Neural Substrates of Reward Magnitude, Probability, and Risk during a Wheel of Fortune Decision-making Task Nih Public Access Cingulate Cortex in Decision-making

Economic decision-making involves the weighting of magnitude and probability of potential gains/losses. While previous work has examined the neural systems involved in decision-making, there is a need to understand how the parameters associated with decision-making (e.g., magnitude of expected reward, probability of expected reward and risk) modulate activation within these neural systems. In the current fMRI study, we modified the monetary wheel of fortune (WOF) task [Ernst, M., Nelson, E.E., McClure, E.B., Monk, C.S., Munson, S., Eshel, N., et al. (2004). Choice selection and reward anticipation: an fMRI study. Neuropsychologia 42(12), 1585-1597.] to examine in 25 healthy young adults the neural responses to selections of different reward magnitudes, probabilities, or risks. Selection of high, relative to low, reward magnitude increased activity in insula, amygdala, middle and posterior cingulate cortex, and basal ganglia. Selection of low-probability, as opposed to high-probability reward, increased activity in anterior cingulate cortex, as did selection of risky, relative to safe reward. In summary, decision-making that did not involve conflict, as in the magnitude contrast, recruited structures known to support the coding of reward values, and those that integrate motivational and perceptual information for behavioral responses. In contrast, decision-making under conflict, as in the probability and risk contrasts, engaged the dorsal anterior cingulate cortex whose role in conflict monitoring is well established. However, decision-making under conflict failed to activate the structures that track reward values per se. Thus, the presence of conflict in decision-making seemed to significantly alter the pattern of neural responses to simple rewards. In addition, this paradigm further clarifies the functional specialization of the cingulate cortex in processes of decision-making.

[1]  K. Doya,et al.  Current trends in decision making. , 2007, Annals of the New York Academy of Sciences.

[2]  E. Koechlin,et al.  Dissociating the role of the medial and lateral anterior prefrontal cortex in human planning. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Bruce W. Smith,et al.  The impact of affect and frequency on lexical decision: The role of the amygdala and inferior frontal cortex , 2006, NeuroImage.

[4]  E. Rolls,et al.  Cerebral Cortex Advance Access published June 22, 2007 Expected Value, Reward Outcome, and Temporal Difference Error Representations in a Probabilistic Decision Task , 2022 .

[5]  N. Ramnani,et al.  Distinct portions of anterior cingulate cortex and medial prefrontal cortex are activated by reward processing in separable phases of decision-making cognition , 2004, Biological Psychiatry.

[6]  Brian Knutson,et al.  Neural Antecedents of Financial Decisions , 2007, The Journal of Neuroscience.

[7]  M. Platt,et al.  Risk-sensitive neurons in macaque posterior cingulate cortex , 2005, Nature Neuroscience.

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

[9]  Brian Knutson,et al.  Amygdalar Recruitment during Anticipation of Monetary Rewards , 2003, Annals of the New York Academy of Sciences.

[10]  M. Ernst,et al.  Neural substrates of choice selection in adults and adolescents: Development of the ventrolateral prefrontal and anterior cingulate cortices , 2007, Neuropsychologia.

[11]  Brian Knutson,et al.  A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI , 2003, NeuroImage.

[12]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

[13]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[14]  Jeffrey C. Cooper,et al.  Functional magnetic resonance imaging of reward prediction , 2005, Current opinion in neurology.

[15]  D. Kahneman,et al.  Functional Imaging of Neural Responses to Expectancy and Experience of Monetary Gains and Losses tasks with monetary payoffs , 2001 .

[16]  A. Craig.  How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

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

[18]  P. Glimcher,et al.  The neural correlates of subjective value during intertemporal choice , 2007, Nature Neuroscience.

[19]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[20]  C. Ranganath,et al.  Behavioral and neural predictors of upcoming decisions , 2005, Cognitive, affective & behavioral neuroscience.

[21]  D. Yves von Cramon,et al.  Frontomedian activation depends on both feedback validity and valence: fMRI evidence for contextual feedback evaluation , 2005, NeuroImage.

[22]  Christopher Andrew,et al.  Differential neural responses to overt and covert presentations of facial expressions of fear and disgust , 2000, NeuroImage.

[24]  B. Vogt.  Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[25]  D. LeBihan,et al.  Modulation of Parietal Activation by Semantic Distance in a Number Comparison Task , 2001, NeuroImage.

