Roles of the Different Sub-Regions of the Insular Cortex in Various Phases of the Decision-Making Process

This paper presents a coherent account of the role of the insular cortex (IC) in decision-making. We follow a conceptualization of decision-making that is very close to one previously proposed by Ernst and Paulus (2005): that the decision process is a progression of four phases: (1) re-focusing attention; (2) evaluation; (3) action; and (4) outcome processing, and we present evidence for the insula’s role in all these phases. We review the existing work on insula’s functional anatomy that subdivides the IC into posterior, dorsal anterior and ventral anterior regions. We re-map the results provided by the existing literature into these subdivisions wherever possible, to identify the components’ role in each decision making phase. In addition, we identify a self-regulating quality of the IC focused on harm avoidance.

[1]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.

[2]  B. Feige,et al.  The Role of Higher-Order Motor Areas in Voluntary Movement as Revealed by High-Resolution EEG and fMRI , 1999, NeuroImage.

[3]  D. Tranel,et al.  The insula: a critical neural substrate for craving and drug seeking under conflict and risk , 2014, Annals of the New York Academy of Sciences.

[4]  D. Yves von Cramon,et al.  Why am I unsure? Internal and external attributions of uncertainty dissociated by fMRI , 2004, NeuroImage.

[5]  A. Tversky,et al.  Prospect theory: an analysis of decision under risk — Source link , 2007 .

[6]  E. Rowland Theory of Games and Economic Behavior , 1946, Nature.

[7]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[8]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[9]  Charlene C. Wu,et al.  The Affective Impact of Financial Skewness on Neural Activity and Choice , 2011, PloS one.

[10]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

[11]  M. Brass,et al.  To Do or Not to Do: The Neural Signature of Self-Control , 2007, The Journal of Neuroscience.

[12]  S. Petersen,et al.  Role of the anterior insula in task-level control and focal attention , 2010, Brain Structure and Function.

[13]  T L Faber,et al.  Neural activity related to drug craving in cocaine addiction. , 2001, Archives of general psychiatry.

[14]  A. D. Craig,et al.  Once an island, now the focus of attention , 2010, Brain Structure and Function.

[15]  Karl J. Friston,et al.  Activation of reward circuitry in human opiate addicts , 1999, The European journal of neuroscience.

[16]  Yves Joanette,et al.  FUNCTION AND STRUCTURE , 1996 .

[17]  Antoine Bechara,et al.  The hidden island of addiction: the insula , 2009, Trends in Neurosciences.

[18]  Arnd Dörfler,et al.  Cerebral representation of the relief of itch by scratching. , 2009, Journal of neurophysiology.

[19]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

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

[21]  Camelia M. Kuhnen,et al.  The Neural Basis of Financial Risk Taking , 2005, Neuron.

[22]  András Jakab,et al.  Connectivity-based parcellation reveals interhemispheric differences in the insula , 2011, Brain Topography.

[23]  Arnaud D'Argembeau,et al.  The Iowa Gambling Task in fMRI images , 2009, Human brain mapping.

[24]  Maarten A. S. Boksem,et al.  A Potential Role of the Inferior Frontal Gyrus and Anterior Insula in Cognitive Control, Brain Rhythms, and Event-Related Potentials , 2011, Front. Psychology.

[25]  A. Bechara,et al.  A Neuropsychological Approach to Understanding Risk-Taking for Potential Gains and Losses , 2012, Frontiers in Neuroscience.

[26]  Hauke R. Heekeren,et al.  Neural foundations of risk–return trade-off in investment decisions , 2010, NeuroImage.

[27]  A. Schulze-Bonhage,et al.  Functional organization of the human anterior insular cortex , 2009, Neuroscience Letters.

[28]  E. Stein,et al.  Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. , 2000, The American journal of psychiatry.

[29]  Hugo D. Critchley,et al.  Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[30]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[31]  Brian Knutson,et al.  Anticipatory affect: neural correlates and consequences for choice , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[33]  Marcel Brass,et al.  When doing nothing is an option: The neural correlates of deciding whether to act or not , 2009, NeuroImage.

[34]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[35]  Matthew A. Lambon Ralph,et al.  The variation of function across the human insula mirrors its patterns of structural connectivity: Evidence from in vivo probabilistic tractography , 2012, NeuroImage.

