Individual differences in substance dependence: at the intersection of brain, behaviour and cognition

Recent theories of drug dependence propose that the transition from occasional recreational substance use to harmful use and dependence results from the impact of disrupted midbrain dopamine signals for reinforcement learning on frontal brain areas that implement cognitive control and decision‐making. We investigated this hypothesis in humans using electrophysiological and behavioral measures believed to assay the integrity of midbrain dopamine system and its neural targets. Our investigation revealed two groups of dependent individuals, one characterized by disrupted dopamine‐dependent reward learning and the other by disrupted error learning associated with depression‐proneness. These results highlight important neurobiological and behavioral differences between two classes of dependent users that can inform the development of individually tailored treatment programs.

[1]  R. Hodgson,et al.  The severity of alcohol dependence questionnaire: its use, reliability and validity. , 2010, British journal of addiction.

[2]  N. Volkow,et al.  Imaging dopamine's role in drug abuse and addiction , 2009, Neuropharmacology.

[3]  A. Rodríguez-Fornells,et al.  Genetic Variability in the Dopamine System (Dopamine Receptor D4, Catechol-O-Methyltransferase) Modulates Neurophysiological Responses to Gains and Losses , 2009, Biological Psychiatry.

[4]  Michael X. Cohen,et al.  Neurocomputational models of basal ganglia function in learning, memory and choice , 2009, Behavioural Brain Research.

[5]  Clay B. Holroyd,et al.  When is an error not a prediction error? An electrophysiological investigation , 2009, Cognitive, affective & behavioral neuroscience.

[6]  Markus Ullsperger,et al.  Neuropharmacology of performance monitoring , 2009, Neuroscience & Biobehavioral Reviews.

[7]  Clay B. Holroyd,et al.  The feedback correct-related positivity: sensitivity of the event-related brain potential to unexpected positive feedback. , 2008, Psychophysiology.

[8]  Lesley K Fellows,et al.  The human ventromedial frontal lobe is critical for learning from negative feedback. , 2008, Brain : a journal of neurology.

[9]  M. Reuter,et al.  Genetically Determined Differences in Learning from Errors , 2007, Science.

[10]  Tim Curran,et al.  Cross-task individual differences in error processing: Neural, electrophysiological, and genetic components , 2007, Cognitive, affective & behavioral neuroscience.

[11]  Clay B. Holroyd,et al.  Reward prediction error signals associated with a modified time estimation task. , 2007, Psychophysiology.

[12]  Michael X. Cohen,et al.  Reward expectation modulates feedback-related negativity and EEG spectra , 2007, NeuroImage.

[13]  S. Hyman.  The Neurobiology of Addiction: Implications for Voluntary Control of Behavior , 2007, The American journal of bioethics : AJOB.

[14]  P. Anderson.  Global use of alcohol, drugs and tobacco. , 2006, Drug and alcohol review.

[15]  J. Rehm,et al.  Global burden of disease from alcohol, illicit drugs and tobacco. , 2006, Drug and alcohol review.

[16]  B. Moghaddam,et al.  Progression of Cellular Adaptations in Medial Prefrontal and Orbitofrontal Cortex in Response to Repeated Amphetamine , 2006, The Journal of Neuroscience.

[17]  S. Hyman,et al.  Neural mechanisms of addiction: the role of reward-related learning and memory. , 2006, Annual review of neuroscience.

[18]  J. Polich,et al.  Neuropsychology and neuropharmacology of P3a and P3b. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[19]  E. Butelman,et al.  Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction , 2005, Nature Neuroscience.

[20]  G. Koob,et al.  Plasticity of reward neurocircuitry and the 'dark side' of drug addiction , 2005, Nature Neuroscience.

[21]  Michael J. Frank,et al.  Error-Related Negativity Predicts Reinforcement Learning and Conflict Biases , 2005, Neuron.

[22]  S. Hyman.  Addiction: a disease of learning and memory. , 2005, The American journal of psychiatry.

[23]  Olga V. Demler,et al.  Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. , 2005, Archives of general psychiatry.

[24]  R. Ali,et al.  Validation of the World Health Organization Alcohol, Smoking and Substance Involvement Screening Test (ASSIST): report of results from the Australian site. , 2005, Drug and alcohol review.

[25]  Bryan Kolb,et al.  Structural plasticity associated with exposure to drugs of abuse , 2004, Neuropharmacology.

[26]  A. Redish,et al.  Addiction as a Computational Process Gone Awry , 2004, Science.

[27]  Michael J. Frank,et al.  By Carrot or by Stick: Cognitive Reinforcement Learning in Parkinsonism , 2004, Science.

[28]  S. Cragg,et al.  Nicotine amplifies reward-related dopamine signals in striatum , 2004, Nature Neuroscience.

[29]  Nick Yeung,et al.  Alcohol and error processing , 2003, Trends in Neurosciences.

[30]  Samuel M. McClure,et al.  A computational substrate for incentive salience , 2003, Trends in Neurosciences.

[31]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[32]  Jonathan D. Cohen,et al.  Computational perspectives on dopamine function in prefrontal cortex , 2002, Current Opinion in Neurobiology.

[33]  G. Koob,et al.  Neurobiological Similarities in Depression and Drug Dependence: A Self-Medication Hypothesis , 1998, Neuropsychopharmacology.

[34]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[35]  R. Stephens,et al.  Alcohol and depression: Effects on mood and biased processing of self-relevant information. , 1995 .

[36]  G. Di Chiara,et al.  Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[37]  N. Rathod.  Society for the Study of Addiction , 1977 .

[38]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[39]  Clay B. Holroyd,et al.  Which way do I go? Neural activation in response to feedback and spatial processing in a virtual T-maze. , 2009, Cerebral cortex.

[40]  R. Ali,et al.  The effectiveness of a brief intervention for illicit drugs linked to the alcohol, smoking and substance involvement screening test (ASSIST) in primary health care settings: a technical report of phase iii findings of the WHO ASSIST randomized controlled trial. , 2008 .

[41]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[42]  Thérèse J. M. Overbeek,et al.  Dissociable Components of Error Processing on the Functional Significance of the Pe Vis-à-vis the Ern/ne Performance Monitoring Processes Reflected in the Ne and Pe Review of Studies That Report Both Ne and Pe: Associations and Dissociations Pharmacological Effects , 2022 .