Binge drinking impacts dorsal striatal response during decision making in adolescents

Adolescence is a time of both increased risk taking and increased vulnerability to the neurotoxic effects of alcohol. However, it is unclear whether brain functioning abnormalities in adolescent binge drinkers are a result of alcohol use itself or whether they represent premorbid risk characteristics. The current study addresses this question by using a modified version of the Wheel of Fortune (WOF) task, during functional magnetic resonance imaging (fMRI), at both baseline, while all subjects were alcohol-naïve, and revisit, when half of the subjects had emerged into regular binge drinking (n=13) and half remained alcohol and substance-naïve (n=13). Region of interest (ROI) analysis revealed that during decision making, there was a significant binge-drinking related reduction in brain activation in the dorsal striatum, an effect associated with degree of recent use. Furthermore, whole-brain analysis revealed a decrease in fronto-parietal brain activation prior to initiation of alcohol use, in adolescents who went on to binge drink. Additionally, there were numerous regions, both cortical and subcortical, in which there was a significant time-related developmental change, across groups. These results demonstrate how abnormalities in decision-making related circuitry might both lead to and perpetuate alcohol drinking behavior. These findings help aid in our ability to disentangle consequences of binge drinking from potential risk markers for future binge drinking, and may help guide future prevention and intervention strategies.

[1]  Serge A. R. B. Rombouts,et al.  Adolescent risky decision-making: Neurocognitive development of reward and control regions , 2010, NeuroImage.

[2]  Lindsay M. Squeglia,et al.  Binge drinking differentially affects adolescent male and female brain morphometry , 2011, Psychopharmacology.

[3]  J. Juraska,et al.  Effects of ethanol during adolescence on the number of neurons and glia in the medial prefrontal cortex and basolateral amygdala of adult male and female rats , 2012, Brain Research.

[4]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[5]  M. Reiff,et al.  Maturation of brain function associated with response inhibition. , 2003 .

[6]  Ashley R. Smith,et al.  Striatal sensitivity to reward deliveries and omissions in substance dependent patients , 2008, NeuroImage.

[7]  S. Tapert,et al.  Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects. , 2008, Alcoholism, clinical and experimental research.

[8]  B. Biswal,et al.  Functional connectivity of human striatum: a resting state FMRI study. , 2008, Cerebral cortex.

[9]  Karen A. Hudson,et al.  High and low sensation seeking adolescents show distinct patterns of brain activity during reward processing , 2013, NeuroImage.

[10]  C. Geier.  Adolescent cognitive control and reward processing: Implications for risk taking and substance use , 2013, Hormones and Behavior.

[11]  S. Tapert,et al.  Adolescent binge drinking linked to abnormal spatial working memory brain activation: differential gender effects. , 2011, Alcoholism, clinical and experimental research.

[12]  S. Tapert,et al.  Psychometric evaluation of the Customary Drinking and Drug Use Record (CDDR): a measure of adolescent alcohol and drug involvement. , 1998, Journal of studies on alcohol.

[13]  A. Bechara,et al.  Abnormal affective decision making revealed in adolescent binge drinkers using a functional magnetic resonance imaging study. , 2013, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[14]  Fredrick C. Redlich,et al.  Social class and mental illness: Community study. , 1958 .

[15]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[16]  N. Spear,et al.  Ethanol impairs memory of a simple discrimination in adolescent rats at doses that leave adult memory unaffected , 2004, Neurobiology of Learning and Memory.

[17]  Sarah-Jayne Blakemore,et al.  Imaging brain development: The adolescent brain , 2012, NeuroImage.

[18]  Philip Seeman,et al.  Human brain dopamine receptors in children and aging adults , 1987, Synapse.

[19]  R. Philpot,et al.  Repeated ethanol exposure during adolescence alters the developmental trajectory of dopaminergic output from the nucleus accumbens septi , 2009, International Journal of Developmental Neuroscience.

[20]  D. Fair,et al.  Emotional processing and brain activity in youth at high risk for alcoholism. , 2014, Alcoholism, clinical and experimental research.

[21]  L. Sobell,et al.  The reliability of the Alcohol Timeline Followback when administered by telephone and by computer. , 1996, Drug and alcohol dependence.

[22]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[23]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[24]  Christopher S. Monk,et al.  Choice selection and reward anticipation: an fMRI study , 2004, Neuropsychologia.

[25]  F. Crews,et al.  Binge ethanol consumption causes differential brain damage in young adolescent rats compared with adult rats. , 2000, Alcoholism, clinical and experimental research.

[26]  Scott A. Jones,et al.  Reduced cerebellar brain activity during reward processing in adolescent binge drinkers , 2015, Developmental Cognitive Neuroscience.

[27]  J. Ku,et al.  Disruption of Orbitofronto-Striatal Functional Connectivity Underlies Maladaptive Persistent Behaviors in Alcohol-Dependent Patients , 2013, Psychiatry investigation.

[28]  D. Cicchetti.  Methodological Commentary The Precision of Reliability and Validity Estimates Re-Visited: Distinguishing Between Clinical and Statistical Significance of Sample Size Requirements , 2001 .

[29]  Repeated binge-like ethanol drinking alters ethanol drinking patterns and depresses striatal GABAergic transmission. , 2014, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology.

[30]  D. Rosenberg,et al.  Changes in the dopaminergic innervation of monkey prefrontal cortex during late postnatal development: A tyrosine hydroxylase immunohistochemical study , 1994, Biological Psychiatry.

