Behavioral / Systems / Cognitive Activation of Prefrontal Cortex by Transcranial Direct Current Stimulation Reduces Appetite for Risk during Ambiguous Decision Making

As adult humans, we are continuously faced with decisions in which proper weighing of the risk involved is critical. Excessively risky or overly cautious decision making can both have disastrous real-world consequences. Weighing of risks and benefits toward decision making involves a complex neural network that includes the dorsolateral prefrontal cortex (DLPFC), but its role remains unclear. Repetitive transcranial magnetic stimulation studies have shown that disruption of the DLPFC increases risk-taking behavior. Transcranial direct current stimulation (tDCS) allows upregulation of activity in the DLPFC, and we predicted that it might promote more cautious decision making. Healthy participants received one of the following treatments while they performed the Balloon Analog Risk Task: (1) right anodal/left cathodal DLPFC tDCS, (2) left anodal/ right cathodal DLPFC tDCS, or (3) sham tDCS. This experiment revealed that participants receiving either one of the bilateral DLPFC tDCS strategies adopted a risk-averse response style. In a control experiment, we tested whether unilateral DLPFC stimulation (anodal tDCS over the right or left DLPFC with the cathodal electrode over the contralateral supraorbital area) was sufficient to decrease risk-taking behaviors. This experiment showed no difference in decision-making behaviors between the groups of unilateral DLPFC stimulation and sham stimulation. These findings extend the notion that DLPFC activity is critical for adaptive decision making, possibly by suppressing riskier responses. Anodal tDCS over DLPFC by itself did not significantly change risk-taking behaviors; however, when the contralateral DLPFC was modulated with cathodal tCDS, an important decrease in risk taking was observed. Also, the induced cautious decision-making behavior was observed only when activity of both DLPFCs was modulated. The ability to modify risk-taking behavior may be translated into therapeutic interventions for disorders such as drug abuse, overeating, or pathological gambling.

[1]  H. Bang,et al.  Which psychosocial factors moderate or directly affect substance use among inner-city adolescents? , 2007, Addictive behaviors.

[2]  M. Nitsche,et al.  Shaping the effects of transcranial direct current stimulation of the human motor cortex. , 2007, Journal of neurophysiology.

[3]  Á. Pascual-Leone,et al.  One session of high frequency repetitive transcranial magnetic stimulation (rTMS) to the right prefrontal cortex transiently reduces cocaine craving. , 2007, Drug and alcohol dependence.

[4]  Alvaro Pascual-Leone,et al.  Effects of transcranial direct current stimulation on working memory in patients with Parkinson's disease , 2006, Journal of the Neurological Sciences.

[5]  D. Tranel,et al.  Visceral and decision-making functions of the ventromedial prefrontal cortex , 2006 .

[6]  Michael P. Milham,et al.  Distinct neural mechanisms of risk and ambiguity: A meta-analysis of decision-making , 2006, NeuroImage.

[7]  Lorena R. R. Gianotti,et al.  Disruption of Right Prefrontal Cortex by Low-Frequency Repetitive Transcranial Magnetic Stimulation Induces Risk-Taking Behavior , 2006, The Journal of Neuroscience.

[8]  U. Mosimann,et al.  Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex affects divided attention immediately after cessation of stimulation. , 2006, Journal of psychiatric research.

[9]  L. Cohen,et al.  Transcranial DC stimulation (tDCS): A tool for double-blind sham-controlled clinical studies in brain stimulation , 2006, Clinical Neurophysiology.

[10]  L. Leyman,et al.  The influence of rTMS over the left dorsolateral prefrontal cortex on Stroop task performance , 2006, Experimental Brain Research.

[11]  Hanna Damasio,et al.  Does gender play a role in functional asymmetry of ventromedial prefrontal cortex? , 2005, Brain : a journal of neurology.

[12]  R. Uher,et al.  Effect of Left Prefrontal Repetitive Transcranial Magnetic Stimulation on Food Craving , 2005, Biological Psychiatry.

[13]  Mascha van 't Wout,et al.  COGNITIVE NEUROSCIENCE AND NEUROPSYCHOLOGY NEUROREPORT Repetitive , 2005 .

[14]  Jordan Grafman,et al.  Recharging cognition with DC brain polarization , 2005, Trends in Cognitive Sciences.

[15]  M. Paulus,et al.  Neurobiology of Decision Making: A Selective Review from a Neurocognitive and Clinical Perspective , 2005, Biological Psychiatry.

[16]  Sergio P. Rigonatti,et al.  Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory , 2005, Experimental Brain Research.

[17]  Carlo Contoreggi,et al.  Risky decision making and the anterior cingulate cortex in abstinent drug abusers and nonusers. , 2005, Brain research. Cognitive brain research.

[18]  H. Damasio,et al.  The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers , 2005, Trends in Cognitive Sciences.

[19]  S. Sato,et al.  Safety and cognitive effect of frontal DC brain polarization in healthy individuals , 2005, Neurology.

