Altered reward processing in adolescents with prenatal exposure to maternal cigarette smoking

TY - JOUR

T1 - Altered reward processing in adolescents with prenatal exposure to maternal cigarette smoking

AU - Müller, Kathrin U

AU - Mennigen, Eva

AU - Ripke, Stephan

AU - Banaschewski, Tobias

AU - Barker, Gareth J

AU - Büchel, Christian

AU - Conrod, Patricia

AU - Fauth-Bühler, Mira

AU - Flor, Herta

AU - Garavan, Hugh

AU - Heinz, Andreas

AU - Lawrence, Claire

AU - Loth, Eva

AU - Mann, Karl

AU - Martinot, Jean-Luc

AU - Pausova, Zdenka

AU - Rietschel, Marcella

AU - Ströhle, Andreas

AU - Struve, Maren

AU - Walaszek, Bernadeta

AU - Schumann, Gunter

AU - Paus, Tomáš

AU - Smolka, Michael N

AU - IMAGEN Consortium

PY - 2013

Y1 - 2013

N2 - 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.

AB - 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.

KW - Adolescent

KW - Basal Ganglia

KW - Case-Control Studies

KW - Female

KW - Functional Neuroimaging

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Mothers

KW - Pregnancy

KW - Prenatal Exposure Delayed Effects

KW - Retrospective Studies

KW - Reward

KW - Risk Factors

KW - Smoking

KW - Substance-Related Disorders

U2 - 10.1001/jamapsychiatry.2013.44

DO - 10.1001/jamapsychiatry.2013.44

M3 - SCORING: Journal article

C2 - 23784668

VL - 70

SP - 847

EP - 856

JO - JAMA PSYCHIAT

JF - JAMA PSYCHIAT

SN - 2168-622X

IS - 8

M1 - 8

ER -