Changes in nociceptive sensitivity and object recognition in experimental autoimmune encephalomyelitis (EAE)

Exp Neurol. 2013 Mar:241:113-21. doi: 10.1016/j.expneurol.2012.12.012. Epub 2013 Jan 2.

Abstract

Multiple sclerosis is associated with a high incidence of depression, cognitive impairments and neuropathic pain. Previously, we demonstrated that tactile allodynia is present at disease onset in an animal model of MS, experimental autoimmune encephalomyelitis (EAE). We have now monitored changes in object recognition in mice with EAE to determine if altered nociceptive sensitivity is also associated with behavioral signs indicative of cognitive impairment in this model. At the onset of clinical signs, mice with EAE showed impairments in the novel object recognition (NOR) assay, indicative of deficits in cognitive functioning early in the disease course. At the spinal level, we found increased gene expression for the cytokines IL-1β, IL-6 and the glutamate transporter EAAT-2 that coincide with increased nociceptive sensitivity and deficits in object recognition. Increased levels of EAAT-2 mRNA appear to be a response to perturbed protein levels of the transporter as we found a loss of EAAT-2 protein levels in the spinal cord of EAE mice. To determine if changes in the levels of EAAT-2 were responsible for the observed changes in nociceptive sensitivity and cognitive deficits, we treated EAE mice with the β-lactam antibiotic ceftriaxone, an agent known to increase glutamate transporter levels in vivo. Ceftriaxone prevented tactile hypersensitivity and normalized performance in the NOR assay in EAE mice. These findings highlight the important interrelationship between pain and cognitive function in the disease and suggest that targeting spinally mediated pain hypersensitivity is a novel therapeutic avenue to treat impairments in other higher order cortical processes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Brain / drug effects
  • Brain / metabolism
  • Ceftriaxone / therapeutic use
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / chemically induced
  • Encephalomyelitis, Autoimmune, Experimental / complications*
  • Encephalomyelitis, Autoimmune, Experimental / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Excitatory Amino Acid Transporter 2 / genetics
  • Excitatory Amino Acid Transporter 2 / metabolism
  • Exploratory Behavior / drug effects
  • Female
  • Freund's Adjuvant / toxicity
  • Gene Expression Regulation / drug effects
  • Hyperalgesia / drug therapy
  • Hyperalgesia / etiology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Motor Activity / drug effects
  • Motor Activity / physiology
  • Myelin-Oligodendrocyte Glycoprotein / toxicity
  • Pain Measurement
  • Pain Threshold / drug effects
  • Pain Threshold / physiology*
  • Peptide Fragments / toxicity
  • RNA, Messenger / metabolism
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Recognition, Psychology / drug effects
  • Recognition, Psychology / physiology*
  • Rotarod Performance Test
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism
  • Time Factors

Substances

  • Excitatory Amino Acid Transporter 2
  • Interleukin-1beta
  • Interleukin-6
  • Myelin-Oligodendrocyte Glycoprotein
  • Peptide Fragments
  • RNA, Messenger
  • Receptors, N-Methyl-D-Aspartate
  • myelin oligodendrocyte glycoprotein (35-55)
  • Ceftriaxone
  • Freund's Adjuvant