[20]  Will M Aklin,et al.  Evaluation of behavioral measures of risk taking propensity with inner city adolescents. , 2005, Behaviour research and therapy.

[21]  C. Lejuez,et al.  Differences in risk-taking propensity across inner-city adolescent ever- and never-smokers. , 2005, Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco.

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

[23]  Rebecca Elliott,et al.  Role of the orbitofrontal cortex in reinforcement processing and inhibitory control: evidence from functional magnetic resonance imaging studies in healthy human subjects. , 2005, International review of neurobiology.

[24]  Jan Born,et al.  Bifrontal transcranial direct current stimulation slows reaction time in a working memory task , 2005, BMC Neuroscience.

[25]  Walter Paulus,et al.  Facilitation of probabilistic classification learning by transcranial direct current stimulation of the prefrontal cortex in the human , 2004, Neuropsychologia.

[26]  Stacey B. Daughters,et al.  Risk-taking propensity and risky sexual behavior of individuals in residential substance use treatment. , 2004, Addictive behaviors.

[27]  K. Hoffmann,et al.  Direct Current Stimulation over V5 Enhances Visuomotor Coordination by Improving Motion Perception in Humans , 2004, Journal of Cognitive Neuroscience.

[28]  J. Fiez,et al.  Prefrontal responses to drug cues: a neurocognitive analysis , 2004, Nature Neuroscience.

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

[30]  A. Pascual-Leone,et al.  Studies in Cognition: The Problems Solved and Created by Transcranial Magnetic Stimulation , 2003, Journal of Cognitive Neuroscience.

[31]  G. Hajak,et al.  High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking. , 2003, The Journal of clinical psychiatry.

[32]  Will M Aklin,et al.  Evaluation of the Balloon Analogue Risk Task (BART) as a predictor of adolescent real-world risk-taking behaviours. , 2003, Journal of adolescence.

[33]  Jonathan D. Cohen,et al.  The Neural Basis of Economic Decision-Making in the Ultimatum Game , 2003, Science.

[34]  Colin Camerer.  Strategizing in the Brain , 2003, Science.

[35]  G. Hajak,et al.  [Repetitiv Transcranial Magnetic Stimulation in Nicotine Dependence] , 2003, Psychiatrische Praxis.

[36]  G. Hajak,et al.  [Transcranial magnetic stimulation for nicotine dependence]. , 2003, Psychiatrische Praxis.

[37]  M. Nitsche,et al.  Facilitation of Implicit Motor Learning by Weak Transcranial Direct Current Stimulation of the Primary Motor Cortex in the Human , 2003, Journal of Cognitive Neuroscience.

[38]  A. Priori.  Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability , 2003, Clinical Neurophysiology.

[39]  Will M Aklin,et al.  The Balloon Analogue Risk Task (BART) differentiates smokers and nonsmokers. , 2003, Experimental and clinical psychopharmacology.

[40]  Walter Paulus,et al.  Modulation of cortical excitability by weak direct current stimulation--technical, safety and functional aspects. , 2003, Supplements to Clinical neurophysiology.

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

[42]  H. Barbas,et al.  Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey , 2002, Neuroscience.

[43]  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.

[44]  M. Nitsche,et al.  Pharmacological approach to the mechanisms of transcranial DC-stimulation-induced after-effects of human motor cortex excitability. , 2002, Brain : a journal of neurology.

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

[46]  T. Robbins,et al.  Decision-making processes following damage to the prefrontal cortex. , 2002, Brain : a journal of neurology.

[47]  Á. Pascual-Leone,et al.  Subthreshold low frequency repetitive transcranial magnetic stimulation selectively decreases facilitation in the motor cortex , 2002, Clinical Neurophysiology.

[48]  Gregory L. Stuart,et al.  Evaluation of a behavioral measure of risk taking: the Balloon Analogue Risk Task (BART). , 2002, Journal of experimental psychology. Applied.

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

[50]  M. Nitsche,et al.  Sustained excitability elevations induced by transcranial DC motor cortex stimulation in humans , 2001, Neurology.

[51]  R. Rafal,et al.  Virtual neurology , 2001, Nature Neuroscience.

[52]  Kip Smith,et al.  Neuronal substrates for choice under ambiguity, risk, gains, and losses , 2001, NeuroImage.

[53]  Gregory G. Brown,et al.  Prefrontal, Parietal, and Temporal Cortex Networks Underlie Decision-Making in the Presence of Uncertainty , 2001, NeuroImage.

[54]  J. Ridley.  Studies of Interference in Serial Verbal Reactions , 2001 .

[55]  M. Nitsche,et al.  Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation , 2000, The Journal of physiology.

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

[57]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

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

[59]  A. Damasio,et al.  Neurobiology of Decision-Making , 2012, Research and Perspectives in Neurosciences.

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

[61]  D. Purpura,et al.  INTRACELLULAR ACTIVITIES AND EVOKED POTENTIAL CHANGES DURING POLARIZATION OF MOTOR CORTEX. , 1965, Journal of neurophysiology.