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Original Investigation |

Effect of Prenatal Exposure to Tobacco Smoke on Inhibitory Control:  Neuroimaging Results From a 25-Year Prospective Study

Nathalie E. Holz, MA1; Regina Boecker, MA1; Sarah Baumeister, MA1; Erika Hohm, MA1; Katrin Zohsel, PhD1; Arlette F. Buchmann, PhD1; Dorothea Blomeyer, PhD1; Christine Jennen-Steinmetz, PhD2; Sarah Hohmann, MD1; Isabella Wolf, PhD1,3; Michael M. Plichta, PhD4; Andreas Meyer-Lindenberg, MD, PhD4; Tobias Banaschewski, MD, PhD1; Daniel Brandeis, PhD1,5; Manfred Laucht, PhD1,6
[+] Author Affiliations
1Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
2Department of Biostatistics, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
3Department of Neuroimaging, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
4Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
5Department of Child and Adolescent Psychiatry, University of Zürich, Zürich, Switzerland
6Department of Psychology, University of Potsdam, Potsdam, Germany
JAMA Psychiatry. 2014;71(7):786-796. doi:10.1001/jamapsychiatry.2014.343.
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Importance  There is accumulating evidence relating maternal smoking during pregnancy to attention-deficit/hyperactivity disorder (ADHD) without elucidating specific mechanisms. Research investigating the neurobiological underpinnings of this disorder has implicated deficits during response inhibition. Attempts to uncover the effect of prenatal exposure to nicotine on inhibitory control may thus be of high clinical importance.

Objective  To clarify the influence of maternal smoking during pregnancy (hereafter referred to as prenatal smoking) on the neural circuitry of response inhibition and its association with related behavioral phenotypes such as ADHD and novelty seeking in the mother’s offspring.

Design, Setting, and Participants  Functional magnetic resonance imaging was performed for the offspring at 25 years of age during a modified Eriksen flanker/NoGo task, and voxel-based morphometry was performed to study brain volume differences of the offspring. Prenatal smoking (1-5 cigarettes per day [14 mothers] or >5 cigarettes per day [24 mothers]) and lifetime ADHD symptoms were determined using standardized parent interviews at the offspring’s age of 3 months and over a period of 13 years (from 2 to 15 years of age), respectively. Novelty seeking was assessed at 19 years of age. Analyses were adjusted for sex, parental postnatal smoking, psychosocial and obstetric adversity, maternal prenatal stress, and lifetime substance abuse. A total of 178 young adults (73 males) without current psychopathology from a community sample followed since birth (Mannheim, Germany) participated in the study.

Main Outcomes and Measures  Functional magnetic resonance imaging response, morphometric data, lifetime ADHD symptoms, and novelty seeking.

Results  Participants prenatally exposed to nicotine exhibited a weaker response in the anterior cingulate cortex (t168 = 4.46; peak Montreal Neurological Institute [MNI] coordinates x = −2, y = 20, z = 30; familywise error [FWE]–corrected P = .003), the right inferior frontal gyrus (t168 = 3.65; peak MNI coordinates x = 44, y = 38, z = 12; FWE-corrected P = .04), the left inferior frontal gyrus (t168 = 4.09; peak MNI coordinates x = −38, y = 36, z = 8; FWE-corrected P = .009), and the supramarginal gyrus (t168 = 5.03; peak MNI coordinates x = 64, y = −28, z = 22; FWE-corrected P = .02) during the processing of the NoGo compared to neutral stimuli, while presenting a decreased volume in the right inferior frontal gyrus. These findings were obtained irrespective of the adjustment of confounders, ADHD symptoms, and novelty seeking. There was an inverse relationship between inferior frontal gyrus activity and ADHD symptoms and between anterior cingulate cortex activity and novelty seeking.

Conclusions and Relevance  These findings point to a functional involvement of prenatal exposure to tobacco smoke in neural alterations similar to ADHD, which underlines the importance of smoking prevention treatments.

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Figures

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Figure 1.
Whole-Brain Activation During Inhibitory Control

NoGo vs neutral, displayed at familywise error–corrected P < .05 with the corresponding Montreal Neurological Institute z coordinate.

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Figure 2.
Effect of Maternal Smoking During Pregnancy on Brain Activation During Inhibitory Control (NoGo vs Neutral)

Activity is decreased in participants prenatally exposed to tobacco smoke in the anterior cingulate cortex (ACC; familywise error [FWE]–corrected P = .003) (A), the left inferior frontal gyrus (IFG; FWE-corrected P = .009) (B), the right IFG (FWE-corrected P = .04) (C), and the right supramarginal gyrus (SMG; FWE-corrected P = .02) (D). The corresponding mean parameter estimates of the nonexposed and exposed groups are indicated on the right, with the P values given for pairwise comparisons. Error bars indicate SEM; R, right.

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Figure 3.
Association Between Brain Activity and Behavioral Outcomes

Scatterplots of the correlation between the significant clusters of brain activations in the anterior cingulate cortex (ACC) and novelty seeking (A), of the correlation between the significant clusters of brain activations in the left inferior frontal gyrus (IFG) with novelty seeking and lifetime attention-deficit/hyperactivity disorder (ADHD) symptoms (B), and of the correlation between the significant clusters of brain activations in the right IFG and lifetime ADHD symptoms (C) are shown.

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Figure 4.
Effect of Maternal Smoking During Pregnancy on Volume in the Right Inferior Frontal Gyrus (IFG)

A, The volume decreased when the amount of prenatal tobacco exposure increased (familywise error–corrected P = .002). B, The corresponding mean parameter estimates of the nonexposed and the exposed groups are indicated, with the P values given for pairwise comparisons. Error bars indicate SEM; R, right.

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