Emotion, decision-making and substance dependence: a somatic-marker model of addiction.

Similar to patients with orbitofrontal cortex lesions, substance dependent individuals (SDI) show signs of impairments in decision-making, characterised by a tendency to choose the immediate reward at the expense of severe negative future consequences. The somatic-marker hypothesis proposes that decision-making depends in many important ways on neural substrates that regulate homeostasis, emotion and feeling. According to this model, there should be a link between abnormalities in experiencing emotions in SDI, and their severe impairments in decision-making in real-life. Growing evidence from neuroscientific studies suggests that core aspects of substance addiction may be explained in terms of abnormal emotional guidance of decision-making. Behavioural studies have revealed emotional processing and decision-making deficits in SDI. Combined neuropsychological and physiological assessment has demonstrated that the poorer decision-making of SDI is associated with altered reactions to reward and punishing events. Imaging studies have shown that impaired decision-making in addiction is associated with abnormal functioning of a distributed neural network critical for the processing of emotional information, including the ventromedial cortex, the amygdala, the striatum, the anterior cingulate cortex, and the insular/somato-sensory cortices, as well as non-specific neurotransmitter systems that modulate activities of neural processes involved in decision-making. The aim of this paper is to review this growing evidence, and to examine the extent of which these studies support a somatic-marker model of addiction.

[1]  W. Nauta The problem of the frontal lobe: a reinterpretation. , 1971, Journal of psychiatric research.

[2]  T. Robbins,et al.  Involvement of the amygdala in stimulus-reward associations: Interaction with the ventral striatum , 1989, Neuroscience.

[3]  K. Berridge,et al.  The neural basis of drug craving: An incentive-sensitization theory of addiction , 1993, Brain Research Reviews.

[4]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[5]  K. Berridge,et al.  The Mind of an Addicted Brain: Neural Sensitization of Wanting Versus Liking , 1995 .

[6]  A. Damasio REVIEW ■ : Toward a Neurobiology of Emotion and Feeling: Operational Concepts and Hypotheses , 1995 .

[7]  G. Fricchione Descartes’ Error: Emotion, Reason and the Human Brain , 1995 .

[8]  V L Villemagne,et al.  Activation of memory circuits during cue-elicited cocaine craving. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

[10]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[11]  J S Fowler,et al.  Decreases in dopamine receptors but not in dopamine transporters in alcoholics. , 1996, Alcoholism, clinical and experimental research.

[12]  N M White,et al.  Addictive drugs as reinforcers: multiple partial actions on memory systems. , 1996, Addiction.

[13]  A. Damasio,et al.  Deciding Advantageously Before Knowing the Advantageous Strategy , 1997, Science.

[14]  W. Blessing,et al.  The Lower Brainstem and Bodily Homeostasis , 1997 .

[15]  G D Pearlson,et al.  PET study of competition between intravenous cocaine and [11C]raclopride at dopamine receptors in human subjects. , 1997, The American journal of psychiatry.

[16]  S. J. Gatley,et al.  Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects , 1997, Nature.

[17]  N. Volkow,et al.  Dopamine D2 Receptor Availability in Opiate-Dependent Subjects before and after Naloxone-Precipitated Withdrawal , 1997, Neuropsychopharmacology.

[18]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[19]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[20]  J. Englander,et al.  Group psychotherapy for persons with traumatic brain injury: management of frustration and substance abuse. , 1998, The Journal of head trauma rehabilitation.

[21]  P F Renshaw,et al.  Functional magnetic resonance imaging of human brain activation during cue-induced cocaine craving. , 1998, The American journal of psychiatry.

[22]  J. Leathem,et al.  Incidence and outcomes of traumatic brain injury and substance abuse in a New Zealand prison population. , 1998, Brain injury.

[23]  W. Bickel,et al.  Shortened time horizons and insensitivity to future consequences in heroin addicts. , 1998, Addiction.

[24]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[25]  J S Fowler,et al.  Association of methylphenidate-induced craving with changes in right striato-orbitofrontal metabolism in cocaine abusers: implications in addiction. , 1999, The American journal of psychiatry.

