Tactile C fibers and their contributions to pleasant sensations and to tactile allodynia

Abstract

In humans converging evidence indicates that affective aspects of touch are signaled by low threshold mechanoreceptive C tactile (CT) afferents. Analyses of electrophysiological recordings, psychophysical studies in denervated subjects, and functional brain imaging, all indicate that CT primary afferents contribute to pleasant touch and provide an important sensory underpinning of social behavior. Considering both these pleasant and social aspects of gentle skin-to-skin contact, we have put forward a framework within which to consider CT afferent coding properties and pathways-the CT affective touch hypothesis. Recent evidence from studies in mice suggests that CTs, when activated, may have analgesic or anxiolytic effects. However, in neuropathic pain conditions, light touch can elicit unpleasant sensations, so called tactile allodynia. In humans, tactile allodynia is associated with reduced CT mediated hedonic touch processing suggesting loss of the normally analgesic effect of CT signaling. We thus propose that the contribution of CT afferents to tactile allodynia is mainly through a loss of their normally pain inhibiting role.

Keywords: fMRI; psychophysics; social; tactile allodynia; touch; unmyelinated.

Figure 1

CT afferent response to slowly moving mechanical stimulation. (A and B) Responses of two separate units to the experimenter stroking his finger tip over the receptive field. Peak impulse rates were 78 and 64 imp/s (A) and 52 and 73 imp/s (B) (Vallbo et al., 1999). (C) Microneurography recording of nerve response and interspike interval histogram for another single CT afferent to soft brush stroking with a velocity of 3 cm s^-1 and calibrated normal force of 0.4 N. Individual nerve spikes are superimposed on an expanded time scale below the nerve recording to illustrate the typical C impulse shape with a prominent negative peak (Loken et al., 2009).

Figure 2

Field geography of CT afferents on the forearm skin. Color coded two-dimensional density plots of receptive fields of three CT afferents. The colors represent intensity of afferent firing. The geography of receptive fields was explored with a robotic scanning method: a lightweight probe with a small and rounded tip was made to scan the field area in a series of closely adjacent tracks while single unit activity was recorded (Wessberg et al., 2003).

Figure 3

Neural discharge rate and perception of pleasantness in response to soft brush stroking. (A) Dots show average discharge rates during brush stroking for 16 CT afferents. (B) Average ratings of perceived pleasantness in response to soft brush stroking. Data are from 10 subjects. (C) Ratings of pleasantness as a function of neural discharge rate in CT afferents. Mean pleasantness ratings are plotted against the corresponding mean firing frequency for each brushing velocity and force. The plot is based on the data in A and B. The linear correlation was significant (Pearson’s linear regression, R² = 0.70, P = 0.00063). Error bars show s.e.m.

Figure 4

fMRI activation in posterior insular cortex evoked by selective stimulation of CT afferents in the neuronopathy subjects GL and IW lacking Aβ afferents. In both subjects, the posterior insular activation was contralateral to the stimulated forearm and reflects differences in blood oxygen level dependent (BOLD) signal during soft brush stroking and a baseline condition of rest (Olausson et al., ; Olausson et al., 2008).