Neonatal Maternal Separation Impairs Prefrontal Cortical Myelination and Cognitive Functions in Rats Through Activation of Wnt Signaling

Cereb Cortex. 2017 May 1;27(5):2871-2884. doi: 10.1093/cercor/bhw121.

Abstract

Adverse early-life experience such as depriving the relationship between parents and children induces permanent phenotypic changes, and impairs the cognitive functions associated with the prefrontal cortex (PFC). However, the underlying mechanism remains unclear. In this work, we used rat neonatal maternal separation (NMS) model to illuminate whether and how NMS in early life affects cognitive functions, and what the underlying cellular and molecular mechanism is. We showed that rat pups separated from their dam 3 h daily during the first 3 postnatal weeks alters medial prefrontal cortex (mPFC) myelination and impairs mPFC-dependent behaviors. Myelination appears necessary for mPFC-dependent behaviors, as blockade of oligodendrocytes (OLs) differentiation or lysolecithin-induced demyelination, impairs mPFC functions. We further demonstrate that histone deacetylases 1/2 (HDAC1/2) are drastically reduced in NMS rats. Inhibition of HDAC1/2 promotes Wnt activation, which negatively regulates OLs development. Conversely, selective inhibition of Wnt signaling by XAV939 partly rescue myelination arrestment and behavior deficiency caused by NMS. These findings indicate that NMS impairs mPFC cognitive functions, at least in part, through modulation of oligodendrogenesis and myelination. Understanding the mechanism of NMS on mPFC-dependent behaviors is critical for developing pharmacological and psychological interventions for child neglect and abuse.

Keywords: early-life stress; histone deacetylases 1/2; learning; memory; oligodendrocyte.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Anxiety / etiology
  • Cognition Disorders / etiology*
  • Cognition Disorders / pathology
  • Demyelinating Diseases / etiology
  • Demyelinating Diseases / pathology*
  • Enzyme Inhibitors / pharmacology
  • Exploratory Behavior / drug effects
  • Gene Expression Regulation, Developmental / drug effects
  • Gene Expression Regulation, Developmental / physiology
  • Heterocyclic Compounds, 3-Ring / pharmacology
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Lipopolysaccharides / toxicity
  • Maternal Deprivation*
  • Maze Learning / drug effects
  • Myelin Basic Protein / metabolism
  • Neurogenesis / drug effects
  • Prefrontal Cortex / drug effects
  • Prefrontal Cortex / metabolism*
  • Prefrontal Cortex / pathology*
  • Prefrontal Cortex / ultrastructure
  • Rats
  • Rats, Sprague-Dawley
  • Valproic Acid / pharmacology
  • Wnt Proteins / genetics
  • Wnt Proteins / metabolism*
  • Wnt Signaling Pathway / drug effects
  • Wnt Signaling Pathway / physiology*

Substances

  • Enzyme Inhibitors
  • Heterocyclic Compounds, 3-Ring
  • Lipopolysaccharides
  • Myelin Basic Protein
  • Wnt Proteins
  • XAV939
  • Valproic Acid
  • Histone Deacetylases