Spinal signalling of C-fiber mediated pleasant touch in humans

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Abstract

C-tactile afferents form a distinct channel that encodes pleasant tactile stimulation. Prevailing views indicate they project, as with other unmyelinated afferents, in lamina I-spinothalamic pathways. However, we found that spinothalamic ablation in humans, whilst profoundly impairing pain, temperature and itch, had no effect on pleasant touch perception. Only discriminative touch deficits were seen. These findings preclude privileged C-tactile-lamina I-spinothalamic projections and imply integrated hedonic and discriminative spinal processing from the body.

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Most cited references 33

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The functional organization of cutaneous low-threshold mechanosensory neurons.

Lishi Li, Michael Rutlin, Victoria Abraira … (2011)

Innocuous touch of the skin is detected by distinct populations of neurons, the low-threshold mechanoreceptors (LTMRs), which are classified as Aβ-, Aδ-, and C-LTMRs. Here, we report genetic labeling of LTMR subtypes and visualization of their relative patterns of axonal endings in hairy skin and the spinal cord. We found that each of the three major hair follicle types of trunk hairy skin (guard, awl/auchene, and zigzag hairs) is innervated by a unique and invariant combination of LTMRs; thus, each hair follicle type is a functionally distinct mechanosensory end organ. Moreover, the central projections of Aβ-, Aδ-, and C-LTMRs that innervate the same or adjacent hair follicles form narrow LTMR columns in the dorsal horn. These findings support a model of mechanosensation in which the activities of Aβ-, Aδ-, and C-LTMRs are integrated within dorsal horn LTMR columns and processed into outputs that underlie the perception of myriad touch sensations. Copyright © 2011 Elsevier Inc. All rights reserved.

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The neurophysiology of unmyelinated tactile afferents.

Håkan Olausson, Johan Wessberg, India Morrison … (2010)

CT (C tactile) afferents are a distinct type of unmyelinated, low-threshold mechanoreceptive units existing in the hairy but not glabrous skin of humans and other mammals. Evidence from patients lacking myelinated tactile afferents indicates that signaling in these fibers activate the insular cortex. Since this system is poor in encoding discriminative aspects of touch, but well-suited to encoding slow, gentle touch, CT fibers in hairy skin may be part of a system for processing pleasant and socially relevant aspects of touch. CT fiber activation may also have a role in pain inhibition. This review outlines the growing evidence for unique properties and pathways of CT afferents.

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The skin as a social organ.

S Loken, Håkan Olausson, India Morrison (2010)

In general, social neuroscience research tends to focus on visual and auditory channels as routes for social information. However, because the skin is the site of events and processes crucial to the way we think about, feel about, and interact with one another, touch can mediate social perceptions in various ways. This review situates cutaneous perception within a social neuroscience framework by discussing evidence for considering touch (and to some extent pain) as a channel for social information. Social information conveys features of individuals or their interactions that have potential bearing on future interactions, and attendant mental and emotional states. Here, we discuss evidence for an affective dimension of touch and explore its wider implications for the exchange of social information. We consider three important roles for this affective dimension of the cutaneous senses in the transmission and processing of social information: first, through affiliative behavior and communication; second, via affective processing in skin-brain pathways; and third, as a basis for intersubjective representation.

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Author and article information

Contributors

Andrew G Marshall:

ORCID: https://orcid.org/0000-0001-8273-7089

Peggy Mason: Role: Reviewing Editor

Christian Büchel: Role: Senior Editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 24 December 2019

Publication date Collection: 2019

Volume: 8

Electronic Location Identifier: e51642

Affiliations

[1 ]deptInstitute of Aging and Chronic Disease University of Liverpool LiverpoolUnited Kingdom

[2 ]deptSchool of Natural Sciences and Psychology Liverpool John Moores University LiverpoolUnited Kingdom

[3 ]deptDepartment of Pain Medicine Walton Centre NHS Foundation Trust LiverpoolUnited Kingdom

[4 ]deptSpecialist Palliative Care Team University Hospital Aintree LiverpoolUnited Kingdom

[5 ]deptCenter for Social and Affective Neuroscience Linköping University LinköpingSweden

[6 ]deptDepartment of Clinical Neurophysiology Linköping University Hospital LinköpingSweden

[7 ]deptInstitute of Psychology, Health and Society University of Liverpool LiverpoolUnited Kingdom

University of Chicago United States

University Medical Center Hamburg-Eppendorf Germany

University of Chicago United States

School of Medicine Australia

Medizinische Fakultät Mannheim, Universität Heidelberg Germany

Author information

Andrew G Marshall https://orcid.org/0000-0001-8273-7089

Article

Publisher ID: 51642

DOI: 10.7554/eLife.51642

PMC ID: 6964968

PubMed ID: 31872799

SO-VID: b6cc377f-9437-49c3-9e21-a73b85b7ed0f

License:

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 05 September 2019

Date accepted : 23 December 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000323, Pain Relief Foundation;

Award Recipient : Andrew G Marshall Francis P McGlone

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Author impact statement Pleasant touch perception in humans is unaffected by spinothalamic disruption indicating integrated spinal processing of hedonic and discriminative tactile inputs rather than privileged C-tactile-lamina I-spinothalamic projections.

ScienceOpen disciplines: Life sciences

Keywords: touch,c-tactile,pain,spinothalamic tract,anterolateral cordotomy,human

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: touch, c-tactile, pain, spinothalamic tract, anterolateral cordotomy, human

Spinal signalling of C-fiber mediated pleasant touch in humans

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Abstract

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Most cited references 33

The functional organization of cutaneous low-threshold mechanosensory neurons.

The neurophysiology of unmyelinated tactile afferents.

The skin as a social organ.

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