Increased error-related brain activity in generalized anxiety disorder

The error-related negativity (ERN) is a negative deflection approximately 50ms following an erroneous response, and is thought to reflect activity of the anterior cingulate cortex (ACC), a region of the medial prefrontal cortex implicated in the pathophysiology of a number of affective disorders, including generalized anxiety disorder (GAD). Pathological worry, the hallmark of GAD, has been linked to increased error-related brain activity, although no studies to date have examined the ERN among a clinical GAD sample. The present study measured electrocortical indices of error monitoring in a well-characterized, medication-free GAD sample. Brain activity was recorded in 17 GAD and 24 control subjects. The GAD group was characterized by a larger ERN and an increased difference between error and correct trials; a larger ERN was associated with increased self-reported anxiety and depression symptoms. Individuals with GAD have exaggerated early neural responses to errors, consistent with fMRI work implicating ACC abnormalities in GAD.

[1]  E. Foa,et al.  Increased error-related brain activity in pediatric obsessive-compulsive disorder before and after treatment. , 2008, The American journal of psychiatry.

[2]  Evaluation-related frontocentral negativity evoked by correct responses and errors , 2007, Behavioural Brain Research.

[3]  Avram J Holmes,et al.  Spatiotemporal dynamics of error processing dysfunctions in major depressive disorder. , 2008, Archives of general psychiatry.

[4]  Hans-Ulrich Wittchen,et al.  Generalized anxiety disorder: prevalence, burden, and cost to society , 2002, Depression and anxiety.

[5]  G. Band,et al.  Age effects on response monitoring in a mental-rotation task , 2000, Biological Psychology.

[6]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[7]  S. Segalowitz,et al.  Error detection in patients with lesions to the medial prefrontal cortex: an ERP study , 2004, Neuropsychologia.

[8]  A. Beck,et al.  Physiological hyperarousal: construct validity of a central aspect of the tripartite model of depression and anxiety , 1999 .

[9]  Clay B. Holroyd,et al.  Error-related scalp potentials elicited by hand and foot movements: evidence for an output-independent error-processing system in humans , 1998, Neuroscience Letters.

[10]  Lorna C. Quandt,et al.  Error detection and posterror behavior in depressed undergraduates. , 2008, Emotion.

[11]  B. Burle,et al.  Error negativity on correct trials: a reexamination of available data , 2003, Biological Psychology.

[12]  W. Hulstijn,et al.  Effects of antipsychotic and antidepressant drugs on action monitoring in healthy volunteers , 2006, Brain Research.

[13]  W. Gehring,et al.  Action-Monitoring Dysfunction in Obsessive-Compulsive Disorder , 2000, Psychological science.

[14]  Jutta Joormann,et al.  Worry, Procrastination, and Perfectionism: Differentiating Amount of Worry, Pathological Worry, Anxiety, and Depression , 2001, Cognitive Therapy and Research.

[15]  Doreen M. Olvet,et al.  Depression symptom severity and error-related brain activity , 2010, Psychiatry Research.

[16]  J. Ford Schizophrenia: the broken P300 and beyond. , 1999, Psychophysiology.

[17]  M. Keller,et al.  Results of a naturalistic longitudinal study of benzodiazepine and SSRI use in the treatment of generalized anxiety disorder and social phobia , 2005, Depression and anxiety.

[18]  J. Ormel,et al.  Common Mental Disorders and Disability Across Cultures: Results From the WHO Collaborative Study on Psychological Problems in General Health Care , 1994 .

[19]  C. Bell DSM-IV: Diagnostic and Statistical Manual of Mental Disorders , 1994 .

[20]  Cameron S. Carter,et al.  Overactive Action Monitoring in Obsessive-Compulsive Disorder , 2003, Psychological science.

[21]  Lee Anna Clark,et al.  The anxiety and depressive disorders: Descriptive psychopathology and differential diagnosis. , 1989 .

[22]  Wouter Hulstijn,et al.  Action monitoring in major depressive disorder with psychomotor retardation , 2008, Cortex.

