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The inner world of overactive monitoring: neural markers of interoception in obsessive–compulsive disorder

  • A. Yoris (a1) (a2) (a3), A. M. García (a1) (a2) (a4), L. Traiber (a3), H. Santamaría-García (a1) (a2) (a5) (a6), M. Martorell (a1), F. Alifano (a1), R. Kichic (a1) (a3), J. S. Moser (a7), M. Cetkovich (a1), F. Manes (a1) (a2) (a8), A. Ibáñez (a1) (a2) (a8) (a9) (a10) and L. Sedeño (a1) (a2)...
Abstract
Background

Obsessive–compulsive disorder (OCD) patients typically overmonitor their own behavior, as shown by symptoms of excessive doubt and checking. Although this is well established for the patients’ relationship with external stimuli in the environment, no study has explored their monitoring of internal body signals, a process known to be affected in anxiety-related syndromes. Here, we explored this issue through a cardiac interoception task that measures sensing of heartbeats. Our aim was to explore key behavioral and electrophysiological aspects of internal-cue monitoring in OCD, while examining their potential distinctiveness in this condition.

Method

We administered a heartbeat detection (HBD) task (with related interoceptive confidence and awareness measures) to three matched groups (OCD patients, panic disorder patients, healthy controls) and recorded ongoing modulations of two task-relevant electrophysiological markers: the heart evoked potential (HEP) and the motor potential (MP).

Results

Behaviorally, OCD patients outperformed controls and panic patients in the HBD task. Moreover, they exhibited greater amplitude modulation of both the HEP and the MP during cardiac interoception. However, they evinced poorer confidence and awareness of their interoceptive skills.

Conclusions

Convergent behavioral and electrophysiological data showed that overactive monitoring in OCD extends to the sensing of internal bodily signals. Moreover, this pattern discriminated OCD from panic patients, suggesting a condition-distinctive alteration. Our results highlight the potential of exploring interoceptive processes in the OCD spectrum to better characterize the population's cognitive profile. Finally, these findings may lay new bridges between somatic theories of emotion and cognitive models of OCD.

Copyright
Corresponding author
*Address for correspondence: L. Sedeño, Laboratory of Experimental Psychology and Neuroscience (LPEN), Institute of Cognitive and Translational Neuroscience (INCyT), C1078AAI, Pacheco de Melo 1860, Buenos Aires, Argentina. (Email: lucas.sedeno@gmail.com)
References
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Aouizerate B, Guehl D, Cuny E, Rougier A, Bioulac B, Tignol J, Burbaud P (2004). Pathophysiology of obsessive–compulsive disorder: a necessary link between phenomenology, neuropsychology, imagery and physiology. Progress in Neurobiology 72, 195221.
American Psychiatric Association (1994). DSM-IV: Diagnostic and Statistical Manual. American Psychiatric Association: Washington, DC.
Aravena P, Hurtado E, Riveros R, Cardona JF, Manes F, Ibanez A (2010). Applauding with closed hands: neural signature of action–sentence compatibility effects. PLoS ONE 5, e11751.
Bannon S, Gonsalvez CJ, Croft RJ, Boyce PM (2002). Response inhibition deficits in obsessive–compulsive disorder. Psychiatry Research 110, 165174.
Barlow DH, Campbell LA (2000). Mixed anxiety–depression and its implications for models of mood and anxiety disorders. Comprehensive Psychiatry 41, 5560.
Belloch A, Morillo C, Luciano JV, Garcia-Soriano G, Cabedo E, Carrio C (2010). Dysfunctional belief domains related to obsessive–compulsive disorder: a further examination of their dimensionality and specificity. Spanish Journal of Psychology 13, 376388.
Brener J, Kluvitse C (1988). Heartbeat detection: judgments of the simultaneity of external stimuli and heartbeats. Psychophysiology 25, 554561.