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

[27]  J. Morton,et al.  Choosing the Lesser of Two Evils, the Better of Two Goods: Specifying the Roles of Ventromedial Prefrontal Cortex and Dorsal Anterior Cingulate in Object Choice , 2006, The Journal of Neuroscience.

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

[29]  E. Rolls.  The functions of the orbitofrontal cortex , 1999, Brain and Cognition.

[30]  R. Elliott,et al.  Differential Response Patterns in the Striatum and Orbitofrontal Cortex to Financial Reward in Humans: A Parametric Functional Magnetic Resonance Imaging Study , 2003, The Journal of Neuroscience.

[31]  R. Elliott,et al.  Ventromedial prefrontal cortex mediates guessing , 1999, Neuropsychologia.

[32]  Evan M. Gordon,et al.  Neural Signatures of Economic Preferences for Risk and Ambiguity , 2006, Neuron.

[33]  S. Quartz,et al.  Human Insula Activation Reflects Risk Prediction Errors As Well As Risk , 2008, The Journal of Neuroscience.

[34]  J. Parkinson,et al.  Dissociable Contributions of the Human Amygdala and Orbitofrontal Cortex to Incentive Motivation and Goal Selection , 2003, The Journal of Neuroscience.

[35]  J. Gläscher,et al.  Dissociable Systems for Gain- and Loss-Related Value Predictions and Errors of Prediction in the Human Brain , 2006, The Journal of Neuroscience.

[36]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[37]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[38]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[39]  D. Yves von Cramon,et al.  Predicting events of varying probability: uncertainty investigated by fMRI , 2003, NeuroImage.

[40]  M. Roesch,et al.  Orbitofrontal Cortex, Associative Learning, and Expectancies , 2005, Neuron.

[41]  H. Critchley,et al.  Influence of sympathetic autonomic arousal on cortical arousal: implications for a therapeutic behavioural intervention in epilepsy , 2004, Epilepsy Research.

[42]  Jobu Watanabe,et al.  Context-dependent cortical activation in response to financial reward and penalty: an event-related fMRI study , 2003, NeuroImage.

[43]  M. Buonocore,et al.  Posterior cingulate cortex activation by emotional words: fMRI evidence from a valence decision task , 2003, Human brain mapping.

[44]  K. Berman,et al.  Cerebral Cortex doi:10.1093/cercor/bhj004 Neural Coding of Distinct Statistical Properties of Reward Information in Humans , 2005 .

[45]  S. Dehaene,et al.  Understanding dissociations in dyscalculia: a brain imaging study of the impact of number size on the cerebral networks for exact and approximate calculation. , 2000, Brain : a journal of neurology.

[46]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

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

[48]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[49]  Henrik Walter,et al.  Prediction error as a linear function of reward probability is coded in human nucleus accumbens , 2006, NeuroImage.

[50]  C. Carter,et al.  Anterior cingulate cortex and conflict detection: An update of theory and data , 2007, Cognitive, affective & behavioral neuroscience.

[51]  Michael X. Cohen,et al.  Functional connectivity with anterior cingulate and orbitofrontal cortices during decision-making. , 2005, Brain research. Cognitive brain research.

[52]  M. First,et al.  Structured clinical interview for DSM-IV axis II personality disorders : SCID-II , 1997 .

[53]  R. James R. Blair,et al.  The role of the amygdala and rostral anterior cingulate in encoding expected outcomes during learning , 2006, NeuroImage.

[54]  Cameron S. Carter,et al.  Separating semantic conflict and response conflict in the Stroop task: A functional MRI study , 2005, NeuroImage.

[55]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

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

[57]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  Sandra Jazbec,et al.  Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents , 2005, NeuroImage.

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

[60]  F. Castellanos,et al.  A Functional Magnetic Resonance Imaging Investigation of Uncertainty in Adolescents with Anxiety Disorders , 2008, Biological Psychiatry.

[61]  R. James R. Blair,et al.  Response options and expectations of reward in decision-making: The differential roles of dorsal and rostral anterior cingulate cortex , 2007, NeuroImage.

[62]  Corianne Rogalsky,et al.  Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism , 2003, NeuroImage.

[63]  M. Paulus.  Neurobiology of decision-making: quo vadis? , 2005, Brain research. Cognitive brain research.

[64]  A. D. Craig,et al.  Human feelings: why are some more aware than others? , 2004, Trends in Cognitive Sciences.

[65]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.