Dual alterations of thalamic nociceptive activity by stimulation of the periaqueductal gray matter

Abstract

Effects produced by electrical stimulation of the mesencephalic periaqueductal gray matter (PAG) on single nociceptive neurons of the somesthetic thalamus were studied in rats anesthetized with α-chloralose and urethane. Stimulation of the PAG excited the nociceptive neurons, and, although the probability of firing them with a single pulse was low, trains of pulses increased their preexisting activity considerably and lastingly. Poststimulus spike density histograms of the activity evoked by stimulation of the sciatic nerve displayed several peaks which have been analyzed previously. In brief, a short-latency, high-count peak was related to the intensity of stimulation ( I peak); three to four long-latency, low-count peaks were characteristic of nociception (modality, or M peaks). PAG stimulation modified mainly the M peaks. With stimulation of the caudal portion of the PAG, fusion of the M peaks was observed and persisted. With stimulation of its rostral portion each M peak was augmented. At several PAG sites, however, increasing the stimulus frequency and pulse-train duration converted the augmentation effect into fusion of the M peaks. Thalamic neurons that relay tactile afferents were not fired by stimulation of the PAG, although after such a stimulation they began to fire spontaneously. These results parallel the dual behavioral effects previously observed with PAG stimulation. When repeated trains of pulses were used, analgesia was induced that outlasted the period of stimulation. However, with stimulation of the rostral PAG, behavioral agitation and lowering of the nociceptive thresholds were observed. It is likely that augmentation of the M peaks represents central sensitization to noxious stimulation, and fusion of the M peaks represents a conversion of pain into less pain-like sensations. These effects may be mediated via a pathway that connects the PAG with the ventrobasal and the parafascicular nuclei of the thalamus.