Elsevier

Experimental Neurology

Volume 147, Issue 2, October 1997, Pages 428-436
Experimental Neurology

Regular Article
Chronic Spinal Nerve Ligation Induces Changes in Response Characteristics of Nociceptive Spinal Dorsal Horn Neurons and in Their Descending Regulation Originating in the Periaqueductal Gray in the Rat

https://doi.org/10.1006/exnr.1997.6555Get rights and content

Abstract

We studied whether a chronic neuropathy induced by unilateral spinal nerve ligation changes the response characteristics of spinal dorsal horn wide-dynamic range (WDR) neurons or their periaqueductal gray (PAG)-induced descending modulation. Experiments were performed in rats with behaviorally demonstrated allodynia induced by spinal nerve ligation and in a group of nonneuropathic control rats. The stimulus–response functions of WDR neurons for mechanical and thermal stimuli and the modulation of their peripherally evoked responses by electrical stimulation of the PAG were determined under pentobarbital anesthesia. The results showed that neuropathy caused a significant leftward shift in stimulus–response functions for mechanical stimuli. In contrast, stimulus–response functions for noxious heat stimuli in the neuropathic limb were, if anything, shifted rightward, although this shift was short of statistical significance. In neuropathic rats, PAG stimulation produced a significantly stronger attenuation of spinal neuronal responses induced by noxious heat in the unoperated than in the operated side. At the intensity that produced attenuation of noxious heat stimuli, PAG stimulation did not produce any significant change in spinal neuronal responses evoked by mechanical stimuli either from the operated or the nonoperated hindlimb of the neuropathic rats. Spontaneous activity of WDR neurons was higher in the operated side of neuropathic rats than in control rats. Afterdischarges evoked by peripheral stimuli were observed in 1/16 of the WDR neurons ipsilateral to spinal nerve ligation and not at all in other experimental groups. The WDR neurons studied were not activated by innocuous or noxious cold stimuli. The results indicate that spinal nerve ligation induces increased spontaneous activity and enhanced responses to mechanical stimuli in the spinal dorsal horn WDR neurons, whereas noxious heat-evoked responses are not significantly changed or if anything, attenuated. Moreover, the inhibition of noxious heat stimuli by PAG stimulation is attenuated in the neuropathic side. It is proposed that the observed changes in the response characteristics of the spinal dorsal horn WDR neurons and in their descending modulation may contribute to the neuropathic symptoms in these animals.

References (36)

  • K. Takaishi et al.

    Behavioral and electrophysiological assessment of hyperalgesia and changes in dorsal horn responses following partial sciatic nerve ligation in rats

    Pain

    (1996)
  • R.-D. Treede et al.

    Peripheral and central mechanisms of cutaneous hyperalgesia

    Prog. Neurobiol.

    (1992)
  • M.O. Urban et al.

    Participation of central descending nociceptive facilitatory systems in secondary hyperalgesia

    Brain Res.

    (1996)
  • A.L. Vaccarino et al.

    Temporal processes of formalin pain: Differential role of the cingulum bundle, fornix pathway and medial bulboreticular formation

    Pain

    (1992)
  • E.P. Wiertelak et al.

    Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade

    Brain Res.

    (1994)
  • A.I. Basbaum et al.

    Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry

    Annu. Rev. Neurosci.

    (1984)
  • G.J. Bennett

    Animal models of neuropathic pain

    Prog. Pain Res. Manage.

    (1994)
  • Cited by (0)

    View full text