Gender-Specific Effects of Prenatal and Adolescent Exposure to Tobacco Smoke on Auditory and Visual Attention

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.

Maternal Smoking During Pregnancy and Offspring Brain Structure and Function: Review and Agenda for Future Research

“…fMRI studies in adolescents suggest associations between MSDP and inefficient recruitment of task-relevant brain regions, including the temporal lobe, hippocampus, and cerebellum during response inhibition, attention, and memory tasks. As well, additive effects of MSDP and current smoking during adolescence were seen on temporal lobe activation (Jacobsen, Slotkin et al, 2007), suggesting that MSDP may potentiate effects of adolescent smoking on brain functional deficits. Of note, however, additive effects of current and prenatal exposure on brain function were in contrast to structural findings, which showed stronger effects of current exposure relative to prenatal exposure and no additive effects of current and prenatal exposure on white matter microstructure.…”

“…In general, the current body of literature is very small, and although each study involved unique analyses, several of the 11 studies involved analyses within overlapping participant samples (Jacobsen et al, 2006;Jacobsen, Picciotto et al, 2007;Jacobsen, Slotkin et al, 2007;Paus et al, 2008;Toro et al, 2008). Thus, integrated findings are based on only eight unique samples.…”

“…Jacobsen et al (2006) propose that prenatally exposed adolescents may smoke in order to overcome MSDP-related cognitive deficits (i.e., memory deficits). Jacobsen, Slotkin, et al (2007) also investigated effects of MSDP on fMRI response to auditory and visual attention tasks in a sample of 63 adolescent smokers and nonsmokers ages 16-18 years (33 exposed, measured by retrospective maternal report). MSDP (with and without adolescent smoking) was associated with greater temporal lobe activation (bilateral superior temporal gyrus) during an auditory attention task.…”

“…First, following the approach of Jacobsen et al (2006, Jacobsen, Slotkin, et al, 2007Jacobsen, Picciotto, et al, 2007), a cross-sectional approach could be used to investigate the effects of MSDP on brain structure/function in individuals diagnosed with clinical disorders (ADHD, CD, nicotine dependence). Such studies could lead to differential intervention approaches in exposed versus unexposed patients.…”

Prenatal Exposure to Maternal Cigarette Smoking and the Adolescent Cerebral Cortex

“…A recent study examined group differences in task-related brain activity, measured with functional magnetic resonance imaging (fMRI) in adolescent smokers with and without the history of PEMCS during the performance of attentional tasks; combined current (smokers) and prenatal exposure was associated with higher fMRI signal in several cortical regions involved in auditory attention (Jacobsen et al, 2007). At a receptor level, another study reported subtle differences in the expression of nicotinic and muscarinic acetylcholine receptors in the brains of 5-to 12-week-old foetuses exposed and nonexposed to maternal cigarette smoking (Falk et al, 2005).…”