Disrupted cortico‐limbic connectivity during reward processing in remitted bipolar I disorder

Bipolar disorder (BD) is associated with elevated reward sensitivity and persistent positive affect, yet the neural mechanisms underlying these patterns are not well understood. In the present study, we examined putative disruptions in communication within a well‐known cortico‐limbic reward circuit during reward processing as a potential contributing mechanism to these symptoms.

[1]  N. Anderson.  Likableness ratings of 555 personality-trait words. , 1968, Journal of personality and social psychology.

[2]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[3]  R. C. Young,et al.  A Rating Scale for Mania: Reliability, Validity and Sensitivity , 1978, British Journal of Psychiatry.

[4]  J. Fleiss,et al.  Intraclass correlations: uses in assessing rater reliability. , 1979, Psychological bulletin.

[5]  C. Carver,et al.  Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS Scales , 1994 .

[6]  S. Bressler.  Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[7]  A. Rush,et al.  The Inventory of Depressive Symptomatology (IDS): psychometric properties , 1996, Psychological Medicine.

[8]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[9]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[10]  M. Bauer,et al.  Impact of an easy-access VA clinic-based program for patients with bipolar disorder. , 1997, Psychiatric services.

[11]  S. Ikemoto,et al.  The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking , 1999, Brain Research Reviews.

[12]  Sheri L. Johnson,et al.  Exploring Behavioral Activation and Inhibition Sensitivities Among College Students at Risk for Bipolar Spectrum Symptomatology , 1999, Journal of psychopathology and behavioral assessment.

[13]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[14]  J. Fuster.  The Module Crisis of a Paradigm , 2000, Neuron.

[15]  D. Solomon,et al.  Increases in manic symptoms after life events involving goal attainment. , 2000, Journal of abnormal psychology.

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

[17]  S. Woods,et al.  The economic burden of bipolar disease. , 2000, The Journal of clinical psychiatry.

[18]  J. Giedd.  Bipolar disorder and attention-deficit/hyperactivity disorder in children and adolescents. , 2000, The Journal of clinical psychiatry.

[19]  Sheri L. Johnson,et al.  Responsiveness to Threat and Incentive in Bipolar Disorder: Relations of the BIS/BAS Scales with Symptoms , 2001, Journal of psychopathology and behavioral assessment.

[20]  E. Murray,et al.  The amygdala and reward , 2002, Nature Reviews Neuroscience.

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

[22]  R. Baldessarini,et al.  Suicidal Behaviour in Bipolar Disorder , 2003, CNS drugs.

[23]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[24]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[25]  Sheri L. Johnson,et al.  Cognitive, Behavioral, and Affective Responses to Reward: Links with Hypomanic Symptoms , 2005 .

[26]  Sheri L. Johnson.  Mania and dysregulation in goal pursuit: a review. , 2005, Clinical psychology review.

[27]  S. Haber,et al.  Reward-Related Cortical Inputs Define a Large Striatal Region in Primates That Interface with Associative Cortical Connections, Providing a Substrate for Incentive-Based Learning , 2006, The Journal of Neuroscience.

[28]  B. Balleine,et al.  Parallel incentive processing: an integrated view of amygdala function , 2006, Trends in Neurosciences.

[29]  R. Nusslock,et al.  Behavioral Approach System (BAS) Sensitivity and Bipolar Spectrum Disorders: A Retrospective and Concurrent Behavioral High-Risk Design , 2006 .

[30]  S. Ishii,et al.  Resolution of Uncertainty in Prefrontal Cortex , 2006, Neuron.

[31]  W. Drevets,et al.  Toward Constructing an Endophenotype Strategy for Bipolar Disorders , 2006, Biological Psychiatry.

[32]  M. Frank,et al.  Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. , 2006, Psychological review.

[33]  A. Nierenberg,et al.  Pharmacological Treatment Patterns at Study Entry for the First 500 STEP-BD Participants. , 2006, Psychiatric services.

[34]  B. Abler,et al.  Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fMRI study , 2007, Psychopharmacology.

[35]  H. Groenewegen,et al.  The Ventral Striatum as an Interface Between the Limbic and Motor Systems , 2007, CNS Spectrums.

[36]  E. Koechlin,et al.  Anterior Prefrontal Function and the Limits of Human Decision-Making , 2007, Science.

[37]  P. Thompson,et al.  Evidence for deficient modulation of amygdala response by prefrontal cortex in bipolar mania , 2008, Psychiatry Research: Neuroimaging.

[38]  R. Nusslock,et al.  Behavioral Approach System and Behavioral Inhibition System sensitivities and bipolar spectrum disorders: prospective prediction of bipolar mood episodes. , 2008, Bipolar disorders.

[39]  O. Monchi,et al.  Dopamine Depletion Impairs Frontostriatal Functional Connectivity during a Set-Shifting Task , 2008, The Journal of Neuroscience.

[40]  D. Kupfer,et al.  Elevated striatal and decreased dorsolateral prefrontal cortical activity in response to emotional stimuli in euthymic bipolar disorder: no associations with psychotropic medication load. , 2008, Bipolar disorders.

[41]  Brian Knutson,et al.  Neural Responses to Monetary Incentives in Major Depression , 2008, Biological Psychiatry.

[42]  S. Heckers,et al.  Abnormal Reward System Activation in Mania , 2008, Neuropsychopharmacology.

[43]  S. Nicola,et al.  Basolateral Amygdala Neurons Facilitate Reward-Seeking Behavior by Exciting Nucleus Accumbens Neurons , 2008, Neuron.

[44]  Timothy Edward John Behrens,et al.  How Green Is the Grass on the Other Side? Frontopolar Cortex and the Evidence in Favor of Alternative Courses of Action , 2009, Neuron.