[23]  D. Tucker,et al.  Frontolimbic response to negative feedback in clinical depression. , 2003, Journal of abnormal psychology.

[24]  K. R. Ridderinkhof,et al.  To P(E) or not to P(E): a P3-like ERP component reflecting the processing of response errors. , 2009, Psychophysiology.

[25]  Cynthia L. Turk,et al.  Distinct and Overlapping Features of Rumination and Worry: The Relationship of Cognitive Production to Negative Affective States , 2002, Cognitive Therapy and Research.

[26]  P. Kendall,et al.  Generalized Anxiety Disorder , 2012 .

[27]  C. Carter,et al.  The anterior cingulate as a conflict monitor: fMRI and ERP studies , 2002, Physiology & Behavior.

[28]  F. Ferri,et al.  Neural correlates of worry in generalized anxiety disorder and in normal controls: a functional MRI study , 2009, Psychological Medicine.

[29]  M. Whisman,et al.  Neuroticism as a common feature of the depressive and anxiety disorders: a test of the revised integrative hierarchical model in a national sample. , 2006, Journal of abnormal psychology.

[30]  Maarten A. S. Boksem,et al.  Error-related ERP components and individual differences in punishment and reward sensitivity , 2006, Brain Research.

[31]  Greg Hajcak,et al.  The stability of error-related brain activity with increasing trials. , 2009, Psychophysiology.

[32]  Robert Roman,et al.  Intracerebral Error-Related Negativity in a Simple Go/NoGo Task , 2005 .

[33]  R A McCormick,et al.  Testing a tripartite model: I. Evaluating the convergent and discriminant validity of anxiety and depression symptom scales. , 1995, Journal of abnormal psychology.

[34]  M. Coles,et al.  Performance monitoring in a confusing world: error-related brain activity, judgments of response accuracy, and types of errors. , 2000, Journal of experimental psychology. Human perception and performance.

[35]  Andrew C Heath,et al.  Heritability of frontal brain function related to action monitoring. , 2008, Psychophysiology.

[36]  Tom Johnstone,et al.  Anticipatory activation in the amygdala and anterior cingulate in generalized anxiety disorder and prediction of treatment response. , 2009, The American journal of psychiatry.

[37]  V. B. Brooks,et al.  ‘Error’ potentials in limbic cortex (anterior cingulate area 24) of monkeys during motor learning , 1986, Neuroscience Letters.

[38]  Richard J. Davidson,et al.  A Functional Magnetic Resonance Imaging Predictor of Treatment Response to Venlafaxine in Generalized Anxiety Disorder , 2008, Biological Psychiatry.

[39]  N. Fox,et al.  A History of Childhood Behavioral Inhibition and Enhanced Response Monitoring in Adolescence Are Linked to Clinical Anxiety , 2009, Biological Psychiatry.

[40]  G. Hajcak,et al.  Distinct electrocortical and behavioral evidence for increased attention to threat in generalized anxiety disorder , 2010, Depression and anxiety.

[41]  Christian Kaufmann,et al.  Overactive error-related brain activity as a candidate endophenotype for obsessive-compulsive disorder: evidence from unaffected first-degree relatives. , 2011, The American journal of psychiatry.

[42]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[43]  D. Tucker,et al.  Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation , 2004, Clinical Neurophysiology.

[44]  W. Ray,et al.  Startle response in Generalized Anxiety Disorder , 2009, Depression and anxiety.

[45]  Judith M Ford,et al.  Response-monitoring dysfunction in aging and Alzheimer’s disease: an event-related potential study , 2003, Neurobiology of Aging.

[46]  P. Kendall,et al.  Anxiety and depression : distinctive and overlapping features , 1989 .

[47]  T. Endrass,et al.  Performance monitoring and error significance in patients with obsessive-compulsive disorder , 2010, Biological Psychology.

[48]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[49]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[50]  W. Gehring,et al.  Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder , 2005, Biological Psychiatry.

[51]  D. Meyer,et al.  A Neural System for Error Detection and Compensation , 1993 .

