Different developmental trajectories for anticipation and receipt of reward during adolescence

Hoogendam, Janna Marie; Kahn, René S.; Hillegers, Manon H. J.; Buuren, Mariët van; Vink, Matthijs

doi:10.1016/j.dcn.2013.08.004

Cited by 71 publications

(77 citation statements)

References 70 publications

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“…In contrast, a study of 10-25-year olds (n ¼ 39) modeled linear and quadratic age effects across subjects as opposed to using age groups. They found a positive linear relationship between age and ventral striatal activation to anticipation of reward and, in contrast to the present report, the quadratic term did not significantly contribute beyond the linear term (Hoogendam et al, 2013). It is possible that the more thorough interrogation of the developmental continuum reported on here-with a broader age range (8-27), larger sample (n ¼ 175), and repeated measures (473 sessions)-is necessary to reveal the inverted U-shaped trajectory of activation to reward anticipation during the MID.…”

Section: Discussioncontrasting

confidence: 55%

Effect of GABRA2 Genotype on Development of Incentive-Motivation Circuitry in a Sample Enriched for Alcoholism Risk

Heitzeg

Villafuerte

Weiland

et al. 2014

Neuropsychopharmacol

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Heightened reactivity of the incentive-motivation system has been proposed to underlie adolescent-typical risky behaviors, including problem alcohol involvement. However, even in adolescence considerable individual variation in these behaviors exists, which may have genetic underpinnings and be related to variations in risk for later alcohol use disorder (AUD). Variants in GABRA2 have been associated with adult alcohol dependence as well as phenotypic precursors, including impulsiveness and externalizing behaviors. We investigated the impact of GABRA2 on the developmental trajectory of nucleus accumbens (NAcc) activation during anticipation of monetary reward from childhood to young adulthood. Functional MRI during a monetary incentive delay task was collected in 175 participants, with the majority (n ¼ 151) undergoing repeated scanning at 1-to 2-year intervals. One group entered the study at age 8-13 years (n ¼ 76) and another entered at age 18-23 years (n ¼ 99). Most participants were children of alcoholics (79%) and thus at heightened risk for AUD. A total of 473 sessions were completed, covering ages 8-27 years. NAcc activation was heightened during adolescence compared with childhood and young adulthood. GABRA2 genotype (SNP rs279858) was associated with individual differences in NAcc activation specifically during adolescence, with the minor allele (G) associated with greater activation. Furthermore, NAcc activation mediated an effect of genotype on alcohol problems (n ¼ 104). This work demonstrates an impact of GABRA2 genotype on incentive-motivation neurocircuitry in adolescence, with implications for vulnerability to alcoholism. These findings represent an important step toward understanding the genetic and neural basis of individual differences in how risk for addiction unfolds across development.

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Section: Discussioncontrasting

confidence: 55%

Effect of GABRA2 Genotype on Development of Incentive-Motivation Circuitry in a Sample Enriched for Alcoholism Risk

Heitzeg

Villafuerte

Weiland

et al. 2014

Neuropsychopharmacol

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“…In the manner of previous fMRI studies investigating cognitive functioning, 18,32,36,45 region of interest (ROI) analyses were performed to test for group differences in 5 predefined regions that are known for their involvement in reward processing, including the bilateral ventral striatum, dorsal striatum, insula, SMA, and orbitofrontal cortices (also referred to as ventromedial prefrontal cortex) (figure 2). 22,36,38 Regions were created using the automated anatomical labeling-atlas. 46 For each ROI, the average level of brain activation (ie, percent signal change) was obtained for each subject.…”

Section: Functional Magnetic Resonance Imagingmentioning

confidence: 99%

“…Participants performed a reward task [35][36][37] (figure 1) based on the monetary incentive delay task. 22 This task allows the investigation of anticipation and receipt of reward, separately.…”

Section: Monetary Incentive Delay Taskmentioning

confidence: 99%

“…[35][36][37] Activation during reward anticipation and receipt of reward was investigated in regions involved in processing of reward: the bilateral ventral striatum, dorsal striatum, insula, SMA, and orbitofrontal cortex. 22,36,[38][39][40] As outlined above, we hypothesized that siblings show fronto-striatal deficits during reward processing comparable to that of schizophrenia patients. Specifically, we hypothesized that, similar to patients, activation in the ventral striatum is decreased during reward anticipation.…”