[26]  W. Bickel,et al.  Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. , 1999, Journal of experimental psychology. General.

[27]  Gudrun Wagenknecht,et al.  ”Ecstasy”-induced changes of cerebral glucose metabolism and their correlation to acute psychopathology , 1999, European Journal of Nuclear Medicine.

[28]  JaneR . Taylor,et al.  Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli , 1999, Psychopharmacology.

[29]  G. Bartzokis,et al.  The incidence of T2-weighted MR imaging signal abnormalities in the brain of cocaine-dependent patients is age-related and region-specific. , 1999, AJNR. American journal of neuroradiology.

[30]  M. Reivich,et al.  Limbic activation during cue-induced cocaine craving. , 1999, The American journal of psychiatry.

[31]  N. Volkow,et al.  Reinforcing effects of psychostimulants in humans are associated with increases in brain dopamine and occupancy of D(2) receptors. , 1999, The Journal of pharmacology and experimental therapeutics.

[32]  J S Fowler,et al.  Regional brain metabolic activation during craving elicited by recall of previous drug experiences. , 1999, Life sciences.

[33]  S. Tiffany Cognitive Concepts of Craving , 1999, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[34]  T. Robbins,et al.  Associative Processes in Addiction and Reward The Role of Amygdala‐Ventral Striatal Subsystems , 1999, Annals of the New York Academy of Sciences.

[35]  T. Robbins,et al.  Dissociable Deficits in the Decision-Making Cognition of Chronic Amphetamine Abusers, Opiate Abusers, Patients with Focal Damage to Prefrontal Cortex, and Tryptophan-Depleted Normal Volunteers: Evidence for Monoaminergic Mechanisms , 1999, Neuropsychopharmacology.

[36]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[37]  Karl J. Friston,et al.  Neural responses associated with cue evoked emotional states and heroin in opiate addicts. , 2000, Drug and alcohol dependence.

[38]  Carlo Contoreggi,et al.  Drug abusers show impaired performance in a laboratory test of decision making , 2000, Neuropsychologia.

[39]  E. Stein,et al.  Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. , 2000, The American journal of psychiatry.

[40]  J S Fowler,et al.  Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. , 2000, Cerebral cortex.

[41]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[42]  T. Robbins,et al.  Chemical neuromodulation of frontal-executive functions in humans and other animals , 2000, Experimental Brain Research.

[43]  M. Ernst,et al.  Orbitofrontal cortex and human drug abuse: functional imaging. , 2000, Cerebral cortex.

[44]  J E Steinmetz,et al.  Decision-making biases, antisocial personality, and early-onset alcoholism. , 2000, Alcoholism, clinical and experimental research.

[45]  U. Frith,et al.  Neurocognitive explanations of the antisocial personality disorders , 2000 .

[46]  Steven W Anderson,et al.  Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers , 2001, Neuropsychologia.

[47]  T L Faber,et al.  Neural activity related to drug craving in cocaine addiction. , 2001, Archives of general psychiatry.

[48]  J. Lorberbaum,et al.  From the Departments Of , 2022 .

[49]  C. Kilts Imaging the roles of the amygdala in drug addiction. , 2001, Psychopharmacology bulletin.

[50]  W. Schultz,et al.  Changes in reward‐induced brain activation in opiate addicts , 2001, The European journal of neuroscience.

[51]  A L Malizia,et al.  Changes in regional cerebral blood flow elicited by craving memories in abstinent opiate-dependent subjects. , 2001, The American journal of psychiatry.

[52]  U. Hess,et al.  Impaired emotional facial expression recognition in alcoholism compared with obsessive-compulsive disorder and normal controls , 2001, Psychiatry Research.

[53]  M. Iyo,et al.  Methamphetamine-related psychiatric symptoms and reduced brain dopamine transporters studied with PET. , 2001, The American journal of psychiatry.