Brevers D, Cleeremans A, Bechara A, Greisen M, Kornreich C, Verbanck P, Noel X (2013). Impaired self-awareness in pathological gamblers. Journal of Gambling Studies 29, 119129.
Brunia CH, Van den Bosch WE (1984). Movement-related slow potentials. I. A contrast between finger and foot movements in right-handed subjects. Electroencephalography and Clinical Neurophysiology 57, 515527.
Caldara R, Deiber MP, Andrey C, Michel CM, Thut G, Hauert CA (2004). Actual and mental motor preparation and execution: a spatiotemporal ERP study. Experimental Brain Research 159, 389399.
Cameron OG (2001). Interoception: the inside story – a model for psychosomatic processes. Psychosomatic Medicine 63, 697710.
Canales-Johnson A, Silva C, Huepe D, Rivera-Rei A, Noreika V, Garcia MD, Silva W, Ciraolo C, Vaucheret E, Sedeno L, Couto B, Kargieman L, Baglivo F, Sigman M, Chennu S, Ibanez A, Rodriguez E, Bekinschtein TA (2015). Auditory feedback differentially modulates behavioral and neural markers of objective and subjective performance when tapping to your heartbeat. Cerebral Cortex 25, 44904503.
Carrasco M, Harbin SM, Nienhuis JK, Fitzgerald KD, Gehring WJ, Hanna GL (2013). Increased error-related brain activity in youth with obsessive–compulsive disorder and unaffected siblings. Depression and Anxiety 30, 3946.
Coles ME, Frost RO, Heimberg RG, Rheaume J (2003). “Not just right experiences”: perfectionism, obsessive–compulsive features and general psychopathology. Behaviour Research and Therapy 41, 681700.
Coles ME, Schofield CA, Nota JA (2015). Initial data on recollections of pathways to inflated responsibility beliefs in patients with obsessive–compulsive disorder. Behavioural and Cognitive Psychotherapy 43, 385395.
Couto B, Adolfi F, Velasquez M, Mesow M, Feinstein J, Canales-Johnson A, Mikulan E, Martinez-Pernia D, Bekinschtein T, Sigman M, Manes F, Ibanez A (2015). Heart evoked potential triggers brain responses to natural affective scenes: a preliminary study. Autonomic Neuroscience: Basic and Clinical 193, 132137.
Couto B, Salles A, Sedeno L, Peradejordi M, Barttfeld P, Canales-Johnson A, Dos Santos YV, Huepe D, Bekinschtein T, Sigman M, Favaloro R, Manes F, Ibanez A (2014). The man who feels two hearts: the different pathways of interoception. Social Cognitive and Affective Neuroscience 9, 12531260.
Craig AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews. Neuroscience 3, 655666.
Craig AD (2003). Interoception: the sense of the physiological condition of the body. Current Opinion in Neurobiology 13, 500505.
Craig AD (2004). Human feelings: why are some more aware than others? Trends in Cognitive Sciences 8, 239241.
Critchley HD, Harrison NA (2013). Visceral influences on brain and behavior. Neuron 77, 624638.
Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience 7, 189195.
Cucchi M, Bottelli V, Cavadini D, Ricci L, Conca V, Ronchi P, Smeraldi E (2012). An explorative study on metacognition in obsessive–compulsive disorder and panic disorder. Comprehensive Psychiatry 53, 546553.
Deecke L, Bashore T, Brunia CH, Grunewald-Zuberbier E, Grunewald G, Kristeva R (1984). Movement-associated potentials and motor control. Report of the EPIC VI Motor Panel. Annals of the New York Academy of Sciences 425, 398428.
Deecke L, Eisinger H, Kornhuber HH (1980). Comparison of Bereitschaftspotential, pre-motion positivity and motor potential preceding voluntary flexion and extension movements in man. Progress in Brain Research 54, 171176.
Domschke K, Stevens S, Pfleiderer B, Gerlach AL (2010). Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings. Clinical Psychology Review 30, 111.
