α2* Nicotinic acetylcholine receptors influence hippocampus-dependent learning and memory in adolescent mice

Learn Mem. 2017 May 15;24(6):231-244. doi: 10.1101/lm.045369.117. Print 2017 Jun.

Abstract

The absence of α2* nicotinic acetylcholine receptors (nAChRs) in oriens lacunosum moleculare (OLM) GABAergic interneurons ablate the facilitation of nicotine-induced hippocampal CA1 long-term potentiation and impair memory. The current study delineated whether genetic mutations of α2* nAChRs (Chrna2L9'S/L9'S and Chrna2KO) influence hippocampus-dependent learning and memory and CA1 synaptic plasticity. We substituted a serine for a leucine (L9'S) in the α2 subunit (encoded by the Chrna2 gene) to make a hypersensitive nAChR. Using a dorsal hippocampus-dependent task of preexposure-dependent contextual fear conditioning, adolescent hypersensitive Chrna2L9'S/L9'S male mice exhibited impaired learning and memory. The deficit was rescued by low-dose nicotine exposure. Electrophysiological studies demonstrated that hypersensitive α2 nAChRs potentiate acetylcholine-induced ion channel flux in oocytes and acute nicotine-induced facilitation of dorsal/intermediate CA1 hippocampal long-term potentiation in Chrna2L9'S/L9'S mice. Adolescent male mice null for the α2 nAChR subunit exhibited a baseline deficit in learning that was not reversed by an acute dose of nicotine. These effects were not influenced by locomotor, sensory or anxiety-related measures. Our results demonstrated that α2* nAChRs influenced hippocampus-dependent learning and memory, as well as nicotine-facilitated CA1 hippocampal synaptic plasticity.

MeSH terms

  • Action Potentials / drug effects
  • Action Potentials / genetics
  • Animals
  • Anxiety / genetics
  • Anxiety / pathology
  • Conditioning, Classical / drug effects
  • Conditioning, Classical / physiology
  • Disease Models, Animal
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / genetics
  • Fear / drug effects
  • Fear / physiology
  • Hippocampus / drug effects
  • Hippocampus / physiology*
  • Learning Disabilities / drug therapy
  • Learning Disabilities / genetics*
  • Learning Disabilities / pathology*
  • Locomotion / drug effects
  • Locomotion / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nicotine / therapeutic use
  • Nicotinic Agonists / therapeutic use
  • Oocytes
  • Receptors, Nicotinic / genetics
  • Receptors, Nicotinic / metabolism*
  • Stereotyped Behavior / drug effects
  • Stereotyped Behavior / physiology
  • Xenopus laevis

Substances

  • CHRNA2 protein, mouse
  • Nicotinic Agonists
  • Receptors, Nicotinic
  • Nicotine