Journal of Neurophysiology, Vol 66, Issue 3 1021-1032, Copyright © 1991 by APS

ARTICLES

Changes in tonic descending inhibition of spinal neurons with articular input during the development of acute arthritis in the cat

H. G. Schaible, V. Neugebauer, F. Cervero and R. F. Schmidt
Physiologisches Institut der Universitat Wurzburg, Federal Republic of Germany.

1. In 15 alpha-chloralose-anesthetized cats we studied the presence of tonic descending inhibition (TDI) of spinal neurons with input from the knee and its modulation during an acute inflammation of this joint. TDI of spinal neurons with articular input was assessed by applying reversible cold blocks to the lower thoracic cord. The amount of descending inhibition was estimated from the induction and/or increase of resting discharges and of the responses to mechanical stimuli to the knee and other structures during the transitory and reversible blocks. In each experiment one or a few neurons were investigated while the joint was in normal condition [altogether 15 nociceptive-specific (NS) and 6 wide-dynamic-range (WDR) neurons]. One of the neurons was then selected for long-term recordings during which an acute inflammation in the knee was induced by the intra-articular injection of kaolin and carrageenan. Before and during developing arthritis, cold blocks were applied to examine whether the amount of TDI would change during the inflammatory process. 2. The neurons with input from the normal knee were under TDI because application of the cold block induced or increased resting discharges and the responses to noxious compression of the knee and the adjacent thigh and lower leg. In 10 of 15 NS neurons, the response threshold was lowered into the innocuous range. In 9 of 17 cells tested, the excitatory receptive field expanded to the ipsilateral paw, and 4 neurons became inhibited by paw compression. Seven of 18 neurons tested revealed inhibitory receptive fields on the contralateral leg during cold block. The neurons were located in laminae IV-VII. 3. Fourteen neurons were continuously monitored during development of inflammation, and changes in the effectiveness of TDI were assessed by blocking the cord before and during the development of arthritis. In most neurons baseline resting activity in the intact state of the cord increased while the arthritis developed. This inflammation-evoked enhancement of resting discharges was more pronounced during periods of spinalization. Consequently, the differences between the resting discharges in the cold-blocked and the intact state were progressively enhanced in arthritis. 4. After induction of arthritis, the responses to compression of the knee joint increased in the intact state as well as during cold blocks. In 11 of 14 neurons, the differences between the responses in the spinal and intact state were progressively enlarged during the development of inflammation. A similar result was obtained for flexion of the injected knee.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				S. Neumann, J. M. Braz, K. Skinner, I. J. Llewellyn-Smith, and A. I. Basbaum Innocuous, Not Noxious, Input Activates PKC{gamma} Interneurons of the Spinal Dorsal Horn via Myelinated Afferent Fibers J. Neurosci., August 6, 2008; 28(32): 7936 - 7944. [Abstract] [Full Text] [PDF]

				W. Kincaid, M. J. Neubert, M. Xu, C. J. Kim, and M. M. Heinricher Role for Medullary Pain Facilitating Neurons in Secondary Thermal Hyperalgesia J Neurophysiol, January 1, 2006; 95(1): 33 - 41. [Abstract] [Full Text] [PDF]

				J. Kitagawa, K. Kanda, M. Sugiura, Y. Tsuboi, A. Ogawa, K. Shimizu, N. Koyama, H. Kamo, T. Watanabe, K. Ren, et al. Effect of Chronic Inflammation on Dorsal Horn Nociceptive Neurons in Aged Rats J Neurophysiol, June 1, 2005; 93(6): 3594 - 3604. [Abstract] [Full Text] [PDF]

				Y. B. Peng, Q. D. Ling, M. A. Ruda, and D. R. Kenshalo Electrophysiological Changes in Adult Rat Dorsal Horn Neurons After Neonatal Peripheral Inflammation J Neurophysiol, July 1, 2003; 90(1): 73 - 80. [Abstract] [Full Text] [PDF]