Dum RP, Levinthal DJ, Strick PL (2009). The spinothalamic system targets motor and sensory areas in the cerebral cortex of monkeys. Journal of Neuroscience: the Official Journal of the Society for Neuroscience 29, 1422314235.
Dunn BD, Dalgleish T, Ogilvie AD, Lawrence AD (2007). Heartbeat perception in depression. Behaviour Research and Therapy 45, 19211930.
Ehlers A, Breuer P (1992). Increased cardiac awareness in panic disorder. Journal of Abnormal Psychology 101, 371382.
Endrass T, Klawohn J, Schuster F, Kathmann N (2008). Overactive performance monitoring in obsessive–compulsive disorder: ERP evidence from correct and erroneous reactions. Neuropsychologia 46, 18771887.
Endrass T, Schuermann B, Kaufmann C, Spielberg R, Kniesche R, Kathmann N (2010). Performance monitoring and error significance in patients with obsessive–compulsive disorder. Biological Psychology 84, 257263.
Endrass T, Ullsperger M (2014). Specificity of performance monitoring changes in obsessive–compulsive disorder. Neuroscience and Biobehavioral Reviews 46, 124138.
First MB, Spitzer RL, Gibbon M, Williams JB (2002). Structured Clinical Interview for DSM-IV Axis I Disorders, Research Version, Patient Edition (SCID-I/P) . Biometrics Research, New York State Psychiatric Institute: New York.
Foa EB, Huppert JD, Leiberg S, Langner R, Kichic R, Hajcak G, Salkovskis PM (2002). The Obsessive–Compulsive Inventory: development and validation of a short version. Psychological Assessment 14, 485496.
Fukushima H, Terasawa Y, Umeda S (2011). Association between interoception and empathy: evidence from heartbeat-evoked brain potential. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology 79, 259265.
García-Cordero I, Sedeño L, de la Fuente L, Slachevsky A, Forno G, Klein F, Lillo P, Ferrari J, Rodriguez C, Bustin J, Torralva T, Baez S, Yoris A, Esteves S, Melloni M, Salamone P, Huepe D, Manes F, García AM, Ibañez A (2016). Feeling, learning from, and being aware of inner states: interoceptive dimensions in neurodegeneration and stroke. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 371, 20160006.
Garfinkel SN, Seth AK, Barrett AB, Suzuki K, Critchley HD (2015). Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biological Psychology 104, 6574.
Gehring WJ, Himle J, Nisenson LG (2000). Action-monitoring dysfunction in obsessive–compulsive disorder. Psychological Science 11, 16.
Gray MA, Taggart P, Sutton PM, Groves D, Holdright DR, Bradbury D, Brull D, Critchley HD (2007). A cortical potential reflecting cardiac function. Proceedings of the National Academy of Sciences USA 104, 68186823.
Hajcak G, Franklin ME, Foa EB, Simons RF (2008). Increased error-related brain activity in pediatric obsessive–compulsive disorder before and after treatment. American Journal of Psychiatry 165, 116123.
Hanna GL, Carrasco M, Harbin SM, Nienhuis JK, LaRosa CE, Chen P, Fitzgerald KD, Gehring WJ (2012). Error-related negativity and tic history in pediatric obsessive–compulsive disorder. Journal of the American Academy of Child and Adolescent Psychiatry 51, 902910.
Hermans D, Engelen U, Grouwels L, Joos E, Lemmens J, Pieters G (2008). Cognitive confidence in obsessive–compulsive disorder: distrusting perception, attention and memory. Behaviour Research and Therapy 46, 98113.
Ibanez A, Cardona JF, Dos Santos YV, Blenkmann A, Aravena P, Roca M, Hurtado E, Nerguizian M, Amoruso L, Gomez-Arevalo G, Chade A, Dubrovsky A, Gershanik O, Kochen S, Glenberg A, Manes F, Bekinschtein T (2013). Motor–language coupling: direct evidence from early Parkinson's disease and intracranial cortical recordings. Cortex 49, 968984.
