Cortical network dysfunction caused by a subtle defect of myelination

Glia. 2016 Nov;64(11):2025-40. doi: 10.1002/glia.23039. Epub 2016 Jul 29.

Abstract

Subtle white matter abnormalities have emerged as a hallmark of brain alterations in magnetic resonance imaging or upon autopsy of mentally ill subjects. However, it is unknown whether such reduction of white matter and myelin contributes to any disease-relevant phenotype or simply constitutes an epiphenomenon, possibly even treatment-related. Here, we have re-analyzed Mbp heterozygous mice, the unaffected parental strain of shiverer, a classical neurological mutant. Between 2 and 20 months of age, Mbp(+/-) versus Mbp(+/+) littermates were deeply phenotyped by combining extensive behavioral/cognitive testing with MRI, 1H-MR spectroscopy, electron microscopy, and molecular techniques. Surprisingly, Mbp-dependent myelination was significantly reduced in the prefrontal cortex. We also noticed a mild but progressive hypomyelination of the prefrontal corpus callosum and low-grade inflammation. While most behavioral functions were preserved, Mbp(+/-) mice exhibited defects of sensorimotor gating, as evidenced by reduced prepulse-inhibition, and a late-onset catatonia phenotype. Thus, subtle but primary abnormalities of CNS myelin can be the cause of a persistent cortical network dysfunction including catatonia, features typical of neuropsychiatric conditions. GLIA 2016;64:2025-2040.

Keywords: Cnp mutant; MRI; catatonia; electron microscopy; myelin basic protein (Mbp) mutant; prepulse inhibition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 2',3'-Cyclic Nucleotide 3'-Phosphodiesterase / genetics
  • 2',3'-Cyclic Nucleotide 3'-Phosphodiesterase / metabolism
  • Age Factors
  • Animals
  • Disease Models, Animal
  • Exploratory Behavior / physiology
  • Female
  • Leukoencephalopathies / diagnostic imaging
  • Leukoencephalopathies / genetics
  • Leukoencephalopathies / pathology*
  • Leukoencephalopathies / physiopathology*
  • Maze Learning / physiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Microglia / metabolism
  • Microglia / pathology
  • Microglia / ultrastructure
  • Myelin Basic Protein / genetics
  • Myelin Basic Protein / metabolism
  • Myelin Sheath / genetics
  • Myelin Sheath / metabolism*
  • Myelin Sheath / ultrastructure
  • Neural Pathways / metabolism
  • Neural Pathways / pathology*
  • Neural Pathways / physiopathology
  • Nitric Oxide Synthase Type II / genetics
  • Nitric Oxide Synthase Type II / metabolism
  • Pregnancy
  • Prepulse Inhibition / genetics
  • Reflex, Startle / genetics
  • White Matter / pathology*
  • White Matter / ultrastructure

Substances

  • Myelin Basic Protein
  • Nitric Oxide Synthase Type II
  • 2',3'-Cyclic Nucleotide 3'-Phosphodiesterase
  • Cnp protein, mouse