The error-related negativity for error processing in interoception

&NA; The error‐related negativity (ERN) is an event‐related potential in the electroencephalogram (EEG) observed within the first 100 ms after commission of an error. Increased ERN amplitudes have been observed in several psychological disorders characterized by high negative affect. While the ERN has extensively been studied in tasks using exteroceptive stimuli, its relation to interoceptive stimuli is unknown. Since errors related to interoception might be particularly relevant for survival and negative affect, this study aimed to explore the ERN for errors related to interoceptive, respiratory sensations (intERN). Moreover, we compared the intERN with a commonly observed ERN related to exteroceptive, visual stimuli (extERN) and examined their associations with interoception‐related negative affect. We studied the ERN using a respiratory occlusion task (intERN) and a visual flanker task (extERN) in 40 healthy volunteers during continuous 129 channel EEG recordings. In the occlusion task, participants received inspiratory occlusions of two different durations and indicated whether each occlusion was short or long. In the Flanker task, participants indicated the direction of arrowheads. Interoception‐related negative affect was assessed with the Anxiety Sensitivity Index. Comparable with the extERN, the intERN was observed at fronto‐central scalp positions after error commission in the occlusion task, but it peaked significantly earlier than the extERN. Mean amplitudes of the intERN and extERN showed no significant difference and were not correlated. Moreover, higher levels of anxiety sensitivity were correlated with significantly greater amplitudes of the intERN, but with lower amplitudes of the extERN. The present results firstly demonstrate an error‐related negativity EEG‐potential that is related to interoceptive sensations (intERN). This intERN is not associated with a commonly observed ERN elicited by exteroceptive stimuli and is distinctly linked to higher levels of interoception‐related negative affect. The intERN might be a promising neural marker for future studies on interoception, negative affect and error processing. HighlightsAn error‐related negativity (ERN) potential for interoceptive sensations is presentedThe interoceptive respiratory ERN is not associated with an exteroceptive visual ERNThe interoceptive ERN is linked to higher levels of anxiety sensitivityThe exteroceptive ERN is related to lower levels of anxiety sensitivity

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

[2]  Norbert Kathmann,et al.  Age Effects on Adjustments of Performance Monitoring to Task Difficulty , 2012 .

[3]  Michael Falkenstein,et al.  Independent component analysis of erroneous and correct responses suggests online response control , 2010, Human brain mapping.

[4]  M. Posner,et al.  Localization of a Neural System for Error Detection and Compensation , 1994 .

[5]  Greg H. Proudfit,et al.  In an uncertain world, errors are more aversive: evidence from the error-related negativity. , 2015, Emotion.

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

[7]  P. Davenport,et al.  Respiratory-related cortical potentials evoked by inspiratory occlusion in humans. , 1986, Journal of applied physiology.

[8]  Gilles Pourtois,et al.  Unavoidable errors: A spatio-temporal analysis of time-course and neural sources of evoked potentials associated with error processing in a speeded task , 2008, Neuropsychologia.

[9]  G. Woodman.  Masked targets trigger event-related potentials indexing shifts of attention but not error detection. , 2010, Psychophysiology.

[10]  Martin Lotze,et al.  Brain activation during anticipation of interoceptive threat , 2012, NeuroImage.

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

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

[13]  John J. B. Allen,et al.  Task-related dissociation in ERN amplitude as a function of obsessive–compulsive symptoms , 2009, Neuropsychologia.

[14]  Derek H. Arnold,et al.  The oddball effect: perceived duration and predictive coding. , 2011, Journal of vision.

[15]  Anna Weinberg,et al.  Error-related brain activity in the age of RDoC: A review of the literature. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

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

[18]  Greg Hajcak,et al.  What We’ve Learned From Mistakes , 2012 .

[19]  Rhodri Cusack,et al.  Listening to Your Heart , 2010, Psychological science.

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

[21]  K. R. Ridderinkhof,et al.  Response inhibition in conflict tasks is revealed in delta plots , 2004 .