Janeck AS, Calamari JE, Riemann BC, Heffelfinger SK (2003). Too much thinking about thinking?: metacognitive differences in obsessive–compulsive disorder. Journal of Anxiety Disorders 17, 181195.
Janig W (1996). Neurobiology of visceral afferent neurons: neuroanatomy, functions, organ regulations and sensations. Biological Psychology 42, 2951.
Johannes S, Wieringa BM, Mantey M, Nager W, Rada D, Muller-Vahl KR, Emrich HM, Dengler R, Munte TF, Dietrich D (2001). Altered inhibition of motor responses in Tourette syndrome and obsessive–compulsive disorder. Acta Neurologica Scandinavica 104, 3643.
Kaczkurkin AN (2013). The effect of manipulating task difficulty on error-related negativity in individuals with obsessive–compulsive symptoms. Biological Psychology 93, 122131.
Khalsa SS, Rudrauf D, Feinstein JS, Tranel D (2009). The pathways of interoceptive awareness. Nature Neuroscience 12, 14941496.
Kleckner IR, Wormwood JB, Simmons WK, Barrett LF, Quigley KS (2015). Methodological recommendations for a heartbeat detection-based measure of interoceptive sensitivity. Psychophysiology 52, 14321440.
Kruczyk M, Umer HM, Enroth S, Komorowski J (2013). Peak finder metaserver – a novel application for finding peaks in ChIP-seq data. BMC Bioinformatics 14, 280.
Leopold C, Schandry R (2001). The heartbeat-evoked brain potential in patients suffering from diabetic neuropathy and in healthy control persons. Clinical Neurophysiology 112, 674682.
Lin Y, Moran TP, Schroder HS, Moser JS (2015). The role of hand of error and stimulus orientation in the relationship between worry and error-related brain activity: implications for theory and practice. Psychophysiology 52, 12811292.
Manly BFJ (2007). Randomization, Bootstrap, and Monte Carlo Methods in Biology. Chapman & Hall/CRC: Boca Raton, FL.
Mataix-Cols D, Wooderson S, Lawrence N, Brammer MJ, Speckens A, Phillips ML (2004). Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive–compulsive disorder. Archives of General Psychiatry 61, 564576.
Montoya P, Schandry R, Muller A (1993). Heartbeat evoked potentials (HEP): topography and influence of cardiac awareness and focus of attention. Electroencephalography and Clinical Neurophysiology 88, 163172.
Moser JS, Moran TP, Schroder HS, Donnellan MB, Yeung N (2013). On the relationship between anxiety and error monitoring: a meta-analysis and conceptual framework. Frontiers in Human Neuroscience 7, 466.
Moulding R, Anglim J, Nedeljkovic M, Doron G, Kyrios M, Ayalon A (2011). The Obsessive Beliefs Questionnaire (OBQ): examination in nonclinical samples and development of a short version. Assessment 18, 357374.
Muller LE, Schulz A, Andermann M, Gabel A, Gescher DM, Spohn A, Herpertz SC, Bertsch K (2015). Cortical representation of afferent bodily signals in borderline personality disorder: neural correlates and relationship to emotional dysregulation. JAMA Psychiatry 72, 10771086.
Nagai M, Kishi K, Kato S (2007). Insular cortex and neuropsychiatric disorders: a review of recent literature. European Psychiatry: the Journal of the Association of European Psychiatrists 22, 387394.
Nichols TE, Holmes AP (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping 15, 125.
Odlaug BL, Chamberlain SR, Derbyshire KL, Leppink EW, Grant JE (2014). Impaired response inhibition and excess cortical thickness as candidate endophenotypes for trichotillomania. Journal of Psychiatric Research 59, 167173.
Pollatos O, Herbert BM, Mai S, Kammer T (2016). Changes in interoceptive processes following brain stimulation. Philosophical Transaction of the Royal Society of London 371, 20160016.
