The Role of the Amygdala in Signaling Prospective Outcome of Choice

Can brain activity reveal a covert choice? Making a choice often evokes distinct emotions that accompany decision processes. Amygdala has been implicated in choice behavior that is guided by a prospective negative outcome. However, its specific involvement in emotional versus cognitive processing of choice behavior has been a subject of controversy. In this study, the human amygdala was monitored by functional magnetic resonance imaging (fMRI) while subjects were playing in a naturalistic choice paradigm against the experimenter. In order to win, players had to occasionally choose to bluff their opponent, risk "getting caught," and suffer a loss. A critical period, when choice has been made but outcome was still unknown, activated the amygdala preferentially following the choice that entailed risk of loss. Thus, the response of the amygdala differentiated between subject's covert choice of either playing fair or foul. These results support a role of the amygdala in choice behavior, both in the appraisal of inherent value of choice and the signaling of prospective negative outcomes.

[1]  Joseph E LeDoux,et al.  Why We Think Plasticity Underlying Pavlovian Fear Conditioning Occurs in the Basolateral Amygdala , 1999, Neuron.

[2]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[3]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[4]  Joseph E LeDoux,et al.  Fear Conditioning Enhances Different Temporal Components of Tone-Evoked Spike Trains in Auditory Cortex and Lateral Amygdala , 1997, Neuron.

[5]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[6]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[7]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[8]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

[9]  Joseph E LeDoux.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1996 .

[10]  W. Singer,et al.  Activation of Heschl’s Gyrus during Auditory Hallucinations , 1999, Neuron.

[11]  Joseph E LeDoux,et al.  Human Amygdala Activation during Conditioned Fear Acquisition and Extinction: a Mixed-Trial fMRI Study , 1998, Neuron.

[12]  E. Murray,et al.  Control of Response Selection by Reinforcer Value Requires Interaction of Amygdala and Orbital Prefrontal Cortex , 2000, The Journal of Neuroscience.

[13]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[14]  M Meunier,et al.  Effects of aspiration versus neurotoxic lesions of the amygdala on emotional responses in monkeys , 1999, The European journal of neuroscience.

[15]  S. Paradiso.  The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[16]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[17]  Karl J. Friston,et al.  Brain Systems Mediating Aversive Conditioning: an Event-Related fMRI Study , 1998, Neuron.

[18]  P C Bucy,et al.  Preliminary analysis of functions of the temporal lobes in monkeys. 1939. , 1997, The Journal of neuropsychiatry and clinical neurosciences.

[19]  M. Shadlen,et al.  Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque , 1999, Neuron.

[20]  A. Tversky,et al.  Prospect theory: analysis of decision under risk , 1979 .

[21]  Robert Sugden,et al.  Preference Reversal: Information-Processing Effect or Rational Non-transitive Choice? , 1989 .

[22]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

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

[24]  L. Squire,et al.  Independence of memory functions and emotional behavior: Separate contributions of the hippocampal formation and the amygdala , 1991, Hippocampus.

[25]  Karl J. Friston,et al.  Brain systems mediating aversive conditioning: An event related fMRI study , 1998, NeuroImage.

[26]  Joseph E LeDoux,et al.  Impaired fear conditioning following unilateral temporal lobectomy in humans , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  T. Hendler,et al.  Feeling or Features Different Sensitivity to Emotion in High-Order Visual Cortex and Amygdala , 2001, Neuron.

[28]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[29]  J. Gore,et al.  Activation of the left amygdala to a cognitive representation of fear , 2001, Nature Neuroscience.

[30]  W. Singer,et al.  The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery , 1998, The European journal of neuroscience.

[31]  A R Damasio,et al.  Descartes' error and the future of human life. , 1994, Scientific American.

[32]  Brian Knutson,et al.  FMRI Visualization of Brain Activity during a Monetary Incentive Delay Task , 2000, NeuroImage.

[33]  I. Ritov,et al.  Emotion-based choice , 1999 .

[34]  M. Abdellaoui.  Rational Choice under Uncertainty , 2004 .

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

[36]  Joseph E LeDoux.  Fear and the brain: where have we been, and where are we going? , 1998, Biological Psychiatry.

[37]  G. Schoenbaum,et al.  Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning , 1998, Nature Neuroscience.

[38]  R. Sugden,et al.  Regret Theory: An alternative theory of rational choice under uncertainty Review of Economic Studies , 1982 .

[39]  E A Stein,et al.  Functional MRI of human Pavlovian fear conditioning: patterns of activation as a function of learning. , 1999, Neuroreport.

[40]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[41]  M. Posner.  The Brain and Emotion , 1999, Nature Medicine.

[42]  A. Tversky,et al.  Prospect Theory : An Analysis of Decision under Risk Author ( s ) : , 2007 .

[43]  E. Murray,et al.  Excitotoxic Lesions of the Amygdala Fail to Produce Impairment in Visual Learning for Auditory Secondary Reinforcement But Interfere with Reinforcer Devaluation Effects in Rhesus Monkeys , 1997, The Journal of Neuroscience.

[44]  Joseph E LeDoux.  The emotional brain , 1996 .

[45]  R. Dolan,et al.  A subcortical pathway to the right amygdala mediating "unseen" fear. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  A. Sirigu,et al.  Differential amygdala responses to winning and losing: a functional magnetic resonance imaging study in humans , 2000, The European journal of neuroscience.

[47]  Wolfgang Grodd,et al.  Functional MRI reveals left amygdala activation during emotion , 1997, Psychiatry Research: Neuroimaging.

[48]  I. Ritov,et al.  Decision Affect Theory: Emotional Reactions to the Outcomes of Risky Options , 1997 .

[49]  R. Adolphs,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans , 1995, Science.

[50]  R. J. Dolan,et al.  Differential neural response to positive and negative feedback in planning and guessing tasks , 1997, Neuropsychologia.

[51]  T. Robbins,et al.  Different types of fear-conditioned behaviour mediated by separate nuclei within amygdala , 1997, Nature.

[52]  B T Hyman,et al.  Neuropsychological correlates of bilateral amygdala damage. , 1990, Archives of neurology.

[53]  Robert Sugden,et al.  Disappointment and Dynamic Consistency in Choice under Uncertainty , 1986 .

[54]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  P. Holland,et al.  Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforcer Devaluation Effects , 1996, The Journal of Neuroscience.

[56]  D. Paré,et al.  Neuronal Correlates of Fear in the Lateral Amygdala: Multiple Extracellular Recordings in Conscious Cats , 2000, The Journal of Neuroscience.

[57]  Wolfgang Grodd,et al.  Functional Imaging of Conditioned Aversive Emotional Responses in Antisocial Personality Disorder , 2000, Neuropsychobiology.

[58]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

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