Psychophysical Investigations into the Role of Low-Threshold C Fibres in Non-Painful Affective Processing and Pain Modulation.

Sumaiya Shaikh,Saad S. Nagi,David A. Mahns,Francis McGlone,Sliman J. Bensmaia

doi:10.1371/journal.pone.0138299

Sumaiya Shaikh, Saad S. Nagi + Show 3 more

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https://doi.org/10.1371/journal.pone.0138299

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Abstract

We recently showed that C low-threshold mechanoreceptors (CLTMRs) contribute to touch-evoked pain (allodynia) during experimental muscle pain. Conversely, in absence of ongoing pain, the activation of CLTMRs has been shown to correlate with a diffuse sensation of pleasant touch. In this study, we evaluated (1) the primary afferent fibre types contributing to positive (pleasant) and negative (unpleasant) affective touch and (2) the effects of tactile stimuli on tonic muscle pain by varying affective attributes and frequency parameters. Psychophysical observations were made in 10 healthy participants. Two types of test stimuli were applied: stroking stimulus using velvet or sandpaper at speeds of 0.1, 1.0 and 10.0 cm/s; focal vibrotactile stimulus at low (20 Hz) or high (200 Hz) frequency. These stimuli were applied in the normal condition (i.e. no experimental pain) and following the induction of muscle pain by infusing hypertonic saline (5%) into the tibialis anterior muscle. These observations were repeated following the conduction block of myelinated fibres by compression of sciatic nerve. In absence of muscle pain, all participants reliably linked velvet-stroking to pleasantness and sandpaper-stroking to unpleasantness (no pain). Likewise, low-frequency vibration was linked to pleasantness and high-frequency vibration to unpleasantness. During muscle pain, the application of previously pleasant stimuli resulted in overall pain relief, whereas the application of previously unpleasant stimuli resulted in overall pain intensification. These effects were significant, reproducible and persisted following the blockade of myelinated fibres. Taken together, these findings suggest the role of low-threshold C fibres in affective and pain processing. Furthermore, these observations suggest that temporal coding need not be limited to discriminative aspects of tactile processing, but may contribute to affective attributes, which in turn predispose individual responses towards excitatory or inhibitory modulation of pain.

Highlights

It is widely appreciated that large myelinated mechano-afferents subserve the sensory-discriminative facet of touch, which includes pressure, vibration/texture, stretch and movement of hair follicles
These affective judgments were preserved following the conduction block of myelinated fibres, indicating that affective touch sensations can be sustained by C-fibre inputs alone
Such stimulus fidelity was observed following the induction of muscle pain: those stimuli perceived as pleasant reduced the overall perception of pain, whereas those perceived as unpleasant, but not painful, increased the overall pain

Summary

Introduction

It is widely appreciated that large myelinated mechano-afferents subserve the sensory-discriminative facet of touch, which includes pressure, vibration/texture, stretch and movement of hair follicles. In addition to the well-studied aspects of discriminative touch, there exists a distinct and independently variable affective quality of tactile sensation that contributes to our emotional response to touch [1,2]. The abbreviation ‘CLTMRs’ refers to the C low-threshold mechanoreceptors found in a myriad of species, including C-tactile fibres in humans) This afferent class responds to non-noxious touch with a predilection for slow-moving, low-force, stroking stimuli such as gentle brushing [8,9,10]. It is noteworthy that the use of a scale with the endpoints ‘unpleasant’ (-10) and ‘pleasant’ (+10) meant that the subjects reported low-velocity brushing (0.1 cm/s) in the negative/unpleasant range [11] Whether this effect could be attributed to large- or small-fibre function, or the need for temporal summation, is a matter for conjecture. Other studies have hypothesised a rather indirect role of CLTMRs in pain processing by way of the malfunction of the pleasant-touch system [15]

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