Deficient Goal-Directed Control in a Population Characterized by Extreme Goal Pursuit

AbstractComputational neuroscience has contributed to understanding compulsive behavior by distinguishing habitual from goal-directed choice through model-free and model-based learning. Yet, questions remain about applying this approach to psychiatric conditions that are characterized by complex behaviors that occur outside the laboratory. Here, we compared individuals with anorexia nervosa (AN), whose self-starvation appears both excessively goal-directed and habitual, with healthy controls (HC) to assess: 1) whether their behavior is characterized by enhanced or diminished model-based behavior, 2) the domain specificity of any abnormalities by comparing learning in a food-specific context as well as in a monetary context, and 3) whether impairments are secondary to starvation by comparing learning before and after initial treatment. Across all conditions, individuals with AN showed an impairment in model-based, but not model-free, learning, suggesting a general and persistent contribution of habitual over goal-directed control, across domains and timepoints.

[1]  C. Mazure,et al.  The Yale-Brown-Cornell Eating Disorder Scale: development, use, reliability and validity. , 1994, Journal of psychiatric research.

[2]  Petra Himmel,et al.  Stevens Handbook Of Experimental Psychology Learning Motivation And Emotion , 2016 .

[3]  Noah A. Shamosh,et al.  Individual Differences in Delay Discounting , 2008, Psychological science.

[4]  Christina L. Boisseau,et al.  Comparison of the Association Between Goal-Directed Planning and Self-reported Compulsivity vs Obsessive-Compulsive Disorder Diagnosis , 2019, JAMA psychiatry.

[5]  G. Frank,et al.  Association of Elevated Reward Prediction Error Response With Weight Gain in Adolescent Anorexia Nervosa. , 2017, The American journal of psychiatry.

[6]  Wouter Kool,et al.  Incentives Boost Model-Based Control Across a Range of Severity on Several Psychiatric Constructs , 2019, Biological Psychiatry.

[7]  J. Hagman,et al.  Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. , 2013, The American journal of psychiatry.

[8]  N. Daw,et al.  Dopamine selectively remediates 'model-based' reward learning: a computational approach. , 2016, Brain : a journal of neurology.

[9]  W. Goodman,et al.  The Yale-Brown Obsessive Compulsive Scale. II. Validity. , 1989, Archives of general psychiatry.

[10]  Karolina M. Lempert,et al.  Temporal discounting across three psychiatric disorders: Anorexia nervosa, obsessive compulsive disorder, and social anxiety disorder , 2017, Depression and anxiety.

[11]  B. Balleine,et al.  Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning , 2006, Behavioural Brain Research.

[12]  Amir Dezfouli,et al.  Speed/Accuracy Trade-Off between the Habitual and the Goal-Directed Processes , 2011, PLoS Comput. Biol..

[13]  Daphna Shohamy,et al.  Dopamine Modulation of Intertemporal Decision-making: Evidence from Parkinson Disease , 2016, Journal of Cognitive Neuroscience.

[14]  B. Balleine,et al.  Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning , 2004, The European journal of neuroscience.

[15]  R. Kessler,et al.  The Prevalence and Correlates of Eating Disorders in the National Comorbidity Survey Replication , 2007, Biological Psychiatry.

[16]  C. Fairburn,et al.  Assessment of eating disorders: interview or self-report questionnaire? , 1994, The International journal of eating disorders.

[17]  T. Robbins,et al.  Functional neuroimaging of avoidance habits in obsessive-compulsive disorder. , 2015, The American journal of psychiatry.

[18]  N. Daw,et al.  Characterizing a psychiatric symptom dimension related to deficits in goal-directed control , 2016, eLife.

[19]  H. Bruch.  The golden cage , 1978 .

[20]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[21]  S. Tiffany,et al.  A cognitive model of drug urges and drug-use behavior: role of automatic and nonautomatic processes. , 1990, Psychological review.

[22]  S. Fields.  The Golden Cage: The Enigma of Anorexia Nervosa , 1978 .

