Neonatal nicotine exposure impairs nicotinic enhancement of central auditory processing and auditory learning in adult rats

Eur J Neurosci. 2006 Aug;24(3):857-66. doi: 10.1111/j.1460-9568.2006.04945.x. Epub 2006 Jul 18.

Abstract

Children of women who smoke cigarettes during pregnancy display cognitive deficits in the auditory-verbal domain. Clinical studies have implicated developmental exposure to nicotine, the main psychoactive ingredient of tobacco, as a probable cause of subsequent auditory deficits. To test for a causal link, we have developed an animal model to determine how neonatal nicotine exposure affects adult auditory function. In adult control rats, nicotine administered systemically (0.7 mg/kg, s.c.) enhanced the sensitivity to sound of neural responses recorded in primary auditory cortex. The effect was strongest in cortical layers 3 and 4, where there is a dense concentration of nicotinic acetylcholine receptors (nAChRs) that has been hypothesized to regulate thalamocortical inputs. In support of the hypothesis, microinjection into layer 4 of the nonspecific nAChR antagonist mecamylamine (10 microM) strongly reduced sound-evoked responses. In contrast to the effects of acute nicotine and mecamylamine in adult control animals, neither drug was as effective in adult animals that had been treated with 5 days of chronic nicotine exposure (CNE) shortly after birth. Neonatal CNE also impaired performance on an auditory-cued active avoidance task, while having little effect on basic auditory or motor functions. Thus, neonatal CNE impairs nicotinic regulation of cortical function, and auditory learning, in the adult. Our results provide evidence that developmental nicotine exposure is responsible for auditory-cognitive deficits in the offspring of women who smoke during pregnancy, and suggest a potential underlying mechanism, namely diminished function of cortical nAChRs.

Publication types

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

MeSH terms

  • Acetylcholine / metabolism*
  • Animals
  • Animals, Newborn
  • Auditory Cortex / drug effects
  • Auditory Cortex / growth & development
  • Auditory Cortex / physiopathology
  • Auditory Pathways / drug effects
  • Auditory Pathways / growth & development
  • Auditory Pathways / physiopathology
  • Avoidance Learning / drug effects
  • Avoidance Learning / physiology
  • Cognition Disorders / chemically induced
  • Cognition Disorders / physiopathology
  • Disease Models, Animal
  • Female
  • Geniculate Bodies / drug effects
  • Geniculate Bodies / growth & development
  • Geniculate Bodies / physiopathology
  • Language Development Disorders / chemically induced*
  • Language Development Disorders / physiopathology
  • Learning Disabilities / chemically induced*
  • Learning Disabilities / physiopathology
  • Male
  • Nicotine / adverse effects*
  • Nicotinic Agonists / adverse effects
  • Nicotinic Antagonists / pharmacology
  • Pregnancy
  • Prenatal Exposure Delayed Effects / physiopathology*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, Nicotinic / drug effects*
  • Receptors, Nicotinic / metabolism
  • Smoking / adverse effects

Substances

  • Nicotinic Agonists
  • Nicotinic Antagonists
  • Receptors, Nicotinic
  • Nicotine
  • Acetylcholine