Histone Deacetylase Inhibition Rescues Maternal Deprivation-Induced GABAergic Metaplasticity through Restoration of AKAP Signaling

Neuron. 2015 Jun 3;86(5):1240-52. doi: 10.1016/j.neuron.2015.05.024.

Abstract

Adverse early-life experiences such as child neglect and abuse increase the risk of developing addiction and stress-related disorders through alterations in motivational systems including the mesolimbic dopamine (DA) pathway. Here we investigated whether a severe early-life stress (i.e., maternal deprivation, MD) promotes DA dysregulation through an epigenetic impairment of synaptic plasticity within ventral tegmental area (VTA) DA neurons. Using a single 24-hr episode of MD and whole-cell patch clamp recording in rat midbrain slices, we show that MD selectively induces long-term depression (LTD) and shifts spike timing-dependent plasticity (STDP) toward LTD at GABAergic synapses onto VTA DA neurons through epigenetic modifications of postsynaptic scaffolding A-kinase anchoring protein 79/150 (AKAP79/150) signaling. Histone deacetylase (HDAC) inhibition rescues GABAergic metaplasticity and normalizes AKAP signaling in MD animals. MD-induced reversible HDAC-mediated GABAergic dysfunction within the VTA may be a mechanistic link for increased propensity to mental health disorders following MD.

Publication types

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

MeSH terms

  • A Kinase Anchor Proteins / physiology*
  • Animals
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • GABAergic Neurons / drug effects
  • GABAergic Neurons / physiology*
  • Histone Deacetylase Inhibitors / pharmacology*
  • Male
  • Maternal Deprivation*
  • Neuronal Plasticity / drug effects
  • Neuronal Plasticity / physiology*
  • Organ Culture Techniques
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / physiology*

Substances

  • A Kinase Anchor Proteins
  • AKAP5 protein, human
  • Akap5 protein, rat
  • Histone Deacetylase Inhibitors