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

Abstract

; for the IMAGEN Consortium 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.

Prefrontal Response and Frontostriatal Functional Connectivity to Monetary Reward in Abstinent Alcohol-Dependent Young Adults

“…Ideally, the field needs prospective studies that include the developmental window allowing assessment of the initiation of alcohol use and development of alcohol dependence. Relevant to this need, findings from the large, multisite IMAGEN consortium have contributed importantly to our understanding of the role of reward circuitry in young people at risk for addiction or early in the process of substance use (e.g., [50], [51], [52]). This study has reported that adolescents who are smokers [50], had prenatal exposure to nicotine [51], or had “potentially problematic” substance use [52] exhibit low VS responsiveness to reward.…”

“…Relevant to this need, findings from the large, multisite IMAGEN consortium have contributed importantly to our understanding of the role of reward circuitry in young people at risk for addiction or early in the process of substance use (e.g., [50], [51], [52]). This study has reported that adolescents who are smokers [50], had prenatal exposure to nicotine [51], or had “potentially problematic” substance use [52] exhibit low VS responsiveness to reward. Similarly, although we were not able to examine brain function before and after onset of alcohol use or dependence, we note that our sample has unique features that allow us to investigate frontostriatal function early in the course of alcohol use problems.…”

Weak ventral striatal responses to monetary outcomes predict an unwillingness to resist cigarette smoking

“…Namely, relative to nonsmokers, smokers display blunted subjective, behavioral, and neurobiological responses to nondrug rewards (e.g., al-Adawi & Powell, 1997; Martin-Soelch, Missimer, Leenders, & Schultz, 2003; Rose et al, 2012). These biases may be related to neuroadaptations associated with chronic cigarette use, preexisting vulnerabilities in reward functioning, or both (George & Koob, 2010; Kalivas & Volkow, 2005; Muller et al, 2013; Nees et al, 2013; Schneider et al, 2012; Sweitzer, Donny, & Hariri, 2012). Regardless of origin, this relative insensitivity to nondrug rewards presumably diminishes the impact of potential sources of motivation for maintaining smoking abstinence and thus serves as an important obstacle to smoking cessation.…”

Smoking, psychiatric illness and the brain

“…5 Nonetheless, children with ADHD born from mothers who smoked during pregnancy have been reported to have more severe behavioural problems than children with ADHD born from nonsmoking mothers, with a dose-response relationship between the amount smoked and several cognitive and clinical variables in the children. 6 At a neurobiological level maternal smoking during pregnancy has been shown to be associated with grey matter loss and cortical thinning 7 as well as functional alteration in neural circuitry involved in inhibitory control and reward 8,9 in children. There is also strong epidemiological evidence that smoking is associated with increased risk for dementia and the development of Alzheimer disease.…”