Effect of Tactile Inputs on Thalamic Responses to Noxious Colorectal Distension in Rat

Abstract

Recent discoveries of visceral nociceptive inputs sharing the classical tactile pathway in the dorsal-column medial lemniscus system have opened a new venue for the investigation of somatovisceral interactions. The current study was designed to determine whether somatic innocuous inputs modulate visceral nociceptive transmission at the thalamic level. The investigation was carried out by means of extracellular single-unit recordings in the ventroposterior lateral nucleus of the thalamus in rats anesthetized with pentobarbital. Noxious visceral stimulation was achieved by reproducible colorectal distension (CRD, 20–80 mmHg) with a balloon catheter. Tactile stimulation was delivered by means of a feedback-controlled mechanical stimulator. The response of the neurons to CRD was compared before and after the conditioning procedure by giving tactile stimulation either immediately before CRD or overlapping it. Twenty-five ventroposterior lateral (VPL) thalamic neurons were found among numerous tactile-only neurons to have convergent inputs from both tactile and visceral sources. Their responses to CRD were excitatory (19), inhibitory (4), or bimodal. When cutaneous tactile stimuli were delivered before CRD, the responses were reduced in 18 cases. The reduction, however, was usually short-lasting, immediately following tactile stimulation and could not be enhanced by a prolonged conditioning procedure. It was unlikely to be attributable to neuronal habituation as the inverted procedure, CRD stimulation before tactile, often produced the opposite effect, that is, an enhanced response to skin stimulation. Repeated CRD could bring about sensitization of the responses of thalamic neurons as manifested by increased spontaneous discharge, lowered response threshold, and increased response level. Under such circumstances, the original effect of tactile stimulation on CRD responses could be weakened. In conclusion, tactile stimulation may in most circumstances inhibit thalamic neuronal responses to visceral nociceptive input produced by CRD. However, the effect appears to be mild and short-lasting at the individual neuronal level in the VPL thalamus.