Literature DB >> 24553929

Human C-tactile afferents are tuned to the temperature of a skin-stroking caress.

Rochelle Ackerley1, Helena Backlund Wasling, Jaquette Liljencrantz, Håkan Olausson, Richard D Johnson, Johan Wessberg.   

Abstract

Human C-tactile (CT) afferents respond vigorously to gentle skin stroking and have gained attention for their importance in social touch. Pharmacogenetic activation of the mouse CT equivalent has positively reinforcing, anxiolytic effects, suggesting a role in grooming and affiliative behavior. We recorded from single CT axons in human participants, using the technique of microneurography, and stimulated a unit's receptive field using a novel, computer-controlled moving probe, which stroked the skin of the forearm over five velocities (0.3, 1, 3, 10, and 30 cm s(-1)) at three temperatures (cool, 18 °C; neutral, 32 °C; warm, 42 °C). We show that CTs are unique among mechanoreceptive afferents: they discharged preferentially to slowly moving stimuli at a neutral (typical skin) temperature, rather than at the cooler or warmer stimulus temperatures. In contrast, myelinated hair mechanoreceptive afferents proportionally increased their firing frequency with stroking velocity and showed no temperature modulation. Furthermore, the CT firing frequency correlated with hedonic ratings to the same mechano-thermal stimulus only at the neutral stimulus temperature, where the stimuli were felt as pleasant at higher firing rates. We conclude that CT afferents are tuned to respond to tactile stimuli with the specific characteristics of a gentle caress delivered at typical skin temperature. This provides a peripheral mechanism for signaling pleasant skin-to-skin contact in humans, which promotes interpersonal touch and affiliative behavior.

Entities:  

Keywords:  C-fiber; human; low-threshold mechanoreceptor; somatosensory; thermal; touch

Mesh:

Year:  2014        PMID: 24553929      PMCID: PMC3931502          DOI: 10.1523/JNEUROSCI.2847-13.2014

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


  34 in total

1.  Receptive field properties of unmyelinated tactile afferents in the human skin.

Authors:  Johan Wessberg; Håkan Olausson; Katarina Wiklund Fernström; Ake B Vallbo
Journal:  J Neurophysiol       Date:  2003-03       Impact factor: 2.714

2.  Low-threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve.

Authors:  M Nordin
Journal:  J Physiol       Date:  1990-07       Impact factor: 5.182

3.  An analysis of fibre diameter and receptor characteristics of myelinated cutaneous afferent fibres in cat.

Authors:  C C HUNT; A K McINTYRE
Journal:  J Physiol       Date:  1960-08       Impact factor: 5.182

4.  Touch, pain and tickling: an electro-physiological investigation on cutaneous sensory nerves.

Authors:  Y Zotterman
Journal:  J Physiol       Date:  1939-02-14       Impact factor: 5.182

5.  Coding of pleasant touch by unmyelinated afferents in humans.

Authors:  Line S Löken; Johan Wessberg; India Morrison; Francis McGlone; Håkan Olausson
Journal:  Nat Neurosci       Date:  2009-04-12       Impact factor: 24.884

6.  Innervation territories of mechanically activated C nociceptor units in human skin.

Authors:  R Schmidt; M Schmelz; M Ringkamp; H O Handwerker; H E Torebjörk
Journal:  J Neurophysiol       Date:  1997-11       Impact factor: 2.714

7.  Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds.

Authors:  India Morrison; Malin Björnsdotter; Håkan Olausson
Journal:  J Neurosci       Date:  2011-06-29       Impact factor: 6.167

Review 8.  Microneurographic single-unit recordings to assess receptive properties of afferent human C-fibers.

Authors:  M Schmelz; R Schmidt
Journal:  Neurosci Lett       Date:  2009-05-28       Impact factor: 3.046

9.  Peripheral neural correlates of temperature sensations in man.

Authors:  F Konietzny
Journal:  Hum Neurobiol       Date:  1984

10.  The dynamic response of warm units in human skin nerves.

Authors:  F Konietzny; H Hensel
Journal:  Pflugers Arch       Date:  1977-07-29       Impact factor: 3.657

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  87 in total

Review 1.  Neural Basis of Touch and Proprioception in Primate Cortex.

Authors:  Benoit P Delhaye; Katie H Long; Sliman J Bensmaia
Journal:  Compr Physiol       Date:  2018-09-14       Impact factor: 9.090

2.  Low-threshold mechanoreceptors play a frequency-dependent dual role in subjective ratings of mechanical allodynia.

Authors:  Line S Löken; Eugene P Duff; Irene Tracey
Journal:  J Neurophysiol       Date:  2017-09-27       Impact factor: 2.714

Review 3.  Cutaneous afferent innervation of the human foot sole: what can we learn from single-unit recordings?

Authors:  Nicholas D J Strzalkowski; Ryan M Peters; J Timothy Inglis; Leah R Bent
Journal:  J Neurophysiol       Date:  2018-06-06       Impact factor: 2.714

4.  Emotional visual stimuli affect the evaluation of tactile stimuli presented on the arms but not the related electrodermal responses.

Authors:  Roberta Etzi; Massimiliano Zampini; Georgiana Juravle; Alberto Gallace
Journal:  Exp Brain Res       Date:  2018-09-29       Impact factor: 1.972

5.  The role of affective touch in whole-body embodiment remains equivocal.

Authors:  Mark Carey; Laura Crucianelli; Catherine Preston; Aikaterini Fotopoulou
Journal:  Conscious Cogn       Date:  2020-12-07

Review 6.  The biology of skin wetness perception and its implications in manual function and for reproducing complex somatosensory signals in neuroprosthetics.

Authors:  Davide Filingeri; Rochelle Ackerley
Journal:  J Neurophysiol       Date:  2017-01-25       Impact factor: 2.714

Review 7.  Emotion Perception from Face, Voice, and Touch: Comparisons and Convergence.

Authors:  Annett Schirmer; Ralph Adolphs
Journal:  Trends Cogn Sci       Date:  2017-02-04       Impact factor: 20.229

8.  Stroking and tapping the skin: behavioral and electrodermal effects.

Authors:  Roberta Etzi; Carlotta Carta; Alberto Gallace
Journal:  Exp Brain Res       Date:  2017-12-06       Impact factor: 1.972

9.  The arousing power of everyday materials: an analysis of the physiological and behavioral responses to visually and tactually presented textures.

Authors:  Roberta Etzi; Alberto Gallace
Journal:  Exp Brain Res       Date:  2016-02-03       Impact factor: 1.972

10.  Effects of MDMA on attention to positive social cues and pleasantness of affective touch.

Authors:  Anya K Bershad; Leah M Mayo; Kathryne Van Hedger; Francis McGlone; Susannah C Walker; Harriet de Wit
Journal:  Neuropsychopharmacology       Date:  2019-04-30       Impact factor: 7.853

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