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

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.

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

Figure 1.

Experimental setup, locations of units, and examples of CT responses. A, Schematic of the setup with the rotary mechano-thermal stimulator positioned over the participant's arm. B, C, Receptive field locations of maximal responses from all the CT units (B) and myelinated units (C) stimulated in the mechano-thermal experiment. D, E, Examples of raw spike traces and firing-frequency histograms from an individual CT unit in response to a stroking velocity of 3 cm s⁻¹ at the neutral (32°C; D) and cool (18°C; E) temperatures.

Figure 2.

Neural firing and pleasantness ratings at different velocities and temperatures. A–D, Mean firing frequency of an individual CT unit's response (A), all CT (B) and all hair (C) units, and pleasantness ratings (D) to the five stroking velocities and three temperatures. For CT responses and pleasantness ratings, stroking at 3 cm s⁻¹ at a neutral temperature produced the highest responses. All measures were affected by the stroking velocity, but only the CT firing frequency and pleasantness ratings showed an effect to temperature, where neutral produced the highest responses. E, CT firing frequency and pleasantness ratings correlated significantly, but only at the neutral temperature (regression line). Error bars indicate ±SEM.