Neuroeconomics and Adolescent Substance Abuse: Individual Differences in Neural Networks and Delay Discounting

doi:10.1016/j.jaac.2013.04.013

Journal of the American Academy of Child & Adolescent Psychiatry

Volume 52, Issue 7, July 2013, Pages 747-755.e6

https://doi.org/10.1016/j.jaac.2013.04.013 Get rights and content

Objective

Many adolescents with substance use problems show poor response to evidence-based treatments. Treatment outcome has been associated with individual differences in impulsive decision making as reflected by delay discounting (DD) rates (preference for immediate rewards). Adolescents with higher rates of DD were expected to show greater neural activation in brain regions mediating impulsive/habitual behavioral choices and less activation in regions mediating reflective/executive behavioral choices.

Method

Thirty adolescents being treated for substance abuse completed a DD task optimized to balance choices of immediate versus delayed rewards, and a control condition accounted for activation during magnitude valuation. A group independent component analysis on functional magnetic resonance imaging time courses identified neural networks engaged during DD. Network activity was correlated with individual differences in discounting rate.

Results

Higher discounting rates were associated with diminished engagement of an executive attention control network involving the dorsolateral prefrontal cortex, dorsomedial prefrontal cortex, inferior parietal cortex, cingulate cortex, and precuneus. Higher discounting rates also were associated with less deactivation in a “bottom-up” reward valuation network involving the amygdala, hippocampus, insula, and ventromedial prefrontal cortex. These 2 networks were significantly negatively correlated.

Conclusions

Results support relations between competing executive and reward valuation neural networks and temporal decision making, an important, potentially modifiable risk factor relevant for the prevention and treatment of adolescent substance abuse.

Clinical trial registration information—The Neuroeconomics of Behavioral Therapies for Adolescent Substance Abuse, http://clinicaltrials.gov/, NCT01093898.

Section snippets

Neural Mechanisms of DD

A meta-analysis identified 25 regions of significant neural activation during DD tasks.⁹ Three primary regions of robust activation include value-related regions (ventral striatum), value consideration regions (medial prefrontal cortex [PFC]), and future forecasting regions (posterior cingulate cortex). These regions are consistent with the valuation network proposed by Peters and Buchel,¹⁰ who also proposed 2 additional networks important in DD: a cognitive control network, involving

Participants

Participants were recruited from 2 ongoing studies investigating behavioral treatments for adolescent substance abuse (marijuana trial and alcohol trial). Fifty-two subjects enrolled in the treatment studies during recruitment for the present study. Two teens refused screening and 9 screened eligible but declined to participate in this study. Six subjects were not eligible for MRI owing to metal in their body (most often braces), and 2 reported claustrophobia and were not scanned. In addition,

Pairwise Contrasts

Voxel-wise, brain-wide planned contrasts of SS-CON and LL-CON choices resulted in distributed neural activations typically attributed to impulsive and deliberative choice behavior. Task-related activations are reported in Table S3, Table S4, available online, and represent those that survived a cluster-level correction for multiple comparisons.

SS Versus CON

Compared with the judgment of relative monetary amount in the CON trials, the choice of SS rewards was associated with activation of the dorsomedial,

Discussion

Whole-brain pairwise contrasts indicated extensive activations broadly consistent with many other DD fMRI studies.⁹ Group ICA yielded 7 components reflecting theoretically consistent regions of neural coactivation during all trials. Activation in 2 components or networks showed significant relations with individual DD rates. However, neither effect survived the Bonferroni correction, supporting the need to replicate these findings. One network, a putative valuation network, showed ventral

