Genetic inactivation of synaptosomal-associated protein 25 (SNAP-25) in adult hippocampal neural progenitors impairs pattern discrimination learning but not survival or structural maturation of newborn dentate granule cells

Hippocampus. 2018 Oct;28(10):735-744. doi: 10.1002/hipo.23008.

Abstract

Adult neurogenesis is necessary for proper cognition and behavior, however, the mechanisms that underlie the integration and maturation of newborn neurons into the pre-existing hippocampal circuit are not entirely known. In this study, we sought to determine the role of action potential (AP)-dependent synaptic transmission by adult-generated dentate granule cells (DGCs) in their survival and function within the existing circuitry. We used a triple transgenic mouse (NestinCreERT2 :Snap25fl/fl : tdTomato) to inducibly inactivate AP-dependent synaptic transmission within adult hippocampal progenitors and their progeny. Behavioral testing in a hippocampal-dependent A/B contextual fear-discrimination task revealed impaired discrimination learning in mice harboring SNAP-25-deficient adult-generated dentate granule cells (DGCs). Despite poor performance on this neurogenesis-dependent task, the production and survival of newborn DGCs was quantitatively unaltered in tamoxifen-treated NestinCreERT2 :Snap25fl/fl : tdTomato SNAP compared to tamoxifen-treated NestinCreERT2 :Snap25wt/wt : tdTomato control mice. Although SNAP-25-deficient adult DGCs displayed a small but statistically significant enhancement in proximal dendritic branching, their overall dendritic length and distal branching complexity was unchanged. SNAP-25-deficient newborn DGCs also displayed robust efferent mossy fiber output to CA3, with normal linear density of large mossy fiber terminals (LMTs). These studies suggest that AP-dependent neurotransmitter release by newborn DGCs is not essential for their survival or rudimentary structural maturation within the adult hippocampus.

Keywords: Adult hippocampal neurogenesis; contextual fear discrimination; memory; synaptic neurotransmission; time.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Cells, Cultured
  • Discrimination Learning / drug effects
  • Discrimination Learning / physiology
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / genetics
  • Fear / physiology
  • Glutamic Acid / pharmacology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Hippocampus / cytology*
  • Hippocampus / growth & development*
  • Learning Disabilities / genetics*
  • Learning Disabilities / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nestin / genetics
  • Nestin / metabolism
  • Neurogenesis / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Phosphopyruvate Hydratase / metabolism
  • RNA, Messenger / metabolism
  • Synaptosomal-Associated Protein 25 / deficiency*
  • Synaptosomal-Associated Protein 25 / genetics
  • Transfection

Substances

  • Nestin
  • RNA, Messenger
  • Synaptosomal-Associated Protein 25
  • Green Fluorescent Proteins
  • Glutamic Acid
  • Phosphopyruvate Hydratase