[45]  Jeffrey L. Birk,et al.  Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. , 2009, The American journal of psychiatry.

[46]  J. Calabrese,et al.  The International Society for Bipolar Disorders (ISBD) Task Force report on the nomenclature of course and outcome in bipolar disorders. , 2009, Bipolar disorders.

[47]  L. Abramson,et al.  Longitudinal Predictors of Bipolar Spectrum Disorders: A Behavioral Approach System (BAS) Perspective. , 2009, Clinical psychology : a publication of the Division of Clinical Psychology of the American Psychological Association.

[48]  Jeffrey L. Birk,et al.  Reduced Caudate and Nucleus Accumbens Response to Rewards in Unmedicated Subjects with Major Depressive Disorder , 2009 .

[49]  Michael X. Cohen,et al.  Connectivity-based segregation of the human striatum predicts personality characteristics , 2009, Nature Neuroscience.

[50]  T. Meyer,et al.  Positive and Negative Affect in Individuals at High and Low Risk for Bipolar Disorders , 2009 .

[51]  M. Roth,et al.  Remission from mania is associated with a decrease in amygdala activation during motor response inhibition. , 2009, Bipolar disorders.

[52]  D. Kupfer,et al.  Elevated Amygdala Activity to Sad Facial Expressions: A State Marker of Bipolar but Not Unipolar Depression , 2010, Biological Psychiatry.

[53]  Jae-Jin Kim,et al.  Human orbitofrontal-striatum functional connectivity modulates behavioral persistence , 2010, Neuroreport.

[54]  Sheri L. Johnson,et al.  Pushing and Coasting in Dynamic Goal Pursuit , 2010, Psychological science.

[55]  L. Abramson,et al.  The Role of the Behavioral Approach System (BAS) in Bipolar Spectrum Disorders , 2010, Current directions in psychological science.

[56]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[57]  A. Heinz,et al.  Altered representation of expected value in the orbitofrontal cortex in mania , 2009, Human brain mapping.

[58]  J. Gruber.  A review and synthesis of positive emotion and reward disturbance in bipolar disorder. , 2011, Clinical psychology & psychotherapy.

[59]  Alice M Stamatakis,et al.  Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. , 2011, Nature.

[60]  M. Frank.  Computational models of motivated action selection in corticostriatal circuits , 2011, Current Opinion in Neurobiology.

[61]  J. Gruber.  Can Feeling Too Good Be Bad? , 2011 .

[62]  Timothy E. J. Behrens,et al.  Review Frontal Cortex and Reward-guided Learning and Decision-making Figure 1. Frontal Brain Regions in the Macaque Involved in Reward-guided Learning and Decision-making Finer Grained Anatomical Divisions with Frontal Cortical Systems for Reward-guided Behavior , 2022 .

[63]  S. Frangou,et al.  Frontopolar cortical inefficiency may underpin reward and working memory dysfunction in bipolar disorder , 2012, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[64]  D. A. Grant,et al.  High Behavioral Approach System (BAS) sensitivity, reward responsiveness, and goal-striving predict first onset of bipolar spectrum disorders: a prospective behavioral high-risk design. , 2012, Journal of abnormal psychology.

[65]  Michael D. Edge,et al.  The behavioral activation system and mania. , 2012, Annual review of clinical psychology.

[66]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[67]  Russell A. Poldrack,et al.  Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses , 2012, NeuroImage.

[68]  M. Rietschel,et al.  Increased medial orbitofrontal and amygdala activation: evidence for a systems-level endophenotype of bipolar I disorder. , 2012, The American journal of psychiatry.

[69]  J. Price,et al.  Neural circuits underlying the pathophysiology of mood disorders , 2012, Trends in Cognitive Sciences.

[70]  P. Falkai,et al.  Common and distinct neural correlates of emotional processing in Bipolar Disorder and Major Depressive Disorder: A voxel-based meta-analysis of functional magnetic resonance imaging studies , 2012, European Neuropsychopharmacology.

[71]  A. Arnsten,et al.  Neurobiological circuits regulating attention, cognitive control, motivation, and emotion: disruptions in neurodevelopmental psychiatric disorders. , 2012, Journal of the American Academy of Child and Adolescent Psychiatry.

[72]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[73]  M. Phillips,et al.  Waiting to win: elevated striatal and orbitofrontal cortical activity during reward anticipation in euthymic bipolar disorder adults , 2012, Bipolar disorders.

[74]  Michael D. Edge,et al.  People with bipolar I disorder report avoiding rewarding activities and dampening positive emotion. , 2013, Journal of affective disorders.

[75]  M. Phillips,et al.  Ventral Striatum Activity in Response to Reward: Differences Between Bipolar I and II Disorders , 2013, The American journal of psychiatry.

[76]  O. Sporns.  Structure and function of complex brain networks , 2013, Dialogues in clinical neuroscience.

[77]  K. Berridge,et al.  Prefrontal Cortex Modulates Desire and Dread Generated by Nucleus Accumbens Glutamate Disruption , 2013, Biological Psychiatry.

[78]  Keith Bush,et al.  A comparison of statistical methods for detecting context-modulated functional connectivity in fMRI , 2014, NeuroImage.

[79]  Kae Nakamura,et al.  Predictive Reward Signal of Dopamine Neurons , 2015 .

[80]  William A. Cunningham,et al.  Elevated striatal reactivity across monetary and social rewards in bipolar I disorder. , 2015, Journal of abnormal psychology.

[81]  Paul A. Taylor,et al.  FMRI Clustering in AFNI: False-Positive Rates Redux , 2017, Brain Connect..