GABAergic interneuronal loss and reduced inhibitory synaptic transmission in the hippocampal CA1 region after mild traumatic brain injury

Exp Neurol. 2015 Nov:273:11-23. doi: 10.1016/j.expneurol.2015.07.028. Epub 2015 Jul 31.

Abstract

Patients that suffer mild traumatic brain injuries (mTBI) often develop cognitive impairments, including memory and learning deficits. The hippocampus shows a high susceptibility to mTBI-induced damage due to its anatomical localization and has been implicated in cognitive and neurological impairments after mTBI. However, it remains unknown whether mTBI cognitive impairments are a result of morphological and pathophysiological alterations occurring in the CA1 hippocampal region. We investigated whether mTBI induces morphological and pathophysiological alterations in the CA1 using the controlled cortical impact (CCI) model. Seven days after CCI, animals subjected to mTBI showed cognitive impairment in the passive avoidance test and deficits to long-term potentiation (LTP) of synaptic transmission. Deficiencies in inducing or maintaining LTP were likely due to an observed reduction in the activation of NMDA but not AMPA receptors. Significant reductions in the frequency and amplitude of spontaneous and miniature GABAA-receptor mediated inhibitory postsynaptic currents (IPSCs) were also observed 7 days after CCI. Design-based stereology revealed that although the total number of neurons was unaltered, the number of GABAergic interneurons is significantly reduced in the CA1 region 7 days after CCI. Additionally, the surface expression of α1, ß2/3, and γ2 subunits of the GABAA receptor were reduced, contributing to a reduced mIPSC frequency and amplitude, respectively. Together, these results suggest that mTBI causes a significant reduction in GABAergic inhibitory transmission and deficits to NMDA receptor mediated currents in the CA1, which may contribute to changes in hippocampal excitability and subsequent cognitive impairments after mTBI.

Keywords: CA1; Cognitive impairment; Controlled cortical impact; Mild traumatic brain injury; Synaptic transmission.

Publication types

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

MeSH terms

  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Avoidance Learning / physiology
  • Brain Injuries / complications
  • Brain Injuries / pathology*
  • CA1 Region, Hippocampal / pathology*
  • Disease Models, Animal
  • Electric Stimulation
  • Excitatory Amino Acid Antagonists / pharmacology
  • GABAergic Neurons / pathology*
  • Glucose Transporter Type 1 / metabolism
  • Glutamate Decarboxylase / metabolism
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / physiology*
  • Interneurons / pathology
  • Male
  • Memory Disorders / etiology
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / physiology
  • Receptors, GABA-A / metabolism
  • Sodium Channel Blockers / pharmacology
  • Tetrodotoxin / pharmacology
  • Time Factors

Substances

  • Excitatory Amino Acid Antagonists
  • Glucose Transporter Type 1
  • Receptors, GABA-A
  • Sodium Channel Blockers
  • Tetrodotoxin
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1