Prenatal drug exposure and selective attention in preschoolers☆
Introduction
Alterations in arousal modulation and attentional control have repeatedly been demonstrated in infants and toddlers in controlled studies of prenatal cocaine exposure [6], [15], [31], [46], [49]. Similarly, infants with heavier prenatal cocaine exposure, compared with at-risk controls, have difficulty on tasks of inhibitory control [39]. The brain system that supports attention and inhibitory control, collectively called cognitive control, is the frontal–striatal system [8]. In experimental work with other species, this system is especially vulnerable to prenatal cocaine exposure because cocaine changes levels of neurotransmitters during gestation, which in turn have organizational effects on this brain system [34], [51], [52]. Recently, animal models of the behavioral effects of prenatal cocaine have suggested that the frontal–striatal systems necessary for establishing and maintaining selective response sets are at particular risk [24], [25].
Functioning in frontal–striatal areas is different in ADHD, and these differences have been linked to the ability of children with ADHD to form selective attentional sets and to withhold impulsive responses [12]. Imaging studies confirm that at-least by 4 or 5 years of age, selective attention and inhibitory control depend on frontal–striatal functioning [5], [13]. Deficits in selective attention, if found in cocaine-exposed preschoolers, would support the hypothesis that the frontal–striatal system is altered by prenatal cocaine exposure.
Bendersky and colleagues [7] recently reported an effect of prenatal cocaine exposure on impulsivity at 5 years of age. In a large cohort, prenatal cocaine exposure was associated with inferior ability to inhibited an non-rewarded motor response over time. In a modest sized group (n = 30, cocaine exposed) assessed at 6 and 10 years of age, Richardson and colleagues [42], [43] reported deficits of sustained attention associated with cocaine exposure, with cocaine exposed children showing reduced sustained attention but not selective attention deficits. Bandstra and colleagues replicated the sustained attention findings with a larger, higher-risk cohort of cocaine-exposed preschoolers, but did not investigate selective attention [2].
Mayes and colleagues reported preliminary data suggesting that cocaine exposure is associated with selective attention effects in 5 year olds [38]. However, group differences in their study might be accounted for by variability in severity of maternal/caregiver risk factors and prenatal exposure to other substances [28]. In particular, the report must be considered preliminarily because potentially confounding prenatal exposure to cigarettes was not adequately controlled for.
Prenatal cigarette exposure has been associated with deficits in both selective and sustained attention during the preschool years [for a review, Ref. 20]. In two large, well-controlled prospective studies, prenatal cigarette exposure was associated with decreased selective attention in preschoolers assessed using the CPT task [32], [53]. In Fried and colleagues' study, offspring of cigarette smokers had higher rates of commission errors on the CPT task at 4 [32] and 6 years [23]. This negative relationship between smoking and selective attention did not persist to later school ages [21]. Interestingly, this developmental pattern was replicated in another high-risk cohort, in which tobacco exposure was associated with sustained attention deficits at 6 years [33], but not 10 years of age [17]. There was a working memory deficit in the cigarette-exposed adolescents that suggests a developmentally persistent frontal–striatal effect of exposure [21].
Cocaine using mothers are also more likely to smoke marijuana than non-cocaine using women, and marijuana exposure also has effects that are suggestive of frontal–striatal deficits [23]. In separate, longitudinal studies, investigators [21], [3] found marijuana effects on sustained attention at 6 years and older. Fried and colleagues failed to find a marijuana effect at 4 years of age [32] despite the presence of a cigarette effect on CPT errors at that age.
There are conflicting findings regarding prenatal alcohol exposure and performance on attention tasks. Several studies failed to find a relationship between prenatal alcohol exposure and performance on attention tasks at early school age [42], [33], [17], [9], although one study did find such a relationship [53]. Coles and colleagues found performance on a sustained attention task affected by alcohol exposure in adolescents only for the subgroup with dysmorphology [14], suggesting that sample differences might account for the conflict in the literature.
In the current study, two attention tasks, each with sustained and selective attention components, were presented to 330 4-year-old children as part of a longitudinal prospective study of the developmental effects of prenatal cocaine exposure. Both tasks were chosen for their demonstrated sensitivity to ADHD in preschoolers [11] and consequent neuropsychological specificity.
Section snippets
Subjects
A total of 330 children were presented with at least one of two attention tasks: a continuous performance task (CPT) and a picture deletion task (PDT). As participants in a prospective study by Singer and colleagues, they had been followed since birth [46], [47]. The research was approved by hospital and university review boards and consent from custodial caregivers was obtained.
Of the 415 newborns recruited, 404 were living at 4 years. Of these, 28 children were unavailable at 4 years [49]. Of
Rate of passing pretests
Of the 329 children offered the PDT, most (301, 91%) passed the initial pretest and went on to participate in the test phase. Sixteen (5% of 329) failed the pretest and 12 (4% of the 329) refused to participate. The children in the cocaine-exposed group passed the pretest at a lower rate (88% passed) than the non-exposed children (95% passed, χ2 = 4.4, p < 0.04). Pretest success was not different by any other exposure grouping.
Of 181 children offered the CPT, most (n = 154, 85%) passed the pretest
Discussion
Young children whose mothers had used cocaine during their pregnancies produced a higher rate of commission errors on the CPT than children without cocaine exposure. The finding suggests that cocaine-exposed children had difficulty in maintaining selective attention sets. None of the postnatal environmental risk factors, maternal risk factors, or other substances used could account for these differences apart from prenatal cigarette exposure. The negative effect of cocaine was only independent
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Research was conducted in the laboratory of LTS at Case Western Reserve University. Research supported by NIDA R01-07957, General Clinical Research Center Grant (RR00080) to LTS, NIDA F32-05904 to JSN, and a grant from the Schubert Center of Child Development to EJS and R03-AA12618, PO ES11261-01 to CFB. Also, Paul Weishampel, Kristen Weingand, Laurie Ellision, Selena Cook, Astrida Seja Kaugars, and Teresa Linares for research and data assistance. Finally, the Vanderbilt Kennedy Center (P30-HD15052) supported manuscript preparation.