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

[23]  Y Kikuchi,et al.  Chemosensitivity and perception of dyspnea in patients with a history of near-fatal asthma. , 1994, The New England journal of medicine.

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

[25]  O. Pollatos,et al.  Neural systems connecting interoceptive awareness and feelings , 2007, Human brain mapping.

[26]  R. McNally,et al.  Anxiety sensitivity and panic disorder , 2002, Biological Psychiatry.

[27]  J. Hankinson,et al.  Standardisation of spirometry , 2005, European Respiratory Journal.

[28]  C. Sherrington.  Observations on the scratch‐reflex in the spinal dog , 1906, The Journal of physiology.

[29]  Marco Steinhauser,et al.  Errors can elicit an error positivity in the absence of an error negativity: Evidence for independent systems of human error monitoring , 2018, NeuroImage.

[30]  Clay B. Holroyd,et al.  The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. , 2002, Psychological review.

[31]  S. Segalowitz,et al.  Retest reliability of medial frontal negativities during performance monitoring. , 2010, Psychophysiology.

[32]  J. Ito,et al.  Performance Monitoring and Error Processing During a Lexical Decision Task in Patients With Parkinson’s Disease , 2006, Journal of geriatric psychiatry and neurology.

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

[34]  U. Sailer,et al.  Event-related potentials in performance monitoring are influenced by the endogenous opioid system , 2015, Neuropsychologia.

[35]  Dara S. Manoach,et al.  Neural markers of errors as endophenotypes in neuropsychiatric disorders , 2013, Front. Hum. Neurosci..

[36]  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.

[37]  Richard J. Brown,et al.  Symptoms and the body: Taking the inferential leap , 2017, Neuroscience & Biobehavioral Reviews.

[38]  P. Barnes.  Blunted perception and death from asthma. , 1994, The New England journal of medicine.

[39]  M. Zvolensky,et al.  Sixteen-Item Anxiety Sensitivity Index , 2007, Assessment.

[40]  Greg H. Proudfit,et al.  Anxiety and error monitoring: the importance of motivation and emotion , 2013, Front. Hum. Neurosci..

[41]  Patrick Berg,et al.  Artifact Correction of the Ongoing EEG Using Spatial Filters Based on Artifact and Brain Signal Topographies , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[42]  Justin S. Feinstein,et al.  Interoception and Mental Health: A Roadmap , 2017, Biological psychiatry. Cognitive neuroscience and neuroimaging.

[43]  S. Wiens.  Interoception in emotional experience , 2005, Current opinion in neurology.

[44]  Anna Weinberg,et al.  Increased error-related brain activity in generalized anxiety disorder , 2010, Biological Psychology.

[45]  M. Coles,et al.  Dissociation of Pe and ERN/Ne in the conscious recognition of an error. , 2011, Psychophysiology.

[46]  William J. Gehring,et al.  The Error-Related Negativity (ERN/Ne) , 2011 .

[47]  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.

[48]  Clay B. Holroyd,et al.  Why is there an ERN/Ne on correct trials? Response representations, stimulus-related components, and the theory of error-processing , 2001, Biological Psychology.

[49]  Sarah L. Master,et al.  Neurocognitive correlates of liberalism and conservatism , 2007, Nature Neuroscience.

[50]  O. Cameron,et al.  Interoception: The Inside Story—A Model for Psychosomatic Processes , 2001, Psychosomatic medicine.

[51]  Marco Steinhauser,et al.  Error significance but not error expectancy predicts error-related negativities for different error types , 2016, Behavioural Brain Research SreeTestContent1.

[52]  H. Mayberg.  Brain Activation , 1994, Neurology.

[53]  S. Reiss,et al.  Anxiety sensitivity, anxiety frequency and the prediction of fearfulness. , 1986, Behaviour research and therapy.

[54]  David A. Seminowicz,et al.  Cortical responses to pain in healthy individuals depends on pain catastrophizing , 2006, Pain.