Section: Introductionmentioning

confidence: 99%

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Fronto-striatal Dysfunction During Reward Processing in Unaffected Siblings of Schizophrenia Patients

Leeuw

Kahn

Vink

2014

Schizophrenia Bulletin

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Schizophrenia is a psychiatric disorder that is associated with impaired functioning of the fronto-striatal network, in particular during reward processing. However, it is unclear whether this dysfunction is related to the illness itself or whether it reflects a genetic vulnerability to develop schizophrenia. Here, we examined reward processing in unaffected siblings of schizophrenia patients using functional magnetic resonance imaging. Brain activity was measured during reward anticipation and reward outcome in 27 unaffected siblings of schizophrenia patients and 29 healthy volunteers using a modified monetary incentive delay task. Task performance was manipulated online so that all subjects won the same amount of money. Despite equal performance, siblings showed reduced activation in the ventral striatum, insula, and supplementary motor area (SMA) during reward anticipation compared to controls. Decreased ventral striatal activation in siblings was correlated with sub-clinical negative symptoms. During the outcome of reward, siblings showed increased activation in the ventral striatum and orbitofrontal cortex compared to controls. Our finding of decreased activity in the ventral striatum during reward anticipation and increased activity in this region during receiving reward may indicate impaired cue processing in siblings. This is consistent with the notion of dopamine dysfunction typically associated with schizophrenia. Since unaffected siblings share on average 50% of their genes with their ill relatives, these deficits may be related to the genetic vulnerability for schizophrenia.

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“…Deficits in frontostriatal development may become apparent already during adolescence, when the striatum is fully maturing, and the frontal cortex is developing (Casey et al, 2008;Hoogendam et al, 2013;Vink et al, 2014a, b). Offspring of schizophrenia patients may be best suited to investigate the impact of genetic vulnerability on adolescent brain development, as they inherit on average half their DNA from their ill parent.…”

Section: Introductionmentioning

confidence: 99%

Changes in White Matter Organization in Adolescent Offspring of Schizophrenia Patients

Leeuw

Bohlken

Mandl

et al. 2016

Neuropsychopharmacol

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Schizophrenia is associated with frontostriatal network impairments underlying clinical and cognitive symptoms. We previously found disruptions in anatomical pathways, including the tract connecting the left nucleus accumbens and left dorsolateral prefrontal cortex (DLPFC). Similar deficits are observed in unaffected siblings of schizophrenia patients, indicating that these deficits are linked to a genetic vulnerability for the disorder. Frontostriatal tract disruptions may arise during adolescence, preceding the clinical manifestation of the disorder. However, to date, no studies have been performed to investigate frontostriatal tract connections in adolescents who are at increased familial risk for schizophrenia. In this study, we investigate the impact of familial risk on frontostriatal tract connections using diffusion tensor imaging in 27 adolescent offspring of schizophrenia patients and 32 matched control adolescents, aged 10-18 years. Mean fractional anisotropy (FA) was calculated for the tracts connecting the striatum (caudate nucleus, putamen, nucleus accumbens) and frontal cortex regions (DLPFC, medial orbital frontal cortex, inferior frontal gyrus). As expected, based on siblings data, we found an impact of familial risk on frontostriatal development: schizophrenia offspring showed increased FA in the tracts connecting nucleus accumbens and DLPFC as compared with control adolescents. Moreover, while FA increased across age in control adolescents, it did not in schizophrenia offspring. We did not find differences in FA in other frontostriatal tracts. These results indicate altered development of white matter in subjects who are at familial risk for schizophrenia and may precede frontostriatal white matter alterations in adult schizophrenia patients and siblings.

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Different developmental trajectories for anticipation and receipt of reward during adolescence

Cited by 71 publications

References 70 publications

Effect of GABRA2 Genotype on Development of Incentive-Motivation Circuitry in a Sample Enriched for Alcoholism Risk

Effect of GABRA2 Genotype on Development of Incentive-Motivation Circuitry in a Sample Enriched for Alcoholism Risk

Fronto-striatal Dysfunction During Reward Processing in Unaffected Siblings of Schizophrenia Patients

Changes in White Matter Organization in Adolescent Offspring of Schizophrenia Patients

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