Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli

Abstract

1. The responses of primate spinothalamic tract cells innervating the glabrous skin of the foot to noxious thermal stimuli have been examined. 2. Of the 41 cells studied, 98% responded to noxious thermal stimuli. Heating the cutaneous receptive field with a series of stimuli from 35 to 43, 47, and 50 degrees C produced a graded increase in discharge rate. The responses were characterized by an onset, which occurred after the temperature change had either slowed or stopped, an acceleration in the discharge up to a peak, and then an adaptation to a new base-line level. The time constants of adaptation were faster than those reported for C polymodal nociceptors. 3. No systematic differences were found in the responses to noxious thermal stimuli of cells with wide dynamic range receptive fields and of cells with narrow dynamic range, high-threshold receptive fields. There were also no differences in the responses of cells located in the marginal zone and of cells located in the neck of the dorsal horn. 4. The relationship between peak frequency and final skin temperature with a 30 s stimulus duration can best be described by a power function with an exponent of 2.1. An increase in the stimulus duration to 120 s resulted in an increase in the exponent of the power function to 3.2. 5. Repetition of the series of 30-s heat stimuli resulted in an increase in peak frequency, total impulse count, and background activity. Repetition of stimuli having a duration of 120 s produced an increase in the peak frequency at 43 and 45 degrees C, a smaller increase at 47 degrees C, and a decrease at 50 degrees C. Background activity was increased by the lower temperature stimuli, but was decreased following higher temperature stimuli. 6. In six additional cells, the skin was heated with three consecutive presentations at each temperature level (43, 45, 47, and 50 degrees C) for 30 s. No change was observed in the peak frequencies of the responses to successive stimuli of the same intensity. However, the exponent of the power function relating the average peak frequency for the six cells to changes in skin temperature was 3.9. This exponent was larger than that seen when two series of graded heat stimuli of 120 s duration were used, indicating more sensitization despite the fact the total time of exposure to noxious heat was less. 7. A role for both high-threshold and wide dynamic range spinothalamic cells in transmitting nociceptive information to the diencephalon is postulated.

Posterior Triangular Thalamic Neurons Convey Nociceptive Messages to the Secondary Somatosensory and Insular Cortices in the Rat

“…Indeed the main properties of lamina I neurons are close to those of PoT nociceptive neurons: (1) numerous lamina I neurons respond strongly and specifically to noxious stimuli (Christensen and Perl, 1970;Bester et al, 2000), and (2) the slope of the stimulus-response curve of lamina I neurons is maximum between 46 and 50°C (Kenshalo et al, 1979;Bester et al, 2000). However, the receptive fields of lamina I neurons were generally small or very small (typically one digit) (Kenshalo et al, 1979;Bester et al, 2000), whereas those of PoT neurons were markedly larger (one to three portions of the body). This last point likely reflects a strong convergence of lamina I projections within the PoT (Gauriau and Bernard, 2004).…”

“…Because lamina I neurons are involved primarily in nociceptive processing (Christensen and Perl, 1970;Kenshalo et al, 1979;Bushnell et al, 1984;Craig and Kniffki, 1985;Bester et al, 2000), it is probable that they provide the main nociceptive input to PoT NS neurons. Indeed the main properties of lamina I neurons are close to those of PoT nociceptive neurons: (1) numerous lamina I neurons respond strongly and specifically to noxious stimuli (Christensen and Perl, 1970;Bester et al, 2000), and (2) the slope of the stimulus-response curve of lamina I neurons is maximum between 46 and 50°C (Kenshalo et al, 1979;Bester et al, 2000). However, the receptive fields of lamina I neurons were generally small or very small (typically one digit) (Kenshalo et al, 1979;Bester et al, 2000), whereas those of PoT neurons were markedly larger (one to three portions of the body).…”

Neuroplastic Changes Related to Pain Occur at Multiple Levels of the Human Somatosensory System: A Somatosensory-Evoked Potentials Study in Patients with Cervical Radicular Pain

“…Studies suggest, for example, that intense noxious stimulation or tissue injury can produce dramatic changes in sensitivity to both noxious and non-noxious stimulation as well as expansion of the receptive fields of neurons of the dorsal horn (Perl et al, 1976;Price et al, 1978;Kenshalo et al, 1979Kenshalo et al, , 1982McMahon and Wall, 1984;Woolf and King, 1990;Simone et al, 1991;Dougherty and Willis, 1992;Coderre et al, 1993). Sensitization and expansion of receptive fields in response to inflammation and tissue injury or electrical nerve stimulation have also been demonstrated in the thalamus (Guilbaud et al, 1986) and somatosensory cortex (Lamour et al, 1983).…”

Contribution of central neuroplasticity to pathological pain: review of clinical and experimental evidence

“…Dorsal horn neurons fire with increasing frequency in response to repeated applications of a noxious heat stimulus (Perl 1976;Kenshalo et al 1979). This sensitization of dorsal horn neurons occurs after various types of tissue injury including thermal injury (Price et al 1978;Kenshalo et a1.…”

“…Only recently has there been specific empirical evidence indicating noxious stimulus-induced changes in CNS function. The studies of Perl (1976) and Kenshalo et al (1979) were the first to demonstrate that noxious peripheral stimuli do produce changes in the sensitivity of dorsal horn neurons to further stimulation; while Woolf and Wall (Woolf 1983;Woolf and Wall 1986a) were the first to provide empirical evidence for a primary afferent input triggering sustained increases in central excitability. Woolf (1983) demonstrated that injury-induced increases in spinal cord excitability could be maintained even after local anesthesia of the injured site, providing empirical evidence that acute injury could produce lasting spinal changes.…”