Early postnatal nicotine exposure disrupts the α2* nicotinic acetylcholine receptor-mediated control of oriens-lacunosum moleculare cells during adolescence in rats

Neuropharmacology. 2016 Feb:101:57-67. doi: 10.1016/j.neuropharm.2015.09.022. Epub 2015 Sep 16.

Abstract

Maternal cigarette smoking during pregnancy and maternal nicotine exposure in animal models are associated with cognitive impairments in offspring. However, the underlying mechanism remains unknown. Oriens-lacunosum moleculare (OLM) cells expressing α2* nicotinic acetylcholine receptors (nAChRs) are an important component of hippocampal circuitry, gating information flow and long-term potentiation (LTP) in the CA1 region. Here we investigated whether early postnatal nicotine exposure alters the normal role of α2*-nAChR-expressing OLM cells during adolescence in rats. We found that early postnatal nicotine exposure significantly decreased not only the number of α2-mRNA-expressing interneurons in the stratum oriens/alveus, but also α2*-nAChR-mediated responses in OLM cells. These effects of nicotine were prevented by co-administration with the nonselective nAChR antagonist mecamylamine, suggesting that nicotine-induced activation, but not desensitization, of nAChRs mediates the effects. α2*-nAChR-mediated depolarization of OLM cells normally triggers action potentials, causing an increase in spontaneous inhibitory postsynaptic currents in synaptically connected pyramidal cells. However, these α2*-nAChR-mediated effects were profoundly reduced after early postnatal nicotine exposure, suggesting altered control of CA1 circuits by α2*-nAChR-expressing OLM cells. Furthermore, these effects were associated with altered excitatory neural activity and LTP as well as the loss of normal α2*-nAChR-mediated control of excitatory neural activity and LTP. These findings suggest the altered function of α2*-nAChR-expressing OLM cells as an important target of further study for identifying the mechanisms underlying the cognitive impairment induced by maternal smoking during pregnancy.

Keywords: Development; Hippocampus; LTP; Nicotine; OLM cells; α2 nicotinic acetylcholine receptor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Age Factors
  • Animals
  • Animals, Newborn
  • Bicuculline / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • GABA-A Receptor Antagonists / pharmacology
  • Gene Expression Regulation, Developmental / drug effects*
  • Hippocampus / cytology
  • In Vitro Techniques
  • Interneurons / drug effects*
  • Interneurons / metabolism*
  • Long-Term Potentiation / drug effects*
  • Male
  • Nicotine / pharmacology*
  • Nicotinic Agonists / pharmacology*
  • Nicotinic Antagonists / pharmacology
  • Patch-Clamp Techniques
  • Pregnancy
  • Prenatal Exposure Delayed Effects / pathology
  • Quinoxalines / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Valine / analogs & derivatives
  • Valine / pharmacology

Substances

  • Excitatory Amino Acid Antagonists
  • GABA-A Receptor Antagonists
  • Nicotinic Agonists
  • Nicotinic Antagonists
  • Quinoxalines
  • FG 9041
  • Nicotine
  • 2-amino-5-phosphopentanoic acid
  • Valine
  • Bicuculline