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Associations Between Family History of Alcohol and/or Substance Use Problems and Frontal Cortical Development From 9 to 13 Years of Age: A Longitudinal Analysis of the ABCD Study
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Previous investigations that have examined associations between family history (FH) of alcohol/substance use and adolescent brain development have been primarily cross-sectional. Here, leveraging a large population-based sample of youths, we characterized frontal cortical trajectories among 9- to 13-year-olds with (FH+) versus without (FH−) an FH and examined sex as a potential moderator.
We used data from 9710 participants in the Adolescent Brain Cognitive Development (ABCD) Study (release 4.0). FH+ was defined as having ≥1 biological parents and/or ≥2 biological grandparents with a history of alcohol/substance use problems (n = 2433). Our primary outcome was frontal cortical structural measures obtained at baseline (ages 9–11) and year 2 follow-up (ages 11–13). We used linear mixed-effects models to examine the extent to which FH status qualified frontal cortical development over the age span studied. Finally, we ran additional interactions with sex to test whether observed associations between FH and cortical development differed significantly between sexes.
For FH+ (vs. FH−) youths, we observed increased cortical thinning from 9 to 13 years across the frontal cortex as a whole. When we probed for sex differences, we observed significant declines in frontal cortical thickness among boys but not girls from ages 9 to 13 years. No associations were observed between FH and frontal cortical surface area or volume.
Having a FH+ is associated with more rapid thinning of the frontal cortex across ages 9 to 13, with this effect driven primarily by male participants. Future studies will need to test whether the observed pattern of accelerated thinning predicts future substance use outcomes.
Temporal discounting for self and friends in adolescence: A fMRI study
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Adolescence is characterized by impulsivity but also by increased importance of friendships. This study took the novel perspective of testing temporal discounting in a fMRI task where choices could affect outcomes for 96 adolescents (aged 10–20-years) themselves and their best friend. Decisions either benefitted themselves (i.e., the Self Immediate – Self Delay’ condition) or their friend (i.e., ‘Friend Immediate – Friend Delay’ condition); or juxtaposed rewards for themselves and their friends (i.e., the ‘Self Immediate – Friend Delay’ or ‘Friend Immediate – Self Delay’ conditions). We observed that younger adolescents were more impulsive; and all participants were more impulsive when this was associated with an immediate benefit for friends. Individual differences analyses revealed increased activity in the subgenual anterior cingulate cortex extending in the ventral striatum for immediate relative to delayed reward choices for self. Temporal choices were associated with activity in the prefrontal cortex, parietal cortex, insula, and ventral striatum, but only activity in the right inferior parietal lobe was associated with age. Finally, temporal delay choices for friends relative to self were associated with increased activity in the temporo-parietal junction and precuneus. Overall, this study shows a unique role of the social context in adolescents’ temporal decision making.
Developmental trajectories of delay discounting from childhood to young adulthood: longitudinal associations and test-retest reliability
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Delay discounting (DD) indexes an individual’s preference for smaller immediate rewards over larger delayed rewards, and is considered a form of cognitive impulsivity. Cross-sectional studies have demonstrated that DD peaks in adolescence; longitudinal studies are needed to validate this putative developmental trend, and to determine whether DD assesses a temporary state, or reflects a more stable behavioral trait. In this study, 140 individuals aged 9–23 completed a delay discounting (DD) task and cognitive battery at baseline and every-two years thereafter, yielding five assessments over approximately 10 years. Models fit with the inverse effect of age best approximated the longitudinal trajectory of two DD measures, hyperbolic discounting (log[k]) and area under the indifference-point curve (AUC). Discounting of future rewards increased rapidly from childhood to adolescence and appeared to plateau in late adolescence for both models of DD. Participants with greater verbal intelligence and working memory displayed reduced DD across the duration of the study, suggesting a functional interrelationship between these domains and DD from early adolescence to adulthood. Furthermore, AUC demonstrated good to excellent reliability across assessment points that was superior to log(k), with both measures demonstrating acceptable stability once participants reached late adolescence. The developmental trajectories of DD we observed from childhood through young adulthood suggest that DD may index cognitive control more than reward sensitivity, and that despite modest developmental changes with maturation, AUC may be conceptualized as a trait variable related to cognitive control vs impulsivity.
Neural networks during delay discounting as trans-disease marker: A meta-analytical review
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Delay discounting reflects a devaluation of delayed long-term benefits but pursuing immediate rewards. Higher discounting rates (h-DR) are found ubiquitous in many diseases and unhealthy conditions, particularly in addiction disorder (AD), attention-deficit/hyperactivity disorder (ADHD), and obesity. Thus, h-DR was considered to be a common benchmark across many diseases facilitating to understand one disease to relevant others, which was called trans-disease process. However, the common and specific neural biomarkers associated with this process has not yet been studied well. We performed a voxel-wise task-related neuroimaging meta-analysis to clarify the neural pattern of trans-disease process across AD, ADHD and obesity. We recruited 19 eligible papers, including 9 AD papers (154 patients), 6 ADHD papers (106 patients) and 4 obesity studies (94 patients). Neuroimaging meta-analysis demonstrated the presence of neural biomarkers of trans-disease process: these patients showed inadequate brain response in caudate, ventromedial and dorsolateral prefrontal cortex (dlPFC) than do of healthy controls (HCs). Disease-specific neural patterns were also found, with prominent hypoactivation in parahippocampal-striatum network for AD, hyperactivation in dopamine-projection striatum network for ADHD and decreased activity in dorsal anterior cingulate cortex and dlPFC for obesity. This study provided robust evidence to reveal the neural substrates of trans-disease process, as well further promoted the triple brain network model in favor of the theoretical developments of these neuropsychiatric disorders.
The neural basis underlying the relation between the action identification level and delay discounting: The medial and orbital frontal cortex functional connectivity with the precuneus
2021, International Journal of Psychophysiology
Citation Excerpt :
Similar effect was found in pathological gamblers that the episodic tags could enhance the striatal valuation signals during temporal discounting (Wiehler et al., 2017). In parallel to these results, studies showed that imaging future events allowed for increasing value on the later-larger rewards, biasing the subsequent decisions towards choices with a higher long-term pay-off (Benoit et al., 2011; Stanger et al., 2013). Intriguingly, higher identification levels were characteristic of the disengagement from immediate context to act in the light of distal significance (Vallacher and Wegner, 1989).
Previous studies have elucidated that action identification level brings ubiquitous effects in human life. The higher identification level is widely associated with future-oriented perspective, goal-directed actions, less impulsivity and so forth. However, little is known about how it relates to delay discounting. To address this issue, we sought to investigate the neural underpinning to understand their relations using voxel-based morphometry (VBM) and resting-state functional connectivity (RSFC) approaches. The behavioral results revealed that higher identification level was correlated with less discounting rate. The VBM results showed that gray matter (GM) volumes in left orbitofrontal cortex (OFC), left medial prefrontal cortex (mPFC) and right superior frontal gyrus (SFG) were positively correlated with action identification level. The RSFC results found that action identification level was positively associated with the functional connectivity between left OFC-left precuneus, and left mPFC-right precuneus respectively. Moreover, the structural equation modeling (SEM) showed that the association between the identification level and delay discounting was completely mediated by coupling of combined left OFC-left precuneus and left mPFC-right precuneus. These findings suggested that the functional communications within these brain regions in valuation and episodic prospection may account for the relationship between action identification level and delay discounting. The results enhanced our understanding of their relations from neural basis.
The associations of comorbid substance use disorders and psychiatric conditions with adolescent brain structure and function: A review
2020, Journal of the Neurological Sciences
Citation Excerpt :
In parallel, Stanger et al. [118], in their study on adolescents in treatment for AUD and marijuana use disorder (MUD), found participants with higher discounting rates had less deactivation throughout the reward network and less activation in more frontal areas than those with lower discounting rates [118]. While over one third of participants in this sample had comorbid ADHD, it is unclear how that diagnosis interacts with SUDs to affect neural response discounting rates [118]. However, another group found that adolescents with ADHD had lower activation in the right inferior frontal gyrus, dorsolateral PFC, anterior insula, dorsal striatum and bilateral cerebellum during the delayed discounting task, independent of discounting rates, relative to healthy comparisons [94].
Adolescence is a period of rapid neural and behavioral development that often precipitates substance use, substance use disorders (SUDs), and other psychopathology. While externalizing disorders have been closely linked to SUD epidemiologically, the comorbidity of internalizing disorders and SUD is less well understood. Neuroimaging studies can be used to measure structural and functional developments in the brain that mediate the relationship between psychopathology and SUD in adolescence. Externalizing disorders and SUD are both associated with structural and functional changes in the basal ganglia and prefrontal cortex in adolescence. The neural mechanisms underlying internalizing disorders and SUD are less clear, but evidence points to involvement of the amygdala and prefrontal cortex. We also highlight independent contributions of SUD, which may vary in certain ways by the substances assessed. A deeper understanding of the neural basis of the relationship between psychopathology and SUD will allow for more informed interventions in this critical developmental stage.