[36]  Irwin P. Levin,et al.  The effects of insula damage on decision-making for risky gains and losses , 2009, Social neuroscience.

[37]  Charlene C. Wu,et al.  Toward an Affective Neuroscience Account of Financial Risk Taking , 2012, Front. Neurosci..

[38]  Norbert Kathmann,et al.  Neural correlates of error awareness , 2007, NeuroImage.

[39]  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.

[40]  Konstantin Voronin,et al.  Differential Brain Activity in Alcoholics and Social Drinkers to Alcohol Cues: Relationship to Craving , 2004, Neuropsychopharmacology.

[41]  K. R. Ridderinkhof,et al.  Function and Structure of the Right Inferior Frontal Cortex Predict Individual Differences in Response Inhibition: A Model-Based Approach , 2008, The Journal of Neuroscience.

[42]  Raymond J. Dolan,et al.  Deconstructing risk: Separable encoding of variance and skewness in the brain , 2011, NeuroImage.

[43]  E. Ravussin,et al.  Neuroimaging and Obesity , 2002, Annals of the New York Academy of Sciences.

[44]  Lawrence R. Frank,et al.  Anterior cingulate activity modulates nonlinear decision weight function of uncertain prospects , 2006, NeuroImage.

[45]  Gregory G. Brown,et al.  fMRI BOLD response to alcohol stimuli in alcohol dependent young women. , 2004, Addictive behaviors.

[46]  Matthew L. Ho,et al.  Brain metabolic changes during cigarette craving. , 2002, Archives of general psychiatry.

[47]  T. Robbins,et al.  Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making , 2008, Brain : a journal of neurology.

[48]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[49]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[50]  Antonio Damasio,et al.  The somatic marker hypothesis: A neural theory of economic decision , 2005, Games Econ. Behav..

[51]  P. Tobler,et al.  Reward skewness coding in the insula independent of probability and loss. , 2011, Journal of neurophysiology.

[52]  S. Quartz,et al.  Neural Differentiation of Expected Reward and Risk in Human Subcortical Structures , 2006, Neuron.

[53]  Bruce W. Smith,et al.  Neural Substrates of Reward Magnitude, Probability, and Risk during a Wheel of Fortune Decision-making Task Nih Public Access Cingulate Cortex in Decision-making , 2022 .

[54]  Marc A Schuckit,et al.  Decision making by methamphetamine-dependent subjects is associated with error-rate-independent decrease in prefrontal and parietal activation , 2003, Biological Psychiatry.

[55]  A. Tversky,et al.  Loss Aversion in Riskless Choice: A Reference-Dependent Model , 1991 .

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

[57]  Benjamin A. Parris,et al.  The role of the ventrolateral frontal cortex in inhibitory oculomotor control. , 2007, Brain : a journal of neurology.

[58]  Alain Dagher,et al.  Effects of Expectancy and Abstinence on the Neural Response to Smoking Cues in Cigarette Smokers: an fMRI Study , 2006, Neuropsychopharmacology.

[59]  Brian Knutson,et al.  Interpretable Classifiers for fMRI Improve Prediction of Purchases , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[60]  A. Morel,et al.  The human insula: Architectonic organization and postmortem MRI registration , 2013, Neuroscience.

[61]  Soeren Krach,et al.  Dissociation of neural networks for anticipation and consumption of monetary and social rewards , 2010, NeuroImage.

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

[63]  A. Craig,et al.  Emotional moments across time: a possible neural basis for time perception in the anterior insula , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[65]  Daniel Tranel,et al.  The Insula and Evaluative Processes , 2011, Psychological science.

[66]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[67]  A. Young Prospect Theory: An Analysis of Decision Under Risk (Kahneman and Tversky, 1979) , 2011 .

[68]  G. Loewenstein,et al.  Neural Predictors of Purchases , 2007, Neuron.

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

[70]  Adam R. Walczak,et al.  At the heart of the ventral attention system: The right anterior insula , 2009, Human brain mapping.

[71]  R. Passingham,et al.  Knowing When to Stop: The Brain Mechanisms of Chasing Losses , 2008, Biological Psychiatry.

