types on average corresponds to a spatial period of ∼0.4 mm and provide evidence that a subfield's spatial selectivity arises because its associated receptor organ measures mechanical events limited to a single papillary ridge. Accordingly, the sensitivity topography of a neuron's receptive fields is quite stable over repeated mappings and over scanning speeds representative of real-world hand use. The sensitivity topography is substantially conserved also for different scanning directions, but the subfields can be relatively displaced by direction-dependent shear deformations of the skin surface.SIGNIFICANCE STATEMENTThe branching of the distal axon of human first-order tactile neurons with receptor organs associated with fingerprint ridges (Meissner and Merkel end-organs) results in cutaneous receptive fields composed of several distinct subfields spread across multiple ridges. We show that the subfields' spatial selectivity typically corresponds to the dimension of the ridges (∼0.4 mm) and a neuron's subfield layout is well preserved across tangential movement speeds and directions representative of natural use of the fingertips. We submit that the receptor organs underlying subfields essentially measure mechanical events at individual ridges. That neurons receive convergent input from multiple subfields does not preclude the possibility that spatial details can be resolved on the scale of single fingerprint ridges by a population code.
Copyright © 2021 the authors.

Entities:  

Year:  2021        PMID: 33722975      PMCID: PMC8055081          DOI: 10.1523/JNEUROSCI.1716-20.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  80 in total

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2.  Meissner corpuscles and their spatially intermingled afferents underlie gentle touch perception.

Authors:  Nicole L Neubarth; Alan J Emanuel; Yin Liu; Mark W Springel; Annie Handler; Qiyu Zhang; Brendan P Lehnert; Chong Guo; Lauren L Orefice; Amira Abdelaziz; Michelle M DeLisle; Michael Iskols; Julia Rhyins; Soo J Kim; Stuart J Cattel; Wade Regehr; Christopher D Harvey; Jan Drugowitsch; David D Ginty
Journal:  Science       Date:  2020-06-19       Impact factor: 47.728

3.  Transformation of the neural code for tactile detection from thalamus to cortex.

Authors:  Yuriria Vázquez; Emilio Salinas; Ranulfo Romo
Journal:  Proc Natl Acad Sci U S A       Date:  2013-06-24       Impact factor: 11.205

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Authors:  P Grigg
Journal:  J Appl Physiol (1985)       Date:  1986-04

5.  Edge-orientation processing in first-order tactile neurons.

Authors:  J Andrew Pruszynski; Roland S Johansson
Journal:  Nat Neurosci       Date:  2014-08-31       Impact factor: 24.884

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7.  Speed invariance of tactile texture perception.

Authors:  Zoe M Boundy-Singer; Hannes P Saal; Sliman J Bensmaia
Journal:  J Neurophysiol       Date:  2017-07-19       Impact factor: 2.714

Review 8.  Neural mechanisms of scanned and stationary touch.

Authors:  J R Phillips; K O Johnson
Journal:  J Acoust Soc Am       Date:  1985-01       Impact factor: 1.840

9.  Diminutive digits discern delicate details: fingertip size and the sex difference in tactile spatial acuity.

Authors:  Ryan M Peters; Erik Hackeman; Daniel Goldreich
Journal:  J Neurosci       Date:  2009-12-16       Impact factor: 6.167

10.  Intracellular Dynamics in Cuneate Nucleus Neurons Support Self-Stabilizing Learning of Generalizable Tactile Representations.

Authors:  Udaya B Rongala; Anton Spanne; Alberto Mazzoni; Fredrik Bengtsson; Calogero M Oddo; Henrik Jörntell
Journal:  Front Cell Neurosci       Date:  2018-07-31       Impact factor: 5.505

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  3 in total

Review 1.  Skin and Mechanoreceptor Contribution to Tactile Input for Perception: A Review of Simulation Models.

Authors:  Davide Deflorio; Massimiliano Di Luca; Alan M Wing
Journal:  Front Hum Neurosci       Date:  2022-06-02       Impact factor: 3.473

2.  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

3.  Hand posture, but not vision of the hand, affects tactile spatial resolution in the grating orientation discrimination task.

Authors:  B French; N V Di Chiaro; N P Holmes
Journal:  Exp Brain Res       Date:  2022-09-08       Impact factor: 2.064

  3 in total

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