[52]  B. Burle,et al.  Executive control and response expectancy: a Laplacian ERP study. , 2011, Psychophysiology.

[53]  Murray B. Stein,et al.  Anterior cingulate activation in high trait anxious subjects is related to altered error processing during decision making , 2004, Biological Psychiatry.

[54]  Katherine E. Prater,et al.  Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. , 2010, The American journal of psychiatry.

[55]  Monique Ernst,et al.  Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. , 2007, Archives of general psychiatry.

[56]  D. Tucker,et al.  Regulating action: alternating activation of midline frontal and motor cortical networks , 2001, Clinical Neurophysiology.

[57]  W. Gehring,et al.  Chronic medication does not affect hyperactive error responses in obsessive-compulsive disorder. , 2010, Psychophysiology.

[58]  Yael Arbel,et al.  Parsing the componential structure of post-error ERPs: a principal component analysis of ERPs following errors. , 2009, Psychophysiology.

[59]  Amit Etkin,et al.  Functional neuroanatomy of anxiety: a neural circuit perspective. , 2010, Current topics in behavioral neurosciences.

[60]  Anna Weinberg,et al.  Electrocortical evidence for vigilance-avoidance in Generalized Anxiety Disorder. , 2011, Psychophysiology.

[61]  Joshua W. Brown,et al.  Performance Monitoring by the Anterior Cingulate Cortex During Saccade Countermanding , 2003, Science.

[62]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[63]  Markus Kiefer,et al.  Error processing in major depressive disorder: evidence from event-related potentials. , 2006, Journal of psychiatric research.

[64]  Jonathan D. Cohen,et al.  Resting anterior cingulate activity and abnormal responses to errors in subjects with elevated depressive symptoms: A 128‐channel EEG study , 2006, Human brain mapping.

[65]  D. Tucker,et al.  Electrophysiological Responses to Errors and Feedback in the Process of Action Regulation , 2003, Psychological science.

[66]  W. Hulstijn,et al.  Action monitoring and depressive symptom reduction in major depressive disorder. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[67]  Thérèse J. M. Overbeek,et al.  Dissociable Components of Error Processing on the Functional Significance of the Pe Vis-à-vis the Ern/ne Performance Monitoring Processes Reflected in the Ne and Pe Review of Studies That Report Both Ne and Pe: Associations and Dissociations Pharmacological Effects , 2022 .

[68]  Pearl H Chiu,et al.  Neural evidence for enhanced error detection in major depressive disorder. , 2007, The American journal of psychiatry.

[69]  Robert F. Simons,et al.  Anxiety and error-related brain activity , 2003, Biological Psychology.

[70]  T. Ollendick,et al.  Phobic and Anxiety Disorders in Children and Adolescents , 2004 .

[71]  B. Wetering,et al.  Error-processing deficits in patients with cocaine dependence , 2007, Biological Psychology.

[72]  Structural relationships among dimensions of the DSM-IV anxiety and mood disorders and dimensions of negative affect, positive affect, and autonomic arousal. , 1998 .

[73]  N. Yeung,et al.  On the ERN and the significance of errors. , 2005, Psychophysiology.

[74]  M. Freeston,et al.  Problem solving and problem orientation in generalized anxiety disorder. , 1998, Journal of anxiety disorders.

[75]  F. Vidal,et al.  Is the ‘error negativity’ specific to errors? , 2000, Biological Psychology.

[76]  G. Hajcak,et al.  The error-related negativity (ERN) and psychopathology: toward an endophenotype. , 2008, Clinical psychology review.

[77]  Charles H. Hillman,et al.  Age and physical activity influences on action monitoring during task switching , 2006, Neurobiology of Aging.

[78]  T. Endrass,et al.  Overactive performance monitoring in obsessive-compulsive disorder: ERP evidence from correct and erroneous reactions , 2008, Neuropsychologia.

[79]  R. Dahl,et al.  Attentional Control Moderates Relations Between Negative Affect and Neural Correlates of Action Monitoring in Adolescence , 2010, Developmental neuropsychology.

