C tactile afferent explained

C tactile afferents are nerve receptors in mammalian skin that generally respond to nonpainful stimulation such as light touch. For this reason they are classified as ‘low-threshold mechanoreceptors’. As group C nerve fibers, they are unmyelinated and have slow conduction velocities. They are mostly associated with the sensation of pleasant touch, though they may also mediate some forms of pain. CT afferents were discovered by Åke Vallbo using the technique of microneurography.[1]

Low-threshold C mechanoreceptors

C tactile (CT) neurons are a class of low-threshold C neurons that innervate the human skin. In animals, these neurons are referred to as C low-threshold mechanoreceptors (C-LTMRs). CT neurons belong to a group C nerve fibers; these are unmyelinated, and have slow conduction velocities.

Structure and location

Using microneurography, CT neurons have been found in the hairy skin of humans.[2] In animals, these neurons have been genetically labelled and visualized with their relative patterns of axonal endings in hairy skin and in the spinal cord.[3] Out of the three, two hair follicle subtypes (awl, auchene, and zigzag) have been found to be innervated by C-LTMRs in combination with other LTMRs in the rodent hairy skin. C-LTMRs also seem to exist in the rat glabrous skin (see [5]). This author provided direct electrophysiological existence of a rare population of C-LTMRs in glabrous skin of the rat hind paw. There is also indirect evidence for the presence of this population of primary afferent neurons in the mouse and other species (For references, see [5]).

In humans, new psychophysical data suggests that CT neurons may also be present in the glabrous skin, but it might be that they have different biochemical and structural characteristics to the ones found in the hairy skin.[4] They have been found electrophysiologically in the glabrous skin of the rat hind paw,[5] supporting the evidence of their existence in glabrous skin.

Molecular markers

Since these CTs or C-LTMRs are non-peptidergic, immuno-labelling was a challenge. However, in combination with RNA-seq data and genetically modified mouse models, several labeling markers, i.e. VGLUT3,[6] TAFA4,[7] CaV3.2,[8] CaV3.3[9] and GINIP[10] have been discovered to visualize C-LTMRs using double staining methods in combination with tyrosine hydroxylase (TH).

Role in pain

While these neurons are non-nociceptive and likely mediate low threshold innocuous mechanical sensations, in the context of background muscle pain using hypertonic saline they have been shown to mediate allodynia[11] - pain due to a non-painful stimulus. Later, the role of CTs was also found in mediating allodynia in the model of a delayed onset muscle soreness, i.e. pain following eccentric exercise.[12]

Recently, several animal studies have shown the role of C-LTMRs in neuropathic pain behaviors, which suggests that both mechanical and cold allodynia, but not heat hyperalgesia, is mediated by them.

Pain modulation

In humans, their role in pain increase has been contested as, in some instances, they have been shown to reduce pain, depending on the context of the stimulus.[13] This dual role is also confirmed by the markers found for C-LTMRs in animal models, i.e. some markers are glutaminergic and some are GABAergic in nature.

Role in pleasantness

In humans, these CTs have always been linked to pleasant touch behavior and are most responsive during slow gentle stroking of a brush with the velocity of 3 cm/s.[14] CT neurons project to the insular cortex in the brain,[15] [16] and the firing frequency of CT neurons correlate with perceived pleasantness of skin stroking.