[72]  G Elliott Wimmer,et al.  Nucleus accumbens activation mediates the influence of reward cues on financial risk taking , 2008, Neuroreport.

[73]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

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

[75]  Raymond J. Dolan,et al.  Anterior cingulate activity during error and autonomic response , 2005, NeuroImage.

[76]  Michael Forsting,et al.  There are differences in cerebral activation between females in distinct menstrual phases during viewing of erotic stimuli: a fMRI study , 2006, Experimental Brain Research.

[77]  H. C Lau,et al.  Willed action and attention to the selection of action , 2004, NeuroImage.

[78]  A. Bechara,et al.  PSYCHOLOGICAL SCIENCE Research Article Neural Correlates of Adaptive Decision Making for Risky Gains and Losses , 2022 .

[79]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[80]  H. Garavan Insula and drug cravings , 2010, Brain Structure and Function.

[81]  Cong Huang,et al.  Neural Correlates of Post-error Slowing during a Stop Signal Task: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[82]  K. R. Ridderinkhof,et al.  Error Awareness and Salience Processing in the Oddball Task: Shared Neural Mechanisms , 2012, Front. Hum. Neurosci..

[83]  M. Brass,et al.  Intentional inhibition: How the “veto‐area” exerts control , 2009, Human brain mapping.

[84]  G. Jackson,et al.  Neural correlates of the emergence of consciousness of thirst , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[85]  A. Craig The sentient self , 2010, Brain Structure and Function.

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

[87]  V. Menon,et al.  A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks , 2008, Proceedings of the National Academy of Sciences.

[88]  Wolfgang Prinz,et al.  The role of the preSMA and the rostral cingulate zone in internally selected actions , 2007, NeuroImage.

[89]  Holger Wiese,et al.  Prefrontal cortex activity in self-initiated movements is condition-specific, but not movement-related , 2005, NeuroImage.

[90]  C. Kilts,et al.  The neural correlates of cue-induced craving in cocaine-dependent women. , 2004, The American journal of psychiatry.

[91]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[92]  Mark S. Cohen,et al.  Neural Substrates of Resisting Craving During Cigarette Cue Exposure , 2007, Biological Psychiatry.

[93]  K. R. Ridderinkhof,et al.  Conscious perception of errors and its relation to the anterior insula , 2010, Brain Structure and Function.

[94]  Irwin P. Levin,et al.  The impact of prior risk experiences on subsequent risky decision-making: The role of the insula , 2010, NeuroImage.

[95]  M. Brass,et al.  The hidden side of intentional action: the role of the anterior insular cortex , 2010, Brain Structure and Function.

[96]  A. Craig,et al.  Pain, temperature, and the sense of the body , 1996 .

[97]  Paul M. Cinciripini,et al.  Neural substrates of smoking cue reactivity: A meta-analysis of fMRI studies , 2012, NeuroImage.

[98]  Thilo Van Eimeren,et al.  Implementation of visuospatial cues in response selection , 2006, NeuroImage.

[99]  A. Bechara,et al.  The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making , 2010, Brain Structure and Function.

[100]  P. Reber,et al.  Neural correlates of sexual arousal in homosexual and heterosexual men. , 2007, Behavioral neuroscience.

[101]  Fernando Zelaya,et al.  Distinct roles of prefrontal cortical subregions in the Iowa Gambling Task. , 2009, Cerebral cortex.

[102]  Kewei Chen,et al.  Neuroimaging and obesity: mapping the brain responses to hunger and satiation in humans using positron emission tomography. , 2002, Annals of the New York Academy of Sciences.

[103]  G. Pagnoni,et al.  The neural correlates of the affective response to unreciprocated cooperation , 2008, Neuropsychologia.

[104]  B. King-Casas,et al.  The neurobiology of social decision-making , 2008, Current Opinion in Neurobiology.

[105]  P. Lang,et al.  International Affective Picture System (IAPS): Instruction Manual and Affective Ratings (Tech. Rep. No. A-4) , 1999 .

[106]  L. F. Barrett,et al.  From affect to control: Functional specialization of the insula in motivation and regulation , 2017, bioRxiv.

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

[108]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

[109]  E. Ravussin,et al.  Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[110]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.