[31]  Connie Lim,et al.  Youth risk behavior surveillance - United States, 2011. , 2012, Morbidity and mortality weekly report. Surveillance summaries.

[32]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[33]  H. Uylings,et al.  Development of the dopaminergic innervation in the prefrontal cortex of the rat , 1988, The Journal of comparative neurology.

[34]  E. Levin,et al.  Binge pattern ethanol exposure in adolescent and adult rats: differential impact on subsequent responsiveness to ethanol. , 2000, Alcoholism, clinical and experimental research.

[35]  Susan F Tapert,et al.  A preliminary study of functional magnetic resonance imaging response during verbal encoding among adolescent binge drinkers. , 2010, Alcohol.

[36]  Richard H. Yaxley,et al.  Adolescent Alcohol Exposure Reduces Behavioral Flexibility, Promotes Disinhibition, and Increases Resistance to Extinction of Ethanol Self-Administration in Adulthood , 2014, Neuropsychopharmacology.

[37]  A. Dagher,et al.  Basal ganglia functional connectivity based on a meta-analysis of 126 positron emission tomography and functional magnetic resonance imaging publications. , 2006, Cerebral cortex.

[38]  F. Filbey,et al.  Integrating brain and behavior: evaluating adolescents' response to a cannabis intervention. , 2013, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[39]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[40]  J. Rice,et al.  Comparison of direct interview and family history diagnoses of alcohol dependence. , 1995, Alcoholism, clinical and experimental research.

[41]  N. Spear,et al.  Adolescent but not adult rats exhibit ethanol-mediated appetitive second-order conditioning. , 2008, Alcoholism, clinical and experimental research.

[42]  D. Fair,et al.  Resting state functional connectivity of the nucleus accumbens in youth with a family history of alcoholism , 2014, Psychiatry Research: Neuroimaging.

[43]  Patrick O'Malley,et al.  Monitoring the Future national survey results on drug use, 1975-2018: Overview, key findings on adolescent drug use , 2015 .

[44]  Russell A. Poldrack,et al.  Long-term test–retest reliability of functional MRI in a classification learning task , 2006, NeuroImage.

[45]  Mark S. Cohen,et al.  Parametric Analysis of fMRI Data Using Linear Systems Methods , 1997, NeuroImage.

[46]  Jerry L. Grenard,et al.  Affective decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in 10th grade Chinese adolescent binge drinkers , 2008, Neuropsychologia.

[47]  Ashley R. Smith,et al.  Cumulative gains enhance striatal response to reward opportunities in alcohol‐dependent patients , 2015, Addiction biology.

[48]  E. Levin,et al.  Differential effects of ethanol on memory in adolescent and adult rats. , 1998, Alcoholism, clinical and experimental research.

[49]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[50]  Lindsay M. Squeglia,et al.  Recent binge drinking predicts smaller cerebellar volumes in adolescents , 2013, Psychiatry Research: Neuroimaging.

[51]  V. Felipo,et al.  Repeated alcohol administration during adolescence causes changes in the mesolimbic dopaminergic and glutamatergic systems and promotes alcohol intake in the adult rat , 2009, Journal of neurochemistry.

[52]  L. Spear,et al.  Adolescent and adult heart rate responses to self-administered ethanol. , 2008, Alcoholism, clinical and experimental research.

[53]  A. Pfefferbaum,et al.  Brain responses to emotional salience and reward in alcohol use disorder , 2015, Brain Imaging and Behavior.

[54]  Martin P Paulus,et al.  Neural activation during inhibition predicts initiation of substance use in adolescence. , 2011, Drug and alcohol dependence.

[55]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[56]  D. Cicchetti,et al.  Developing criteria for establishing interrater reliability of specific items: applications to assessment of adaptive behavior. , 1981, American journal of mental deficiency.

[57]  Joseph L. Fleiss,et al.  Reliability of Measurement , 2011 .

[58]  Zhenbo Gao,et al.  Brain areas activated by uncertain reward-based decision-making in healthy volunteers , 2013, Neural regeneration research.

[59]  Joanna Jacobus,et al.  Altered white matter integrity in adolescent binge drinkers. , 2009, Alcoholism, clinical and experimental research.

[60]  Lisa T. Eyler,et al.  Neural correlates of verbal learning in adolescent alcohol and marijuana users. , 2011, Addiction.

[61]  Brian Knutson,et al.  Ventral Striatal Activation During Reward Anticipation Correlates with Impulsivity in Alcoholics , 2009, Biological Psychiatry.

[62]  B. Nagel,et al.  Risky decision-making: an FMRI study of youth at high risk for alcoholism. , 2012, Alcoholism, clinical and experimental research.

[63]  P C Hindmarsh,et al.  Performance of a new pubertal self-assessment questionnaire: a preliminary study. , 2001, Paediatric and perinatal epidemiology.

[64]  Patrick M. O'Malley,et al.  Monitoring the Future National Results on Adolescent Drug Use: Overview of Key Findings, 2004. , 2003 .

[65]  S. Blakemore,et al.  The Developmental Mismatch in Structural Brain Maturation during Adolescence , 2014, Developmental Neuroscience.

[66]  G. Canino,et al.  The DISC Predictive Scales (DPS): efficiently screening for diagnoses. , 2001, Journal of the American Academy of Child and Adolescent Psychiatry.