Interactions between visceral and cutaneous nociception in the rat. I. Noxious cutaneous stimuli inhibit visceral nociceptive neurons and reflexes

Academic Article


  • Numerous studies have demonstrated that neural, behavioral, and reflex responses to a nociceptive test stimulus are inhibited by conditioning nociceptive stimuli; this inhibition has supraspinal, intraspinal, and segmental components. The general phenomenon is defined here as nocigenic inhibition. The present study of nocigenic inhibition documents that noxious cutaneous pinch and heat, used as conditioning stimuli, inhibit neuronal and reflex responses evoked by a noxious visceral stimulus, colorectal distension. A total of 196 dorsal horn neurons were examined: 110 were short latency-abrupt (SL-A) neurons that were excited at short latency by colorectal distension and returned to baseline activity abruptly after termination of the distending stimulus, and 86 were short latency-sustained (SL-S) neurons that also were excited by colorectal distension at short latency, but demonstrated after-discharges for 4-240 s after termination of the distending stimulus. All SL-A and SL-S neurons studied had convergent cutaneous receptive fields. The spontaneous activities of 100% of the 110 SL-A neurons tested were inhibited by >25% by noxious pinch in sites distant from their convergent cutaneous receptive fields. In both anesthetized, intact, and spinalized rats, noxious conditioning pinch or noxious conditioning heat significantly reduced responses of SL-A neurons during noxious test colorectal distension. The magnitude of this nocigenic inhibition was graded with the intensity of the noxious conditioning stimulus. Noxious conditioning tail heating produced a parallel shift to the right in stimulus-response functions relating neuronal responses to the intensity of colorectal distension (20-100 mmHg). The spontaneous activities of the 86 SL-S neurons examined were not uniformly affected by noxious pinch in sites distant from their convergent cutaneous receptive fields: 17% were inhibited by >25%, 64% were unaffected, and 19% were excited by >25%. All SL-S neurons excited by distant noxious pinch were located deeply in the dorsal horn (0.4-1.2 mm below cord dorsum) and had convergent cutaneous receptive fields excited only by noxious stimuli. SL-S neurons inhibited by distant noxious pinch were located both superficially (0.0-0.3 mm below cord dorsum) and deeply in the dorsal horn. The spontaneous activities of the total 196 dorsal horn neurons examined, when classified according to excitatory responses to stimuli in their convergent cutaneous receptive fields, were modulated by noxious pinch in distant (heterosegmental) cutaneous receptive fields as follows: 92% of the class 2 (excited by noxious and nonnoxious cutaneous stimuli) and 10% of the class 3 (excited only by noxious stimuli) neurons were inhibited >25%; 5% of the class 2 and 71% of the class 3 neurons were unaffected; and 2% of the class 2 and 19% of the class 3 neurons were excited >25%. The reflex contraction of abdominal muscles evoked by colorectal distension in decerebrate rats was inhibited in an intensity-dependent fashion by a noxious conditioning heat stimulus (immersion of the tail in 50-60°C water) as evidenced by a significant increase in the threshold distending pressure necessary to evoke the reflex. Noxious pinch of the forepaw also produced significant increases in the threshold distending pressure. These results demonstrate that nocigenic inhibition of spinal visceral nociceptive processing is similar to what has been described for the inhibition of spinal cutaneous nociceptive processing. These results suggest that at least two groups of neurons encoding for visceral nociception exist that can be differentiated by their susceptibility to nocigenic inhibitory influences.
  • Published In

    Digital Object Identifier (doi)

    Author List

  • Ness TJ; Gebhart GF
  • Start Page

  • 20
  • End Page

  • 28
  • Volume

  • 66
  • Issue

  • 1