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: This research was funded by National Institute on Drug Abuse grants DA029442, DA015186, and DA022981, by National Institute on Alcohol Abuse and Alcoholism grant AA016917, and by UL1TR000039 and KL2TR000063 through the NIH National Center for Research Resources and the National Center for Advancing Translational Sciences.

: Disclosure: Dr. Stanger has received support from the National Institutes of Health (NIH) and the Sturgis Foundation. Dr. Budney has received support from the NIH. Dr. Kilts has received support from the NIH and has attended a scientific advisory board meeting for Allergan and a national advisory board meeting for a mental health facility (Skyland Trail). He is a co-holder of U.S. patent 6,373,990 (“Method and Device for the Transdermal Delivery of Lithium”). Drs. Elton, James, and Ryan report no biomedical financial interests or potential conflicts of interest.

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New researchNeuroeconomics and Adolescent Substance Abuse: Individual Differences in Neural Networks and Delay Discounting

Objective

Method

Results

Conclusions

Section snippets

Neural Mechanisms of DD

Participants

Pairwise Contrasts

SS Versus CON

Discussion

Drug Alcohol Depend

Trends Cogn Sci

Neuroimage

Behav Brain Res

Behav Brain Res

J Adolesc Health

Neuroimage

Drug Alcohol Depend

Biol Psychiatry

Delay discounting and the alcohol Stroop in heavy drinking adolescents

Addiction

Applying a behavioral economic framework to understanding adolescent smoking

Psychol Addict Behav

Delay discounting predicts postpartum relapse to cigarette smoking among pregnant women

Exp Clin Psychopharmacol

Delay discounting is associated with treatment response among cocaine-dependent outpatients

Exp Clin Psychopharmacol

Delay discounting predicts treatment outcome among adolescent substance abusers

Exp Clin Psychopharmacol

Functional neuroimaging of intertemporal choice models: a review

J Neurosci Psychol Econ

Development of the adolescent brain: implications for executive function and social cognition

J Child Psychol Psychiatry

Brain development during childhood and adolescence: a longitudinal MRI study

Nat Neurosci

Dynamic mapping of human cortical development during childhood through early adulthood

Proc Natl Acad Sci U S A

Discounting of delayed rewards: a life-span comparison

Psychol Sci.

New research
Neuroeconomics and Adolescent Substance Abuse: Individual Differences in Neural Networks and Delay Discounting