[54]  J S Fowler,et al.  Higher cortical and lower subcortical metabolism in detoxified methamphetamine abusers. , 2001, The American journal of psychiatry.

[55]  M D Devous,et al.  Limbic responsiveness to procaine in cocaine-addicted subjects. , 2001, The American journal of psychiatry.

[56]  J S Fowler,et al.  Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. , 2001, The American journal of psychiatry.

[57]  J. Haycock,et al.  Striatal Dopaminergic and Serotonergic Markers in Human Heroin Users , 2001, Neuropsychopharmacology.

[58]  Kimberly L. Napier,et al.  Three decision-making tasks in cocaine-dependent patients: do they measure the same construct? , 2001, Addiction.

[59]  J C Gore,et al.  Functional magnetic resonance imaging of cocaine craving. , 2001, The American journal of psychiatry.

[60]  J. Swanson,et al.  Relationship between blockade of dopamine transporters by oral methylphenidate and the increases in extracellular dopamine: Therapeutic implications , 2002, Synapse.

[61]  Hanna Damasio,et al.  Decision-making and addiction (part I): impaired activation of somatic states in substance dependent individuals when pondering decisions with negative future consequences , 2002, Neuropsychologia.

[62]  A. Bechara,et al.  Decision-making and addiction (part II): myopia for the future or hypersensitivity to reward? , 2002, Neuropsychologia.

[63]  Marc A Schuckit,et al.  Behavioral and Functional Neuroimaging Evidence for Prefrontal Dysfunction in Methamphetamine-Dependent Subjects , 2002, Neuropsychopharmacology.

[64]  Barry J. Everitt,et al.  Psychomotor Stimulant Addiction: A Neural Systems Perspective , 2002, The Journal of Neuroscience.

[65]  Nunzio Pomara,et al.  Reduced frontal white matter integrity in cocaine dependence: a controlled diffusion tensor imaging study , 2002, Biological Psychiatry.

[66]  T. Robbins,et al.  Decision-making deficits in drug addiction , 2002, Trends in Cognitive Sciences.

[67]  Brian Knutson,et al.  The role of brain emotional systems in addictions: a neuro-evolutionary perspective and new 'self-report' animal model. , 2002, Addiction.

[68]  R. Blair,et al.  Risky decisions and response reversal: is there evidence of orbitofrontal cortex dysfunction in psychopathic individuals? , 2002, Neuropsychologia.

[69]  R. Buchert,et al.  Specific neurotoxicity of chronic use of ecstasy. , 2002, Toxicology letters.

[70]  J. Metcalfe,et al.  Neural Systems and Cue-Induced Cocaine Craving , 2002, Neuropsychopharmacology.

[71]  Daniel Tranel,et al.  Asymmetric Functional Roles of Right and Left Ventromedial Prefrontal Cortices in Social Conduct, Decision-Making, and Emotional Processing , 2002, Cortex.

[72]  Jean Logan,et al.  Brain DA D2 receptors predict reinforcing effects of stimulants in humans: Replication study , 2002, Synapse.

[73]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[74]  Erno J. Hermans,et al.  Defective somatic markers in sub-clinical psychopathy , 2002, Neuroreport.

[75]  J. Busemeyer,et al.  A contribution of cognitive decision models to clinical assessment: decomposing performance on the Bechara gambling task. , 2002, Psychological assessment.

[76]  P. Whitney,et al.  Somatic markers, working memory, and decision making , 2002, Cognitive, affective & behavioral neuroscience.

[77]  G. Heyman,et al.  Decision biases and persistent illicit drug use: an experimental study of distributed choice and addiction. , 2002, Drug and alcohol dependence.

[78]  Linda Chang,et al.  Perfusion MRI and computerized cognitive test abnormalities in abstinent methamphetamine users , 2002, Psychiatry Research: Neuroimaging.

[79]  Joseph A Maldjian,et al.  Decreased gray matter concentration in the insular, orbitofrontal, cingulate, and temporal cortices of cocaine patients , 2002, Biological Psychiatry.