[23]  Catherine A. Hartley,et al.  From Creatures of Habit to Goal-Directed Learners , 2016, Psychological science.

[24]  W. T. Maddox,et al.  Altered implicit category learning in anorexia nervosa. , 2012, Neuropsychology.

[25]  W. James,et al.  The Principles of Psychology. , 1983 .

[26]  Evelyn Attia,et al.  Dietary energy density and diet variety as predictors of outcome in anorexia nervosa. , 2008, The American journal of clinical nutrition.

[27]  Nathaniel D. Daw,et al.  Cognitive Control Predicts Use of Model-based Reinforcement Learning , 2014, Journal of Cognitive Neuroscience.

[28]  P. Salkovskis,et al.  Obsessional-compulsive problems: a cognitive-behavioural analysis. , 1985, Behaviour research and therapy.

[29]  E. Walker,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[30]  P. Dayan,et al.  Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control , 2005, Nature Neuroscience.

[31]  N. Daw,et al.  Reduced model-based decision-making in gambling disorder , 2019, Scientific Reports.

[32]  B. Balleine,et al.  Blockade of NMDA receptors in the dorsomedial striatum prevents action–outcome learning in instrumental conditioning , 2005, The European journal of neuroscience.

[33]  Lindsay E. Hunter,et al.  A common deliberative process underlies model-based planning and patient intertemporal choice , 2018 .

[34]  Michael Moutoussis,et al.  Improving the reliability of model-based decision-making estimates in the two-stage decision task with reaction-times and drift-diffusion modeling , 2019, PLoS Comput. Biol..

[35]  Shinsuke Shimojo,et al.  Neural Computations Underlying Arbitration between Model-Based and Model-free Learning , 2013, Neuron.

[36]  Raymond J. Dolan,et al.  Disentangling the Roles of Approach, Activation and Valence in Instrumental and Pavlovian Responding , 2011, PLoS Comput. Biol..

[37]  N. Daw,et al.  Model-based learning protects against forming habits , 2015, Cognitive, Affective, & Behavioral Neuroscience.

[38]  Alice Y. Chiang,et al.  Working-memory capacity protects model-based learning from stress , 2013, Proceedings of the National Academy of Sciences.

[39]  P. Dayan,et al.  Model-based influences on humans’ choices and striatal prediction errors , 2011, Neuron.

[40]  C. Gillan,et al.  Does cognitive-behavioral therapy affect goal-directed planning in obsessive-compulsive disorder? , 2019, Psychiatry Research.

[41]  福田 博一.  State-Trait Anxiety Inventoryによるペインクリニック外来患者の不安の評価 , 1994 .

[42]  Kendra R. Becker,et al.  Cognitive rigidity and heightened attention to detail occur transdiagnostically in adolescents with eating disorders , 2019, Eating disorders.

[43]  T. Robbins,et al.  Goal-directed learning and obsessive–compulsive disorder , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[44]  Rebecca Shingleton,et al.  Eating behavior in anorexia nervosa: before and after treatment. , 2012, The International journal of eating disorders.

[45]  T. Robbins,et al.  Impaired visual discrimination learning in anorexia nervosa , 2003, Appetite.

[46]  U. Schmidt,et al.  Perfectionism in Anorexia Nervosa: Novel Performance Based Evidence , 2014, PloS one.

[47]  C. Spielberger.  State‐Trait Anxiety Inventory , 2010 .

[48]  A. Reber.  Implicit learning and tacit knowledge , 1993 .

[49]  B. Walsh,et al.  The enigmatic persistence of anorexia nervosa. , 2013, The American journal of psychiatry.

[50]  S. Killcross,et al.  Coordination of actions and habits in the medial prefrontal cortex of rats. , 2003, Cerebral cortex.

[51]  Alan Edelman,et al.  Julia: A Fast Dynamic Language for Technical Computing , 2012, ArXiv.

[52]  C. Fairburn.  Cognitive Behavior Therapy and Eating Disorders , 2008 .

