1. ¹Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA
2. ²Department of Pediatrics, Yale University School of Medicine, New Haven, CT, USA
3. ³Haskins Laboratories, New Haven, CT, USA
4. ⁴Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, NC, USA

Correspondence: Dr LK Jacobsen, Psychiatry and Pediatrics, Yale University School of Medicine, 2 Church Street South, Suite 207, New Haven, CT 06519, USA. Tel: +1 203 764 8480; Fax: +1 203 764 8484; E-mail: leslie.jacobsen@yale.edu

Received 20 December 2006; Revised 14 February 2007; Accepted 16 February 2007; Published online 21 March 2007.

Abstract

Prenatal exposure to active maternal tobacco smoking elevates risk of cognitive and auditory processing deficits, and of smoking in offspring. Recent preclinical work has demonstrated a sex-specific pattern of reduction in cortical cholinergic markers following prenatal, adolescent, or combined prenatal and adolescent exposure to nicotine, the primary psychoactive component of tobacco smoke. Given the importance of cortical cholinergic neurotransmission to attentional function, we examined auditory and visual selective and divided attention in 181 male and female adolescent smokers and nonsmokers with and without prenatal exposure to maternal smoking. Groups did not differ in age, educational attainment, symptoms of inattention, or years of parent education. A subset of 63 subjects also underwent functional magnetic resonance imaging while performing an auditory and visual selective and divided attention task. Among females, exposure to tobacco smoke during prenatal or adolescent development was associated with reductions in auditory and visual attention performance accuracy that were greatest in female smokers with prenatal exposure (combined exposure). Among males, combined exposure was associated with marked deficits in auditory attention, suggesting greater vulnerability of neurocircuitry supporting auditory attention to insult stemming from developmental exposure to tobacco smoke in males. Activation of brain regions that support auditory attention was greater in adolescents with prenatal or adolescent exposure to tobacco smoke relative to adolescents with neither prenatal nor adolescent exposure to tobacco smoke. These findings extend earlier preclinical work and suggest that, in humans, prenatal and adolescent exposure to nicotine exerts gender-specific deleterious effects on auditory and visual attention, with concomitant alterations in the efficiency of neurocircuitry supporting auditory attention.