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

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

[57]  G. A. Miller,et al.  Committee report: publication guidelines and recommendations for studies using electroencephalography and magnetoencephalography. , 2014, Psychophysiology.

[58]  Anna Weinberg,et al.  Integrating multiple perspectives on error-related brain activity: The ERN as a neural indicator of trait defensive reactivity , 2011, Motivation and Emotion.

[59]  Enea F Pavone,et al.  Electrophysiological correlates of crossmodal visual distractor congruency effects: Evidence for response conflict , 2008, Cognitive, affective & behavioral neuroscience.

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

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

[62]  James F. Cavanagh,et al.  Altered cingulate sub-region activation accounts for task-related dissociation in ERN amplitude as a function of obsessive-compulsive symptoms , 2010, Neuropsychologia.

[63]  Nick Yeung,et al.  Shared Neural Markers of Decision Confidence and Error Detection , 2015, The Journal of Neuroscience.

[64]  Anna Weinberg,et al.  Biological Psychology , 2022 .

[65]  J. Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

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

[67]  Sidney J. Segalowitz,et al.  The effects of uncertainty in error monitoring on associated ERPs , 2004, Brain and Cognition.

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

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

[70]  M. Paulus,et al.  Interoception in anxiety and depression , 2010, Brain Structure and Function.

[71]  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.

[72]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[73]  G. Hajcak,et al.  The effect of trial-to-trial feedback on the error-related negativity and its relationship with anxiety , 2009, Cognitive, affective & behavioral neuroscience.

[74]  H. Critchley,et al.  An Interoceptive Predictive Coding Model of Conscious Presence , 2011, Front. Psychology.

[75]  Anna Weinberg,et al.  Increased error-related brain activity distinguishes generalized anxiety disorder with and without comorbid major depressive disorder. , 2012, Journal of abnormal psychology.

[76]  J Hohnsbein,et al.  Effects of crossmodal divided attention on late ERP components. I. Simple and choice reaction tasks. , 1991, Electroencephalography and clinical neurophysiology.

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

[78]  J. Hohnsbein,et al.  Late ERP components in visual and auditory Go/Nogo tasks. , 1995, Electroencephalography and clinical neurophysiology.

[79]  Jonathan D. Cohen,et al.  The neural basis of error detection: conflict monitoring and the error-related negativity. , 2004, Psychological review.

[80]  P. Davenport,et al.  Magnitude estimation of inspiratory resistive loads in children with life-threatening asthma. , 1997, American journal of respiratory and critical care medicine.

[81]  A. Kaczkurkin,et al.  The effect of manipulating task difficulty on error-related negativity in individuals with obsessive-compulsive symptoms , 2013, Biological Psychology.

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

[83]  H. Critchley,et al.  Mind-Body Interactions in Anxiety and Somatic Symptoms , 2016, Harvard review of psychiatry.

[84]  P. Weiner,et al.  The risk of hospitalization and near-fatal and fatal asthma in relation to the perception of dyspnea. , 2002, Chest.

[85]  C. Büchel,et al.  Dyspnea catastrophizing and neural activations during the anticipation and perception of dyspnea. , 2018, Psychophysiology.

[86]  Pei-Ying S. Chan,et al.  Cortical sources of the respiratory-related evoked potential , 2010, Respiratory Physiology & Neurobiology.

[87]  G. Woodman,et al.  Causal Control of Medial–Frontal Cortex Governs Electrophysiological and Behavioral Indices of Performance Monitoring and Learning , 2014, The Journal of Neuroscience.

[88]  John J. B. Allen,et al.  Theta EEG dynamics of the error-related negativity , 2007, Clinical Neurophysiology.

[89]  Interoception Summit participants.  Interoception and Mental Health: A Roadmap , 2017 .

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

[91]  María Isabel Núñez-Peña,et al.  Abnormal Error Monitoring in Math-Anxious Individuals: Evidence from Error-Related Brain Potentials , 2013, PloS one.