[53]  R. Sysko,et al.  Eating behavior among women with anorexia nervosa. , 2005, The American journal of clinical nutrition.

[54]  B. Balleine,et al.  A specific role for posterior dorsolateral striatum in human habit learning , 2009, The European journal of neuroscience.

[55]  D. Shohamy,et al.  Neural Mechanisms Supporting Maladaptive Food Choices in Anorexia Nervosa , 2015, Nature Neuroscience.

[56]  M. Frank,et al.  Computational psychiatry as a bridge from neuroscience to clinical applications , 2016, Nature Neuroscience.

[57]  Michael R. Meager,et al.  Hippocampal Contributions to Model-Based Planning and Spatial Memory , 2019, Neuron.

[58]  A. Graybiel.  Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[59]  H. Spencer.  The Principles of Psychology - Vol. I , 2016 .

[60]  Jeffrey N. Rouder,et al.  Some do and some don’t? Accounting for variability of individual difference structures , 2018, Psychonomic Bulletin & Review.

[61]  P. Dayan,et al.  Disorders of compulsivity: a common bias towards learning habits , 2014, Molecular Psychiatry.

[62]  B. Walsh,et al.  Dietary energy density and diet variety as risk factors for relapse in anorexia nervosa: a replication. , 2012, The International journal of eating disorders.

[63]  A. Markman,et al.  The Curse of Planning: Dissecting Multiple Reinforcement-Learning Systems by Taxing the Central Executive , 2013 .

[64]  B. Balleine,et al.  Habits, action sequences and reinforcement learning , 2012, The European journal of neuroscience.

[65]  Sang Wan Lee,et al.  Neurostimulation Reveals Context-Dependent Arbitration Between Model-Based and Model-Free Reinforcement Learning. , 2019, Cerebral cortex.

[66]  G. Arbanas.  Diagnostic and Statistical Manual of Mental Disorders (DSM-5) , 2015 .

[67]  E. Weber,et al.  Increased Capacity to Delay Reward in Anorexia Nervosa , 2012, Journal of the International Neuropsychological Society.

[68]  S. Killcross,et al.  Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats , 2003, Behavioural Brain Research.

[69]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[70]  B. Balleine,et al.  The Role of Learning in the Operation of Motivational Systems , 2002 .

[71]  Vivian V. Valentin,et al.  Determining the Neural Substrates of Goal-Directed Learning in the Human Brain , 2007, The Journal of Neuroscience.

[72]  K. Foerde,et al.  Decreased feedback learning in anorexia nervosa persists after weight restoration , 2017, The International journal of eating disorders.

[73]  P. Dayan,et al.  States versus Rewards: Dissociable Neural Prediction Error Signals Underlying Model-Based and Model-Free Reinforcement Learning , 2010, Neuron.

[74]  U. Schmidt,et al.  A reward-centred model of anorexia nervosa: A focussed narrative review of the neurological and psychophysiological literature , 2015, Neuroscience & Biobehavioral Reviews.

[75]  N. Volkow,et al.  Addiction: Decreased reward sensitivity and increased expectation sensitivity conspire to overwhelm the brain's control circuit , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[76]  R. Sysko,et al.  Test–retest reliability of the proposed DSM-5 eating disorder diagnostic criteria , 2012, Psychiatry Research.

[77]  D. Bates,et al.  Parsimonious Mixed Models , 2015, 1506.04967.

[78]  Bernd Figner,et al.  On Weight and Waiting: Delay Discounting in Anorexia Nervosa Pretreatment and Posttreatment , 2015, Biological Psychiatry.

[79]  Jiazhou Chen,et al.  Improving the Reliability of Computational Analyses: Model-Based Planning and Its Relationship With Compulsivity. , 2020, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[80]  T. Robbins,et al.  Drug Addiction: Updating Actions to Habits to Compulsions Ten Years On. , 2016, Annual review of psychology.

[81]  Claire M. Gillan,et al.  The role of habit in compulsivity , 2016, European Neuropsychopharmacology.