Defects in dendrite and spine maturation and synaptogenesis associated with an anxious-depressive-like phenotype of GABAA receptor-deficient mice

Neuropharmacology. 2015 Jan:88:171-9. doi: 10.1016/j.neuropharm.2014.07.019. Epub 2014 Aug 5.

Abstract

Mice that were rendered heterozygous for the γ2 subunit of GABAA receptors (γ2(+/-) mice) have been characterized extensively as a model for major depressive disorder. The phenotype of these mice includes behavior indicative of heightened anxiety, despair, and anhedonia, as well as defects in hippocampus-dependent pattern separation, HPA axis hyperactivity and increased responsiveness to antidepressant drugs. The γ2(+/-) model thereby provides strong support for the GABAergic deficit hypothesis of major depressive disorder. Here we show that γ2(+/-) mice additionally exhibit specific defects in late stage survival of adult-born hippocampal granule cells, including reduced complexity of dendritic arbors and impaired maturation of synaptic spines. Moreover, cortical γ2(+/-) neurons cultured in vitro show marked deficits in GABAergic innervation selectively when grown under competitive conditions that may mimic the environment of adult-born hippocampal granule cells. Finally, brain extracts of γ2(+/-) mice show a numerical but insignificant trend (p = 0.06) for transiently reduced expression of brain derived neurotrophic factor (BDNF) at three weeks of age, which might contribute to the previously reported developmental origin of the behavioral phenotype of γ2(+/-) mice. The data indicate increasing congruence of the GABAergic, glutamatergic, stress-based and neurotrophic deficit hypotheses of major depressive disorder.

Keywords: Animal model of anxious depression; Hippocampal synaptogenesis; Neurogenesis; Postnatal development; Synaptic spines.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anxiety / pathology
  • Anxiety / physiopathology*
  • Brain-Derived Neurotrophic Factor / metabolism
  • Cells, Cultured
  • Cerebral Cortex / growth & development
  • Cerebral Cortex / pathology
  • Cerebral Cortex / physiopathology
  • Dendrites / pathology
  • Dendrites / physiology*
  • Depression / pathology
  • Depression / physiopathology*
  • Depressive Disorder, Major
  • Disease Models, Animal
  • Female
  • Glutamic Acid / metabolism
  • Hippocampus / growth & development
  • Hippocampus / pathology
  • Hippocampus / physiopathology
  • Mice, 129 Strain
  • Neurogenesis / physiology
  • Phenotype
  • Receptors, GABA-A / deficiency*
  • Receptors, GABA-A / genetics
  • Synapses / pathology
  • Synapses / physiology*
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Brain-Derived Neurotrophic Factor
  • Gabrg2 protein, mouse
  • Receptors, GABA-A
  • Glutamic Acid
  • gamma-Aminobutyric Acid