Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism

Decision making and risk taking are interrelated processes that are important for daily functioning. The somatic marker hypothesis has provided a conceptual basis for processes involved in risk-taking decision making and has been used to link discrete neural substrates to risk-related behaviors. This investigation examined the hypothesis that the degree of risk-taking is related to the degree of activation in the insular cortex. Seventeen healthy, right-handed subjects performed a risk-taking decision-making task during functional magnetic resonance imaging (fMRI) using a fast event-related design. This investigation yielded three main findings. First, right insula (BA 13) activation was significantly stronger when subjects selected a "risky" response versus selecting a "safe" response. Second, the degree of insula activation was related to the probability of selecting a "safe" response following a punished response. Third, the degree of insula activation was related to the subjects' degree of harm avoidance and neuroticism as measured by the TCI and NEO personality questionnaires, respectively. These results are consistent with the hypothesis that insula activation serves as a critical neural substrate to instantiate aversive somatic markers that guide risk-taking decision-making behavior.

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

[2]  P. Costa,et al.  Normal Personality Assessment in Clinical Practice: The NEO Personality Inventory. , 1992 .

[3]  R. Dolan,et al.  A Functional Anatomy of Anticipatory Anxiety , 1999, NeuroImage.

[4]  P. Montague,et al.  Activity in human ventral striatum locked to errors of reward prediction , 2002, Nature Neuroscience.

[5]  N. Iwata,et al.  Low novelty‐seeking differentiates obsessive‐compulsive disorder from major depression , 2000, Acta psychiatrica Scandinavica.

[6]  C. Cepko,et al.  The External Granule Layer of the Developing Chick Cerebellum Generates Granule Cells and Cells of the Isthmus and Rostral Hindbrain , 2001, The Journal of Neuroscience.

[7]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[8]  K. Davis,et al.  The neural circuitry of pain as explored with functional MRI , 2000, Neurological research.

[9]  F Hentges,et al.  5-HT2a receptor polymorphism gene in bipolar disorder and harm avoidance personality trait. , 2000, American journal of medical genetics.

[10]  Michael Davis,et al.  Cortical Afferents to the Extended Amygdala , 1999, Annals of the New York Academy of Sciences.

[11]  P. Matthews,et al.  Exacerbation of Pain by Anxiety Is Associated with Activity in a Hippocampal Network , 2001, The Journal of Neuroscience.

[12]  M B Keller,et al.  Personality traits in subjects with bipolar I disorder in remission. , 1996, Journal of affective disorders.

[13]  Dragan M. Svrakic,et al.  The Tridimensional Personality Questionnaire: U.S. Normative Data , 1991, Psychological reports.

[14]  G. Glover,et al.  Error‐related brain activation during a Go/NoGo response inhibition task , 2001, Human brain mapping.

[15]  M. Eysenck,et al.  Biased cognitive operations in anxiety: artefact, processing priorities or attentional search? , 1991, Behaviour research and therapy.

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

[17]  F Brambilla,et al.  Neuroendocrine correlates of temperamental traits in humans , 2000, Psychoneuroendocrinology.

[18]  C. Robert Cloninger A systematic method for clinical description and classification of personality variants. A proposal. , 1987, Archives of general psychiatry.

[19]  Kenneth S Kendler,et al.  The etiology of phobias: an evaluation of the stress-diathesis model. , 2002, Archives of general psychiatry.

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

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

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

[23]  J. Frank Yates,et al.  The risk construct. , 1992 .

[24]  T. Canli,et al.  Neuroimaging of emotion and personality: Scientific evidence and ethical considerations , 2002, Brain and Cognition.

[25]  J. Desmond,et al.  An fMRI study of personality influences on brain reactivity to emotional stimuli. , 2001, Behavioral neuroscience.

[26]  Ferruccio Fazio,et al.  In Vivo Serotonin 5HT2A Receptor Binding and Personality Traits in Healthy Subjects: A Positron Emission Tomography Study , 2002, NeuroImage.

[27]  V. Starcevic,et al.  Personality dimensions in panic disorder and generalized anxiety disorder. , 1996, Journal of affective disorders.

[28]  David Borsook,et al.  Noxious hot and cold stimulation produce common patterns of brain activation in humans: a functional magnetic resonance imaging study , 2000, Neuroscience Letters.

[29]  Cloninger Cr A systematic method for clinical description and classification of personality variants: A proposal. , 1987 .

[30]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[31]  E. Weber,et al.  A Theory of Perceived Risk and Attractiveness , 1992 .

[32]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

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

[34]  M. Honda,et al.  Expectation of Pain Enhances Responses to Nonpainful Somatosensory Stimulation in the Anterior Cingulate Cortex and Parietal Operculum/Posterior Insula: an Event-Related Functional Magnetic Resonance Imaging Study , 2000, The Journal of Neuroscience.

[35]  H. Breiter,et al.  Human brain activation under controlled thermal stimulation and habituation to noxious heat: An fMRI study , 1999, Magnetic resonance in medicine.

[36]  M. J. Norušis,et al.  SPSS base system user's guide , 1990 .

[37]  M C Neale,et al.  A longitudinal twin study of personality and major depression in women. , 1993, Archives of general psychiatry.

[38]  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.

[39]  A. Bechara,et al.  Neurobiology of decision-making: risk and reward. , 2001, Seminars in clinical neuropsychiatry.

[40]  R. Elliott,et al.  Activation of Different Anterior Cingulate Foci in Association with Hypothesis Testing and Response Selection , 1998, NeuroImage.

[41]  J. Yates Risk-taking behavior , 1992 .

[42]  T. Robbins,et al.  Decision making and neuropsychiatry , 2001, Trends in Cognitive Sciences.

[43]  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.

[44]  Christopher K. Hsee,et al.  Cross-National Differences in Risk Preference and Lay Predictions , 1999 .

[45]  K. Merikangas,et al.  Are personality traits familial risk factors for substance use disorders? Results of a controlled family study. , 2002, The American journal of psychiatry.

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

[47]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[48]  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.

[49]  H. Critchley,et al.  Fear Conditioning in Humans The Influence of Awareness and Autonomic Arousal on Functional Neuroanatomy , 2002, Neuron.

[50]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

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

[52]  J Blangero,et al.  Anxiety proneness linked to epistatic loci in genome scan of human personality traits. , 1998, American journal of medical genetics.

[53]  Paul Glimcher,et al.  Decisions, Decisions, Decisions Choosing a Biological Science of Choice , 2002, Neuron.

[54]  P. Costa,et al.  Stability and change in personality assessment: the revised NEO Personality Inventory in the year 2000. , 1997, Journal of personality assessment.

[55]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[56]  M. First,et al.  The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. , 1992, Archives of general psychiatry.

[57]  M. Berk,et al.  Relationship between serotonin and the Temperament and Character Inventory , 1999, Psychiatry Research.

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

[59]  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.

[60]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[61]  Elke U. Weber,et al.  Do Risk Attitudes Reflect in the Eye of the Beholder? , 2019, Choice, Decision, and Measurement: Essays in Honor of R. Duncan Luce.

[62]  P. Slovic Perception of risk. , 1987, Science.

[63]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  Barbara A. Mellers,et al.  Representations of Risk Judgments , 1994 .

[65]  Karl J. Friston,et al.  Amygdala–Hippocampal Involvement in Human Aversive Trace Conditioning Revealed through Event-Related Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[66]  F Fazio,et al.  In vivo serotonin 5HT(2A) receptor binding and personality traits in healthy subjects: a positron emission tomography study. , 2002, NeuroImage.