Changes in serotonin, serotonin transporter expression and serotonin denervation supersensitivity: involvement in chronic central pain after spinal hemisection in the rat

Exp Neurol. 2002 Jun;175(2):347-62. doi: 10.1006/exnr.2002.7892.

Abstract

Spinal cord injury (SCI) results in abnormal locomotor and pain syndromes in humans. In a rodent SCI model, T13 unilateral spinal hemisection results in bilateral mechanical allodynia and thermal hyperalgesia, partly by interruption of tonic descending serotonin (5-HT) inhibition. In the current study, we examined changes in density and distribution of 5-HT and 5-HT(T) in cervical (C8) and lumbar (L5) enlargements after T13 spinal hemisection and studied the effects of intrathecally delivered 5-HT (10, 21, and 63 microg), 5-HT antagonist methysergide (125 microg/kg), and 5-HT reuptake inhibitor fluvoxamine (75 microg/kg) on pain-related behaviors. Thirty-day-old male Sprague-Dawley rats were spinally hemisected and sacrificed at 3 (n = 20) and 28 (n = 20) days postsurgery for immunohistochemistry, Western blot, and ELISA analysis and compared against sham-operated animals (n = 10). At day 3, C8 5-HT levels were not significantly changed but at L5 there was a significant decrease in ipsilateral 5-HT in laminae I-II followed by incomplete recovery at 28 days postinjury. At both 3 and 28 days postinjury, C8 5-HT(T) levels were not significantly changed, but at L5 there was significant ipsilateral up-regulation of 5-HT(T) in laminae I-II. A second group of animals (n = 30) was hemisected and, starting at 28 days postinjury, behaviorally tested with intrathecal compounds. Increasing doses of 5-HT attenuated both fore- and hindlimb mechanical allodynia and thermal hyperalgesia, and effects of endogenous 5-HT were attenuated by methysergide and enhanced with fluvoxamine, all without locomotor alterations. Sham controls (n = 10) were unaffected. Thus, permanent changes occur in 5-HT and 5-HT(T) after SCI, denervation 5-HT supersensitivity develops, and modulation of 5-HT attenuates pain-related behaviors. Insight gained by these studies may aid in the understanding of dynamic 5-HT systems which will be useful in treating chronic central pain after SCI.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Blotting, Western
  • Carrier Proteins / analysis
  • Carrier Proteins / metabolism*
  • Denervation
  • Enzyme-Linked Immunosorbent Assay
  • Fluvoxamine / pharmacology
  • Hot Temperature
  • Hyperalgesia / drug therapy
  • Hyperalgesia / etiology
  • Hyperalgesia / metabolism
  • Immunohistochemistry
  • Injections, Spinal
  • Male
  • Membrane Glycoproteins / analysis
  • Membrane Glycoproteins / metabolism*
  • Membrane Transport Proteins*
  • Methysergide / pharmacology
  • Motor Activity / drug effects
  • Nerve Tissue Proteins*
  • Pain / drug therapy
  • Pain / etiology
  • Pain / metabolism*
  • Physical Stimulation
  • Rats
  • Rats, Sprague-Dawley
  • Selective Serotonin Reuptake Inhibitors / pharmacology
  • Serotonin / analysis
  • Serotonin / metabolism*
  • Serotonin Antagonists / pharmacology
  • Serotonin Plasma Membrane Transport Proteins
  • Spinal Cord / metabolism*
  • Spinal Cord Injuries / complications
  • Spinal Cord Injuries / metabolism*

Substances

  • Carrier Proteins
  • Membrane Glycoproteins
  • Membrane Transport Proteins
  • Nerve Tissue Proteins
  • Serotonin Antagonists
  • Serotonin Plasma Membrane Transport Proteins
  • Serotonin Uptake Inhibitors
  • Slc6a4 protein, rat
  • Serotonin
  • Fluvoxamine
  • Methysergide