Pollatos O, Kirsch W, Schandry R (2005). Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study. Human Brain Mapping 26, 5464.
Pollatos O, Matthias E, Schandry R (2007). Heartbeat perception and P300 amplitude in a visual oddball paradigm. Clinical Neurophysiology 118, 22482253.
Pollatos O, Schandry R (2004). Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology 41, 476482.
Rabinak CA, Holman A, Angstadt M, Kennedy AE, Hajcak G, Phan KL (2013). Neural response to errors in combat-exposed returning veterans with and without post-traumatic stress disorder: a preliminary event-related potential study. Psychiatry Research 213, 7178.
Riesel A, Endrass T, Auerbach LA, Kathmann N (2015). Overactive performance monitoring as an endophenotype for obsessive–compulsive disorder: evidence from a treatment study. American Journal of Psychiatry 172, 665673.
Riesel A, Endrass T, Kaufmann C, Kathmann N (2011). Overactive error-related brain activity as a candidate endophenotype for obsessive–compulsive disorder: evidence from unaffected first-degree relatives. American Journal of Psychiatry 168, 317324.
Riesel A, Kathmann N, Endrass T (2014). Overactive performance monitoring in obsessive–compulsive disorder is independent of symptom expression. European Archives of Psychiatry and Clinical Neuroscience 264, 707717.
Ronchi R, Bello-Ruiz J, Lukowska M, Herbelin B, Cabrilo I, Schaller K, Blanke O (2015). Right insular damage decreases heartbeat awareness and alters cardio-visual effects on bodily self-consciousness. Neuropsychologia 70, 1120.
Ruscio AM, Stein DJ, Chiu WT, Kessler RC (2010). The epidemiology of obsessive–compulsive disorder in the National Comorbidity Survey Replication. Molecular Psychiatry 15, 5363.
Salkovskis PM (1985). Obsessional–compulsive problems: a cognitive–behavioural analysis. Behaviour Research and Therapy 23, 571583.
Salkovskis PM, Wroe AL, Gledhill A, Morrison N, Forrester E, Richards C, Reynolds M, Thorpe S (2000). Responsibility attitudes and interpretations are characteristic of obsessive compulsive disorder. Behaviour Research and Therapy 38, 347372.
Schandry R, Bestler M, Montoya P (1993). On the relation between cardiodynamics and heartbeat perception. Psychophysiology 30, 467474.
Schandry R, Sparrer B, Weitkunat R (1986). From the heart to the brain: a study of heartbeat contingent scalp potentials. International Journal of Neuroscience 30, 261275.
Schandry R, Weitkunat R (1990). Enhancement of heartbeat-related brain potentials through cardiac awareness training. International Journal of Neuroscience 53, 243253.
Schrijvers DL, De Bruijn ER, Destoop M, Hulstijn W, Sabbe BG (2010). The impact of perfectionism and anxiety traits on action monitoring in major depressive disorder. Journal of Neural Transmition (Vienna) 117, 869880.
Schulz A, Koster S, Beutel ME, Schachinger H, Vogele C, Rost S, Rauh M, Michal M (2015). Altered patterns of heartbeat-evoked potentials in depersonalization/derealization disorder: neurophysiological evidence for impaired cortical representation of bodily signals. Psychosomatic Medicine 77, 506516.
Schulz A, Matthey JH, Vogele C, Schaan V, Schachinger H, Adler J, Beutel ME, Michal M (2016). Cardiac modulation of startle is altered in depersonalization-/derealization disorder: evidence for impaired brainstem representation of baro-afferent neural traffic. Psychiatry Research 240, 410.
Sedeno L, Couto B, Melloni M, Canales-Johnson A, Yoris A, Baez S, Esteves S, Velasquez M, Barttfeld P, Sigman M, Kichic R, Chialvo D, Manes F, Bekinschtein TA, Ibanez A (2014). How do you feel when you can't feel your body? Interoception, functional connectivity and emotional processing in depersonalization–derealization disorder. PLOS ONE 9, e98769.