Notes and References

  1. Vallbo . Åke . Olausson . Håkan . Wessberg . Johan . Norrsell . Ulf . A system of unmyelinated afferents for innocuous mechanoreception in the human skin . Brain Research . 628 . 1–2 . 301–4 . 1993 . 8313159 . 10.1016/0006-8993(93)90968-S . 29606427 .
  2. McGlone . Francis . Wessberg . Johan . Olausson . Håkan . Discriminative and Affective Touch: Sensing and Feeling . Neuron . 82 . 4 . 737–55 . 2014 . 24853935 . 10.1016/j.neuron.2014.05.001 . free .
  3. Li. Lishi. Rutlin. Michael. Abraira. Victoria E.. Cassidy. Colleen. Kus. Laura. Gong. Shiaoching. Jankowski. Michael P.. Luo. Wenqin. Heintz. Nathaniel. December 2011. The Functional Organization of Cutaneous Low-Threshold Mechanosensory Neurons. Cell. 147. 7. 1615–1627. 10.1016/j.cell.2011.11.027. 0092-8674. 3262167. 22196735.
  4. Nagi. Saad S.. Mahns. David A.. 2013-08-18. Mechanical allodynia in human glabrous skin mediated by low-threshold cutaneous mechanoreceptors with unmyelinated fibres. Experimental Brain Research. en. 231. 2. 139–151. 10.1007/s00221-013-3677-z. 23955107. 6459499. 0014-4819.
  5. Djouhri. Laiche. 2016-02-02. Electrophysiological evidence for the existence of a rare population of C-fiber low threshold mechanoreceptive (C-LTM) neurons in glabrous skin of the rat hindpaw. Neuroscience Letters. 613. 25–29. 10.1016/j.neulet.2015.12.040. 1872-7972. 26752785. 207141915.
  6. Seal. Rebecca P.. Wang. Xidao. Guan. Yun. Raja. Srinivasa N.. Woodbury. C. Jeffery. Basbaum. Allan I.. Edwards. Robert H.. 2009-12-03. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature. 462. 7273. 651–655. 10.1038/nature08505. 1476-4687. 2810205. 19915548. 2009Natur.462..651S.
  7. Delfini. Marie-Claire. Mantilleri. Annabelle. Gaillard. Stéphane. Hao. Jizhe. Reynders. Ana. Malapert. Pascale. Alonso. Serge. François. Amaury. Barrere. Christian. October 2013. TAFA4, a Chemokine-like Protein, Modulates Injury-Induced Mechanical and Chemical Pain Hypersensitivity in Mice. Cell Reports. 5. 2. 378–388. 10.1016/j.celrep.2013.09.013. 24139797. 2211-1247. free.
  8. François. Amaury. Schüetter. Niklas. Laffray. Sophie. Sanguesa. Juan. Pizzoccaro. Anne. Dubel. Stefan. Mantilleri. Annabelle. Nargeot. Joel. Noël. Jacques. 2015-01-14. The Low-Threshold Calcium Channel Cav3.2 Determines Low-Threshold Mechanoreceptor Function. Cell Reports. 10. 3. 370–382. 10.1016/j.celrep.2014.12.042. 2211-1247. 25600872. free.
  9. Reynders. Ana. Mantilleri. Annabelle. Malapert. Pascale. Rialle. Stéphanie. Nidelet. Sabine. Laffray. Sophie. Beurrier. Corinne. Bourinet. Emmanuel. Moqrich. Aziz. 2015-02-12. Transcriptional Profiling of Cutaneous MRGPRD Free Nerve Endings and C-LTMRs. Cell Reports. 10. 6. 1007–1019. 10.1016/j.celrep.2015.01.022. 2211-1247. 4542317. 25683706.
  10. Gaillard. Stéphane. Lo Re. Laure. Mantilleri. Annabelle. Hepp. Régine. Urien. Louise. Malapert. Pascale. Alonso. Serge. Deage. Michael. Kambrun. Charline. October 2014. GINIP, a G αi -Interacting Protein, Functions as a Key Modulator of Peripheral GABA B Receptor-Mediated Analgesia. Neuron. 84. 1. 123–136. 10.1016/j.neuron.2014.08.056. 25242222. 7348640. 0896-6273. free.
  11. Nagi. Saad S.. Rubin. Troy K.. Chelvanayagam. David K.. Macefield. Vaughan G.. Mahns. David A.. 2011-08-15. Allodynia mediated by C-tactile afferents in human hairy skin. The Journal of Physiology. 589. Pt 16. 4065–4075. 10.1113/jphysiol.2011.211326. 1469-7793. 3180003. 21727219.
  12. Nagi. Saad S.. Mahns. David A.. May 2013. C-tactile Fibers Contribute to Cutaneous Allodynia After Eccentric Exercise. The Journal of Pain. 14. 5. 538–548. 10.1016/j.jpain.2013.01.009. 23562300. 1526-5900. free.
  13. . Nagi . Saad S. . McGlone . Francis . Mahns . David A. . 2015 . Psychophysical Investigations into the Role of Low-Threshold C Fibres in Non-Painful Affective Processing and Pain Modulation . PLOS ONE . 10 . 9 . e0138299 . 2015PLoSO..1038299S . 10.1371/journal.pone.0138299 . 1932-6203 . 4570804 . 26372601 . free.
  14. Löken. Line S.. Wessberg. Johan. Morrison. India. McGlone. Francis. Olausson. Håkan. May 2009. Coding of pleasant touch by unmyelinated afferents in humans. Nature Neuroscience. 12. 5. 547–548. 10.1038/nn.2312. 1546-1726. 19363489. 4311541.
  15. Olausson. H.. Lamarre. Y.. Backlund. H.. Morin. C.. Wallin. B.G.. Starck. G.. Ekholm. S.. Strigo. I.. Worsley. K.. 2002. Unmyelinated tactile afferents signal touch and project to insular cortex. Nature Neuroscience. 5. 9. 900–4. 10.1038/nn896. 12145636. Vallbo. Å.B.. Bushnell. M.C.. 14648389.
  16. Bjornsdotter. M.. Loken. L.. Olausson. H.. Vallbo. A.. Wessberg. J.. 2009. Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex. Journal of Neuroscience. 29. 29. 9314–20. 10.1523/JNEUROSCI.0400-09.2009. 19625521. 6665561. free.

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