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Original Investigation |

Altered Reward Processing in Adolescents With Prenatal Exposure to Maternal Cigarette Smoking

Kathrin U. Müller, Dipl-Psych1; Eva Mennigen, MD1; Stephan Ripke, Dipl-Psych1; Tobias Banaschewski, MD, PhD2; Gareth J. Barker, PhD4; Christian Büchel, MD8; Patricia Conrod, PhD4,6; Mira Fauth-Bühler, PhD2; Herta Flor, PhD2,3; Hugh Garavan, PhD9,10; Andreas Heinz, MD11; Claire Lawrence, PhD13; Eva Loth, PhD4,5; Karl Mann, MD2; Jean-Luc Martinot, MD, PhD16; Zdenka Pausova, MD14; Marcella Rietschel, MD2; Andreas Ströhle, MD11; Maren Struve, PhD2; Bernadeta Walaszek, PhD12; Gunter Schumann, MD4,5; Tomáš Paus, MD, PhD7,13,15; Michael N. Smolka, MD1 ; for the IMAGEN Consortium
[+] Author Affiliations
1Section of Neuroscience Systems, Department of Psychiatry and Psychotherapy, and Neuroimaging Center, Technische Universität Dresden, Dresden, Germany
2Central Institute of Mental Health, Medical Faculty Mannheim/Heidelberg University, Mannheim, Germany
3Medical Faculty, University of Heidelberg, Heidelberg, Germany
4Institute of Psychiatry, King’s College London, England
5MRC Social, Genetic, and Developmental Psychiatry Centre, London, England
6Department of Psychiatry, Universite de Montreal, University Hospital Center St Justine Hospital, Montreal, Quebec, Canada
7Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada
8Insitut für systemische Neurowissenschaften, Universitaetsklinikum Hamburg Eppendorf, Hamburg, Germany
9Institute of Neuroscience, School of Psychology, Trinity College Dublin, Dublin, Ireland
10Departments of Psychiatry and Psychology, University of Vermont, Burlington
11Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité–Universitätsmedizin Berlin, Germany
12Physikalisch-Technische Bundesanstalt, Berlin, Germany
13School of Psychology, University of Nottingham, Nottingham, England
14The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
15Rotman Research Institute, University of Toronto, Toronto, Ontario, Canada
16Institut National de la Santé et de la Recherche Médicale CEA Unit 1000 “Imaging and Psychiatry,” University Paris Sud, Orsay, and Department of Adolescent Psychopathology and Medicine, Assistance Publique–Hôpitaux de Paris, Maison de Solenn, University Paris Descartes, Paris, France
JAMA Psychiatry. 2013;70(8):847-856. doi:10.1001/jamapsychiatry.2013.44.
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Importance  Higher rates of substance use and dependence have been observed in the offspring of mothers who smoked during pregnancy. Animal studies indicate that prenatal exposure to nicotine alters the development of brain areas related to reward processing, which might be a risk factor for substance use and addiction later in life. However, no study has examined the effect of maternal smoking on the offspring’s brain response during reward processing.

Objective  To determine whether adolescents with prenatal exposure to maternal cigarette smoking differ from their nonexposed peers in the response of the ventral striatum to the anticipation or the receipt of a reward.

Design  An observational case-control study.

Setting  Data were obtained from the IMAGEN Study, a European multicenter study of impulsivity, reinforcement sensitivity, and emotional reactivity in adolescents. The IMAGEN sample consists of 2078 healthy adolescents (age range, 13-15 years) recruited from March 1, 2008, through December 31, 2011, in local schools.

Participants  We assessed an IMAGEN subsample of 177 adolescents with prenatal exposure to maternal cigarette smoking and 177 nonexposed peers (age range, 13-15 years) matched by sex, maternal educational level, and imaging site.

Main Outcome and Measure  Response to reward in the ventral striatum measured with functional magnetic resonance imaging.

Results  In prenatally exposed adolescents, we observed a weaker response in the ventral striatum during reward anticipation (left side, F = 14.98 [P < .001]; right side, F = 15.95 [P < .001]) compared with their nonexposed peers. No differences were found regarding the responsivity of the ventral striatum to the receipt of a reward (left side, F = 0.21 [P = .65]; right side, F = 0.47 [P = .49]).

Conclusions  The weaker responsivity of the ventral striatum to reward anticipation in prenatally exposed adolescents may represent a risk factor for substance use and development of addiction later in life. This result highlights the need for education and preventive measures to reduce smoking during pregnancy. Future analyses should assess whether prenatally exposed adolescents develop an increased risk for substance use and addiction and which role the reported neuronal differences during reward anticipation plays in this development.

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Figure 1.
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Time course of an example trial of the Monetary Incentive Delay task.

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Figure 2.
Response to Reward Anticipation and Feedback in the Ventral Striatum (VS) in Adolescents With Prenatal Exposure to Maternal Cigarette Smoking and Their Nonexposed Peers

A, Response of the VS in all participants to anticipation of any reward vs no reward. The display is set to threshold t = 4.88 (P < .05, familywise error [FWE] corrected with ≥25 contiguous voxels). B, Differences between nonexposed and exposed adolescents in signal change in the left and right VS to anticipation. Error bars indicate SEM. *P < .01. C, Response of the VS in all participants to feedback of win vs no win. The display is set to threshold t = 4.88 (P < .05, FWE corrected with ≥25 contiguous voxels). D, Differences between nonexposed and exposed adolescents in signal change in left and right VS to feedback. Error bars indicate SEM.

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