Does sympathetic nerve discharge affect the firing of myelinated cutaneous afferents in humans?

ABSTRACT

In clinical practise, the notion that some complex regional pain syndromes (CRPS) are associated with sympathetic facilitation of nociceptive transmission is widespread. However, physiological increases in cutaneous sympathetic nerve activity have not been found to influence the firing properties of cutaneous polymodal nociceptive (high-threshold mechano-heat sensitive) fibers in human subjects. Whether the same applies to low-threshold cutaneous mechanoreceptors is not known. Such an effect could be relevant for sympathetic facilitation of nociception, given that tactile afferents are implicated in the allodynia associated with CRPS. This issue was addressed by recording the responses of single cutaneous mechanoreceptors in the glabrous skin of the finger pads to constant mechanical stimuli, at rest and during physiological increases in cutaneous sympathetic activity produced by arousal stimuli. Unitary recordings were made from 17 rapidly adapting (15 FAI and 2 FAII) and 20 slowly adapting (9 SAI and 11 SAII) afferents located in the finger pads via tungsten microelectrodes inserted percutaneously into the median nerve at the wrist in nine subjects. A servomotor applied 1 s constant-displacement ramp-and-hold indentations to the receptor-bearing digit every 3 s. Displacement and compression force were recorded. Blood flow in the finger pad and sweating in the palm were measured contralaterally. Increases in cutaneous sympathetic outflow caused only modest changes in the spontaneous and compression-evoked firing of tactile afferents. These changes were usually (for 26/37 afferents) related to the associated decreases in skin blood flow. The latency from the start of the ramp stimulus to the onset of firing was inversely correlated to flow (i.e. unit response was delayed during vasoconstriction) for 11/31 units (7/15 FAI, 1/2 FAII, 2/9 SAI, 1/5 SAII), whereas no units showed a positive correlation. Compression-evoked firing rates were positively correlated to flow (i.e. vasoconstriction reduced firing rates) for 14/31 units (2/15 FAI, 1/2 FAII, 7/9 SAI, 4/5 SAII), whereas no units showed a negative correlation. 10/11 SAII afferents exhibited spontaneous background firing, which increased for 4 and decreased for 4 in response to arousal stimuli, presumably reflecting their sensitivity to changes in skin stretch associated with sympathetically mediated reductions in blood volume in the finger pad. Two afferents showed no change, but nor was there significant vasoconstriction in these recordings. Thus, arousal stimuli reduced rather than augmented tactile afferent firing. The close relation to blood flow for all types of afferents, and the different responses among SAII afferents, suggest that sympathetically mediated changes in afferent firing properties are indirect, i.e. secondary to changes in the mechanoreceptors' tissue environment rather than to a direct sympathetic effect on the endings.