				K. Miki, Q.-Q. Zhou, W. Guo, Y. Guan, R. Terayama, R. Dubner, and K. Ren Changes in Gene Expression and Neuronal Phenotype in Brain Stem Pain Modulatory Circuitry After Inflammation J Neurophysiol, February 1, 2002; 87(2): 750 - 760. [Abstract] [Full Text] [PDF]

				Y. Guan, R. Terayama, R. Dubner, and K. Ren Plasticity in Excitatory Amino Acid Receptor-Mediated Descending Pain Modulation after Inflammation J. Pharmacol. Exp. Ther., February 1, 2002; 300(2): 513 - 520. [Abstract] [Full Text] [PDF]

				R. W. Hurley and D. L. Hammond Contribution of Endogenous Enkephalins to the Enhanced Analgesic Effects of Supraspinal {micro} Opioid Receptor Agonists after Inflammatory Injury J. Neurosci., April 1, 2001; 21(7): 2536 - 2545. [Abstract] [Full Text] [PDF]

				H. Bester, C. De Felipe, and S. P. Hunt The NK1 Receptor Is Essential for the Full Expression of Noxious Inhibitory Controls in the Mouse J. Neurosci., February 1, 2001; 21(3): 1039 - 1046. [Abstract] [Full Text] [PDF]

				H. Eutamene, A.-M. Coelho, V. Theodorou, M. Toulouse, M. Chovet, A. Doherty, J. Fioramonti, and L. Bueno Antinociceptive Effect of Pregabalin in Septic Shock-Induced Rectal Hypersensitivity in Rats J. Pharmacol. Exp. Ther., October 1, 2000; 295(1): 162 - 167. [Abstract] [Full Text]

				R. W. Hurley and D. L. Hammond The Analgesic Effects of Supraspinal {micro} and delta Opioid Receptor Agonists Are Potentiated during Persistent Inflammation J. Neurosci., February 1, 2000; 20(3): 1249 - 1259. [Abstract] [Full Text] [PDF]

				M. O. Urban and G. F. Gebhart Supraspinal contributions to hyperalgesia PNAS, July 6, 1999; 96(14): 7687 - 7692. [Abstract] [Full Text] [PDF]

				N. Danziger, J. Weil-Fugazza, D. Le Bars, and D. Bouhassira Alteration of Descending Modulation of Nociception during the Course of Monoarthritis in the Rat J. Neurosci., March 15, 1999; 19(6): 2394 - 2400. [Abstract] [Full Text] [PDF]

				A. K. Houghton, Y. Lu, and K. N. Westlund S-(+)-3-Isobutylgaba and Its Stereoisomer Reduces the Amount of Inflammation and Hyperalgesia in an Acute Arthritis Model in the Rat J. Pharmacol. Exp. Ther., May 1, 1998; 285(2): 533 - 538. [Abstract] [Full Text]

				C. Roza, J. M. A. Laird, and F. Cervero Spinal Mechanisms Underlying Persistent Pain and Referred Hyperalgesia in Rats With an Experimental Ureteric Stone J Neurophysiol, April 1, 1998; 79(4): 1603 - 1612. [Abstract] [Full Text] [PDF]

				M. Gozariu, D. Bragard, J.-C. Willer, and D. Le Bars Temporal Summation of C-Fiber Afferent Inputs: Competition Between Facilitatory and Inhibitory Effects on C-Fiber Reflex in the Rat J Neurophysiol, December 1, 1997; 78(6): 3165 - 3179. [Abstract] [Full Text] [PDF]

				M. V Hurley, D. L Scott, J. Rees, and D. J Newham Sensorimotor changes and functional performance in patients with knee osteoarthritis Ann Rheum Dis, November 1, 1997; 56(11): 641 - 648. [Abstract] [Full Text]

				M. Kaneko and D. L. Hammond Role of Spinal gamma -Aminobutyric AcidA Receptors in Formalin-Induced Nociception in the Rat J. Pharmacol. Exp. Ther., August 1, 1997; 282(2): 928 - 938. [Abstract] [Full Text]