Shao S, Shen K, Wilder-Smith EP, Li X (2011). Effect of pain perception on the heartbeat evoked potential. Clinical Neurophysiology: Official Journal of the International Federation of Clinical Neurophysiology 122, 18381845.
Simons RF (2010). The way of our errors: theme and variations. Psychophysiology 47, 114.
Song A, Jung WH, Jang JH, Kim E, Shim G, Park HY, Choi CH, Kwon JS (2011). Disproportionate alterations in the anterior and posterior insular cortices in obsessive–compulsive disorder. PLoS ONE 6, e22361.
Spielberger CD, Gorsuch RL, Lushene RE (1970). Manual for the Stait-Trait Anxiety Inventory. Consulting Psychological Press: Palo Alto, CA.
Starcevic V, Berle D, Brakoulias V, Sammut P, Moses K, Milicevic D, Hannan A (2011). Functions of compulsions in obsessive–compulsive disorder. Australian and New Zealand Journal of Psychiatry 45, 449457.
Stern ER, Liu Y, Gehring WJ, Lister JJ, Yin G, Zhang J, Fitzgerald KD, Himle JA, Abelson JL, Taylor SF (2010). Chronic medication does not affect hyperactive error responses in obsessive–compulsive disorder. Psychophysiology 47, 913920.
Terasawa Y, Kurosaki Y, Ibata Y, Moriguchi Y, Umeda S (2015). Attenuated sensitivity to the emotions of others by insular lesion. Frontiers in Psychology 6, 1314.
Terhaar J, Viola FC, Bar KJ, Debener S (2012). Heartbeat evoked potentials mirror altered body perception in depressed patients. Clinical Neurophysiology 123, 19501957.
Vartanian LR, Germeroth LJ (2011). Accuracy in estimating the body weight of self and others: impact of dietary restraint and BMI. Body Image 8, 415418.
Vaughan HG Jr., Costa LD, Ritter W (1968). Topography of the human motor potential. Electroencephalography and Clinical Neurophysiology 25, 110.
Weinberg A, Olvet DM, Hajcak G (2010). Increased error-related brain activity in generalized anxiety disorder. Biological Psychology 85, 472480.
Weiss S, Sack M, Henningsen P, Pollatos O (2014). On the interaction of self-regulation, interoception and pain perception. Psychopathology 47, 377382.
Wiens S, Palmer SN (2001). Quadratic trend analysis and heartbeat detection. Biological Psychology 58, 159175.
Willem Van der Does AJ, Antony MM, Ehlers A, Barsky AJ (2000). Heartbeat perception in panic disorder: a reanalysis. Behaviour Research and Therapy 38, 4762.
Xiao Z, Wang J, Zhang M, Li H, Tang Y, Wang Y, Fan Q, Fromson JA (2011). Error-related negativity abnormalities in generalized anxiety disorder and obsessive–compulsive disorder. Progress in Neuro-psychopharmacology and Biological Psychiatry 35, 265272.
Yoris A, Esteves S, Couto B, Melloni M, Kichic R, Cetkovich M, Favaloro R, Moser J, Manes F, Ibanez A, Sedeno L (2015). The roles of interoceptive sensitivity and metacognitive interoception in panic. Behavioral and Brain Functions: BBF 11, 14.
Zaki J, Davis JI, Ochsner KN (2012). Overlapping activity in anterior insula during interoception and emotional experience. NeuroImage 62, 493499.
Zigmond AS, Snaith RP (1983). The Hospital Anxiety and Depression Scale. Acta Psychiatrica Scandinavica 67, 361370.
Zinbarg RE, Barlow DH (1996). Structure of anxiety and the anxiety disorders: a hierarchical model. Journal of Abnormal Psychology 105, 181193.
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