Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions.

On a gambling task that models real-life decisions, patients with bilateral lesions of the ventromedial prefrontal cortex (VM) opt for choices that yield high immediate gains in spite of higher future losses. In this study, we addressed three possibilities that may account for this behaviour: (i) hypersensitivity to reward; (ii) insensitivity to punishment; and (iii) insensitivity to future consequences, such that behaviour is always guided by immediate prospects. For this purpose, we designed a variant of the original gambling task in which the advantageous decks yielded high immediate punishment but even higher future reward. The disadvantageous decks yielded low immediate punishment but even lower future reward. We measured the skin conductance responses (SCRs) of subjects after they had received a reward or punishment. Patients with VM lesions opted for the disadvantageous decks in both the original and variant versions of the gambling task. The SCRs of VM lesion patients after they had received a reward or punishment were not significantly different from those of controls. In a second experiment, we investigated whether increasing the delayed punishment in the disadvantageous decks of the original task or decreasing the delayed reward in the disadvantageous decks of the variant task would shift the behaviour of VM lesion patients towards an advantageous strategy. Both manipulations failed to shift the behaviour of VM lesion patients away from the disadvantageous decks. These results suggest that patients with VM lesions are insensitive to future consequences, positive or negative, and are primarily guided by immediate prospects. This 'myopia for the future' in VM lesion patients persists in the face of severe adverse consequences, i.e. rising future punishment or declining future reward.

[1]  J. M. Warren,et al.  THE FRONTAL GRANULAR CORTEX AND BEHAVIOR , 1964 .

[2]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[3]  G. W. Crane HERE AND NOW , 1978, CAL [magazine] Certified Akers Laboratories.

[4]  J. Fuster Prefrontal Cortex , 2018 .

[5]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[6]  A. Damasio,et al.  Severe disturbance of higher cognition after bilateral frontal lobe ablation , 1985, Neurology.

[7]  G. W. Hoesen,et al.  Neural Systems of the Non‐human Primate Forebrain Implicated in Memory a , 1985 .

[8]  J. Newman,et al.  Passive avoidance in syndromes of disinhibition: psychopathy and extraversion. , 1985, Journal of personality and social psychology.

[9]  A. Damasio,et al.  Lesion analysis in neuropsychology , 1989 .

[10]  A. Damasio,et al.  Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli , 1990, Behavioural Brain Research.

[11]  Adèle,et al.  The Development and Neural Bases of Higher Cognitive Functions. A conference. May 20-24, 1989, Philadelphia, Pa. , 1990, Annals of the New York Academy of Sciences.

[12]  J. Fuster,et al.  Prefrontal Cortex and the Bridging of Temporal Gaps in the Perception‐Action Cycle , 1990, Annals of the New York Academy of Sciences.

[13]  A. Raine,et al.  Reward dominance and passive avoidance learning in adolescent psychopaths , 1990, Journal of abnormal child psychology.

[14]  A. Diamond The development and neural bases of higher cognitive functions. Introduction. , 1990, Annals of the New York Academy of Sciences.

[15]  H. Damasio,et al.  Wisconsin Card Sorting Test performance as a measure of frontal lobe damage. , 1991, Journal of clinical and experimental neuropsychology.

[16]  M. Orrell,et al.  Dementia of frontal lobe type , 1991, Psychological Medicine.

[17]  Laurie A. Miller,et al.  Impulsivity, risk-taking, and the ability to synthesize fragmented information after frontal lobectomy , 1992, Neuropsychologia.

[18]  R. J. Frank,et al.  Three-dimensional in vivo mapping of brain lesions in humans. , 1992, Archives of neurology.

[19]  D. Kosson,et al.  Delay of gratification in psychopathic and nonpsychopathic offenders. , 1992, Journal of abnormal psychology.

[20]  Donald T. Stuss,et al.  Biological and psychological development of executive functions , 1992, Brain and Cognition.

[21]  Stevens S. Smith,et al.  Autonomic responsivity during passive avoidance in incarcerated psychopaths , 1993 .

[22]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[23]  John Monahan,et al.  Violence and mental disorder: Developments in risk assessment. , 1994 .

[24]  E. Barratt Impulsiveness and aggression. , 1994 .

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

[26]  A. Damasio Descartes' error: emotion, reason, and the human brain. avon books , 1994 .

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

[28]  H. Damasio Human Brain Anatomy in Computerized Images , 1995 .

[29]  W. Yule,et al.  Personality and antisocial behavior in children and adolescents: An enquiry into Eysenck's and Gray's theories , 1995, Journal of abnormal child psychology.

[30]  Terri Gullickson Human Brain Anatomy in Computerized Images. , 1995 .

[31]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[33]  A. Damasio,et al.  Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. , 1996, Cerebral cortex.

[34]  T. Robbins,et al.  Dissociation in prefrontal cortex of affective and attentional shifts , 1996, Nature.

[35]  K. Plaisted,et al.  Dementia of frontal lobe type-living in the here and now , 1997 .

[36]  T. Robbins,et al.  Dissociable Forms of Inhibitory Control within Prefrontal Cortex with an Analog of the Wisconsin Card Sort Test: Restriction to Novel Situations and Independence from “On-Line” Processing , 1997, The Journal of Neuroscience.

[37]  J. Fuster The Prefrontal Cortex , 1997 .

[38]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

[39]  E. Rolls The Brain and Emotion , 2000 .

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

[41]  G. Chiara,et al.  Drug Addiction as a Disorder of Associative Learning: Role of Nucleus Accumbens Shell/Extended Amygdala Dopamine , 1999, Annals of the New York Academy of Sciences.

[42]  Hanna Damasio,et al.  Impairment of social and moral behavior related to early damage in human prefrontal cortex , 1999, Nature Neuroscience.

[43]  T. Robbins,et al.  Comparative Cognitive Neuropsychological Studies of Frontal Lobe Function: Implications for Therapeutic Strategies in Frontal Variant Frontotemporal Dementia , 1999, Dementia and Geriatric Cognitive Disorders.

[44]  J. Evenden Impulsivity: a discussion of clinical and experimental findings , 1999, Journal of psychopharmacology.

[45]  T. Robbins,et al.  Specific cognitive deficits in mild frontal variant frontotemporal dementia. , 1999, Brain : a journal of neurology.

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

[47]  A. Leshner,et al.  Drugs of abuse and the brain. , 1999, Proceedings of the Association of American Physicians.

[48]  J. Newman,et al.  Testing Damasio's somatic marker hypothesis with psychopathic individuals: risk takers or risk averse? , 1999, Journal of abnormal psychology.

[49]  J. C. Anderson,et al.  Dendritic asymmetry cannot account for directional responses of neurons in visual cortex , 1999, Nature Neuroscience.

[50]  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.

[51]  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.

[52]  Gregory P. Lee,et al.  Different Contributions of the Human Amygdala and Ventromedial Prefrontal Cortex to Decision-Making , 1999, The Journal of Neuroscience.

[53]  A. Raine,et al.  Reduced prefrontal gray matter volume and reduced autonomic activity in antisocial personality disorder. , 2000, Archives of general psychiatry.

[54]  R. Spinks The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe, 3rd ed. , 2000 .

[55]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

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

[57]  Antonio R. Damasio,et al.  A Neural Basis for Sociopathy , 2000 .

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

[59]  D. Tranel,et al.  Acquired Personality Disturbances Associated With Bilateral Damage to the Ventromedial Prefrontal Region , 2000, Developmental neuropsychology.