[80]  T. Robbins,et al.  The effects of tryptophan depletion on cognitive and affective processing in healthy volunteers , 2002, Psychopharmacology.

[81]  Rita Z. Goldstein,et al.  Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. , 2002, The American journal of psychiatry.

[82]  H. Flor,et al.  Development of alcohol-associated cues and cue-induced brain activation in alcoholics , 2002, European Psychiatry.

[83]  Matthew P. G. Allin,et al.  Ketamine alters neural processing of facial emotion recognition in healthy men: an fMRI study , 2003, Neuroreport.

[84]  David J. Nutt,et al.  Functional connectivity analysis of the neural circuits of opiate craving: “more” rather than “different”? , 2003, NeuroImage.

[85]  A. Damasio,et al.  Role of the Amygdala in Decision‐Making , 2003, Annals of the New York Academy of Sciences.

[86]  Luke Clark,et al.  The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage , 2003, Neuropsychologia.

[87]  A. Lawrence,et al.  Compulsive use of dopamine replacement therapy in Parkinson's disease: reward systems gone awry? , 2003, The Lancet Neurology.

[88]  Ingmar H. A. Franken,et al.  Drug craving and addiction: integrating psychological and neuropsychopharmacological approaches , 2003, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[89]  Kazuo Shigemasu,et al.  Application of the somatic marker hypothesis to individual differences in decision making , 2003, Biological Psychology.

[90]  F Brambilla,et al.  Neuroendocrine responses to experimentally-induced emotions among abstinent opioid-dependent subjects. , 2003, Drug and alcohol dependence.

[91]  Martin P Paulus,et al.  Error‐rate‐related caudate and parietal cortex activation during decision making , 2003, Neuroreport.

[92]  Marc A Schuckit,et al.  Decision making by methamphetamine-dependent subjects is associated with error-rate-independent decrease in prefrontal and parietal activation , 2003, Biological Psychiatry.

[93]  U. Hess,et al.  Impaired emotional facial expression recognition in alcoholics, opiate dependence subjects, methadone maintained subjects and mixed alcohol-opiate antecedents subjects compared with normal controls , 2003, Psychiatry Research.

[94]  Jean-Lud Cadet,et al.  Frontal cortical tissue composition in abstinent cocaine abusers: a magnetic resonance imaging study , 2003, NeuroImage.

[95]  T. Duka,et al.  Mixed emotions: alcoholics’ impairments in the recognition of specific emotional facial expressions , 2003, Neuropsychologia.

[96]  R. Rogers,et al.  Effects of beta-adrenoceptor blockade on components of human decision-making , 2004, Psychopharmacology.

[97]  B. Sahakian,et al.  Relationship between ecstasy use and depression: a study controlling for poly-drug use , 2004, Psychopharmacology.

[98]  Monique Ernst,et al.  Decision making in adolescents with behavior disorders and adults with substance abuse. , 2003, The American journal of psychiatry.

[99]  Kent A. Kiehl,et al.  Orbitofrontal cortex dysfunction in abstinent cocaine abusers performing a decision-making task , 2003, NeuroImage.

[100]  M. Kamachi,et al.  Low doses of alcohol have a selective effect on the recognition of happy facial expressions , 2003, Human psychopharmacology.

[101]  Matthew D. Albaugh,et al.  Decreased Absolute Amygdala Volume in Cocaine Addicts , 2004, Neuron.

[102]  P. Laurienti,et al.  Long-term heavy marijuana users make costly decisions on a gambling task. , 2004, Drug and alcohol dependence.

[103]  N. Volkow,et al.  Partial recovery of brain metabolism in methamphetamine abusers after protracted abstinence. , 2004, The American journal of psychiatry.

[104]  A. Bechara The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage , 2004, Brain and Cognition.

[105]  James L. McClelland,et al.  A reexamination of the evidence for the somatic marker hypothesis: what participants really know in the Iowa gambling task. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[106]  H. Curran,et al.  The acute and sub-acute effects of 'ecstasy' (MDMA) on processing of facial expressions: preliminary findings. , 2004, Drug and alcohol dependence.