[80]  M. Kiefer,et al.  Error-Related Brain Activity in Patients with Obsessive- Compulsive Disorder and in Healthy Controls , 2005 .

[81]  Karin Mogg,et al.  Attentional Bias in Generalized Anxiety Disorder Versus Depressive Disorder , 2005, Cognitive Therapy and Research.

[82]  R. Simons,et al.  Error-related brain activity in obsessive–compulsive undergraduates , 2002, Psychiatry Research.

[83]  R. Dahl,et al.  Increased error-related negativity (ERN) in childhood anxiety disorders: ERP and source localization. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[84]  J. Peuskens,et al.  Action monitoring and perfectionism in anorexia nervosa , 2007, Brain and Cognition.

[85]  M. Coles,et al.  "Where did I go wrong?" A psychophysiological analysis of error detection. , 1995, Journal of experimental psychology. Human perception and performance.

[86]  Michael Falkenstein,et al.  Short-term mobilization of processing resources is revealed in the event-related potential. , 2003, Psychophysiology.

[87]  P. Apkarian,et al.  Motoric response inhibition in finger movement and saccadic eye movement: a comparative study , 1999, Clinical Neurophysiology.

[88]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

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

[90]  T. Endrass,et al.  Error Awareness in a Saccade Countermanding Task , 2005 .

[91]  D. Watson Rethinking the mood and anxiety disorders: a quantitative hierarchical model for DSM-V. , 2005, Journal of abnormal psychology.

[92]  Timothy A. Brown,et al.  Generalized Anxiety Disorder , 2015 .

[93]  Sarah L. Master,et al.  Neurocognitive components of the behavioral inhibition and activation systems: implications for theories of self-regulation. , 2007, Psychophysiology.

[94]  R. Simons,et al.  Error-related psychophysiology and negative affect , 2004, Brain and Cognition.

[95]  Clay B. Holroyd,et al.  Implementation of error-processing in the human anterior cingulate cortex: a source analysis of the magnetic equivalent of the error-related negativity , 2003, Biological Psychology.

[96]  D. Tucker,et al.  Mood, personality, and self-monitoring: negative affect and emotionality in relation to frontal lobe mechanisms of error monitoring. , 2000, Journal of experimental psychology. General.

[97]  R. Simons,et al.  The effects of fear on performance monitoring and attentional allocation. , 2005, Psychophysiology.

[98]  J. Hohnsbein,et al.  ERP components on reaction errors and their functional significance: a tutorial , 2000, Biological Psychology.

[99]  Karen J. Mathewson,et al.  Brain bases of error-related ERPs as influenced by age and task , 2005, Biological Psychology.

[100]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[101]  Markus Kiefer,et al.  The effect of erroneous responses on response monitoring in patients with major depressive disorder: a study with event-related potentials. , 2004, Psychophysiology.

[102]  R. Simons,et al.  To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. , 2003, Psychophysiology.

[103]  D. Dietrich,et al.  Discrepant target detection and action monitoring in obsessive–compulsive disorder , 2001, Psychiatry Research: Neuroimaging.

[104]  R. Knight,et al.  Prefrontal–cingulate interactions in action monitoring , 2000, Nature Neuroscience.

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

[106]  R. Simons,et al.  The way of our errors: theme and variations. , 2010, Psychophysiology.

[107]  G. Hajcak,et al.  Errors Are Aversive , 2008, Psychological science.

[108]  Eun Young Kim,et al.  Error-Related Negativity in Children: Effect of an Observer , 2005, Developmental neuropsychology.

[109]  Borís Burle,et al.  Error Negativity Does Not Reflect Conflict: A Reappraisal of Conflict Monitoring and Anterior Cingulate Cortex Activity , 2008, Journal of Cognitive Neuroscience.

[110]  S. Luck An Introduction to the Event-Related Potential Technique , 2005 .

[111]  J. Ford,et al.  Anatomy of an error: ERP and fMRI , 2003, Biological Psychology.