[107]  K I Bolla,et al.  Cerebral Cortex Advance Access published May 13, 2004 Sex-related Differences in a Gambling Task and Its Neurological Correlates , 2022 .

[108]  H. D. Critchley,et al.  Social and motivational functioning is not critically dependent on feedback of autonomic responses: neuropsychological evidence from patients with pure autonomic failure , 2004, Neuropsychologia.

[109]  Gregory G. Brown,et al.  fMRI BOLD response to alcohol stimuli in alcohol dependent young women. , 2004, Addictive behaviors.

[110]  P. Renshaw,et al.  White matter hyperintensities in subjects with cocaine and opiate dependence and healthy comparison subjects , 2004, Psychiatry Research: Neuroimaging.

[111]  D. Tranel,et al.  The Effects of Vagus Nerve Stimulation on Decision-Making , 2004, Cortex.

[112]  Antoine Bechara,et al.  Risky Business: Emotion, Decision-Making, and Addiction , 2004, Journal of Gambling Studies.

[113]  Y. Shaham,et al.  Incubation of cocaine craving after withdrawal: a review of preclinical data , 2004, Neuropharmacology.

[114]  Jerome R Busemeyer,et al.  Cognitive modeling analysis of decision-making processes in cocaine abusers , 2004, Psychonomic bulletin & review.

[115]  C. Kilts,et al.  The neural correlates of cue-induced craving in cocaine-dependent women. , 2004, The American journal of psychiatry.

[116]  A. Simmons,et al.  Selective activation of the nucleus accumbens during risk-taking decision making , 2004, Neuroreport.

[117]  Nora D. Volkow,et al.  Severity of neuropsychological impairment in cocaine and alcohol addiction: association with metabolism in the prefrontal cortex , 2004, Neuropsychologia.

[118]  Nora D. Volkow,et al.  The addicted human brain viewed in the light of imaging studies: brain circuits and treatment strategies , 2004, Neuropharmacology.

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

[120]  E. Crone,et al.  Heart rate and skin conductance analysis of antecendents and consequences of decision making. , 2004, Psychophysiology.

[121]  Antonio Verdejo-García,et al.  Experience of emotions in substance abusers exposed to images containing neutral, positive, and negative affective stimuli. , 2005, Drug and alcohol dependence.

[122]  Jerome R Busemeyer,et al.  Psychological processes underlying risky decisions in drug abusers. , 2005, Psychology of addictive behaviors : journal of the Society of Psychologists in Addictive Behaviors.

[123]  Monique Ernst,et al.  Cognitive performance and autonomic reactivity in abstinent drug abusers and nonusers. , 2005, Experimental and clinical psychopharmacology.

[124]  M. Farah,et al.  Different underlying impairments in decision-making following ventromedial and dorsolateral frontal lobe damage in humans. , 2004, Cerebral cortex.

[125]  Khader M Hasan,et al.  Reduced Anterior Corpus Callosum White Matter Integrity is Related to Increased Impulsivity and Reduced Discriminability in Cocaine-Dependent Subjects: Diffusion Tensor Imaging , 2005, Neuropsychopharmacology.

[126]  P. C. Fletcher,et al.  Abnormal frontal activations related to decision-making in current and former amphetamine and opiate dependent individuals , 2005, Psychopharmacology.

[127]  Antonio Damasio,et al.  The somatic marker hypothesis: A neural theory of economic decision , 2005, Games Econ. Behav..

[128]  C. Le Moine,et al.  A Specific Limbic Circuit Underlies Opiate Withdrawal Memories , 2005, The Journal of Neuroscience.

[129]  R. Frances Correlation Between Dopamine D2 Receptors in the Ventral Striatum and Central Processing of Alcohol Cues and CravingHeinz A, Siessmeier T, Wrase J, et al (Campus Mitte, Berlin; Univ of Mainz, Germany; Univ of Hamburg, Germany) Am J Psychiatry 161:1783–1789, 2004§ , 2006 .