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Error-related brain activity dissociates hoarding disorder from obsessive-compulsive disorder

Published online by Cambridge University Press:  29 September 2015

C. A. Mathews ,
V. B. Perez ,
B. J. Roach ,
S. Fekri ,
O. Vigil ,
E. Kupferman  and
D. H. Mathalon
C. A. Mathews*
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA Department of Psychiatry, University of Florida, Gainesville, FL, USA
V. B. Perez
Affiliation:
California School of Professional Psychology (CSPP), Alliant International University Department of Psychiatry, University of California, San Diego, CA, USA Veterans Integrated Service Network (VISN) 22, Veterans Affairs San Diego Healthcare System, La Jolla, CA, USA
B. J. Roach
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA San Francisco VA Medical Center, San Francisco, CA, USA
S. Fekri
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA
O. Vigil
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA
E. Kupferman
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA
D. H. Mathalon
Affiliation:
Department of Psychiatry, University of California, San Francisco, CA, USA San Francisco VA Medical Center, San Francisco, CA, USA
*
*Address for correspondence: C. A. Mathews, MD, Department of Psychiatry, University of Florida, 100 S. Newell Dr. L4-100, Gainesville, FL 32610, USA. (Email: [email protected])
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Abstract

Background

Obsessive-compulsive disorder (OCD) is associated with an abnormally large error-related negativity (ERN), an electrophysiological measure of error monitoring in response to performance errors, but it is unclear if hoarding disorder (HD) also shows this abnormality. This study aimed to determine whether the neurophysiological mechanisms underlying error monitoring are similarly compromised in HD and OCD.

Method

We used a visual flanker task to assess ERN in response to performance errors in 14 individuals with HD, 27 with OCD, 10 with HD+OCD, and 45 healthy controls (HC). Age-corrected performance and ERN amplitudes were examined using analyses of variance and planned pairwise group comparisons.

Results

A main effect of hoarding on ERN (p = 0.031) was observed, indicating ERN amplitudes were attenuated in HD relative to non-HD subjects. A group × age interaction effect on ERN was also evident. In HD-positive subjects, ERN amplitude deficits were significantly greater in younger individuals (r = −0.479, p = 0.018), whereas there were no significant ERN changes with increasing age in OCD and HC participants.

Conclusions

The reduced ERN in HD relative to OCD and HC provides evidence that HD is neurobiologically distinct from OCD, and suggests that deficient error monitoring may be a core pathophysiological feature of HD. This effect was particularly prominent in younger HD participants, further suggesting that deficient error monitoring manifests most strongly early in the illness course and/or in individuals with a relatively early illness onset.

Keywords

Electroencephalography/event-related potentials (EEG/ERP)error monitoringerror-related negativity (ERN)hoardingneurophysiologicalobsessive-compulsive disorder (OCD)
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 2 , January 2016 , pp. 367 - 379
Copyright
Copyright © Cambridge University Press 2015 

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References

APA (2013). Disgnostic and Statistical Manual of Mental Disorders, 5th edn. American Psychiatric Association: Arlington, VA.Google Scholar
An, SK, Mataix-Cols, D, Lawrence, NS, Wooderson, S, Giampietro, V, Speckens, A, Brammer, MJ, Phillips, ML (2008). To discard or not to discard: the neural basis of hoarding symptoms in obsessive-compulsive disorder. Molecular Psychiatry 14, 318–331.CrossRefGoogle ScholarPubMed
Ayers, CR, Saxena, S, Espejo, E, Twamley, EW, Granholm, E, Wetherell, JL (2013). Novel treatment for geriatric hoarding disorder: an open trial of cognitive rehabilitation paired with behavior therapy. American Journal of Geriatric Psychiatry 22, 248–252.CrossRefGoogle ScholarPubMed
Ayers, CR, Saxena, S, Golshan, S, Wetherell, JL (2010). Age at onset and clinical features of late life compulsive hoarding. International Journal of Geriatric Psychiatry 25, 142–149.CrossRefGoogle ScholarPubMed
Bartholow, BD, Pearson, MA, Dickter, CL, Sher, KJ, Fabiani, M, Gratton, G (2005). Strategic control and medial frontal negativity: beyond errors and response conflict. Psychophysiology 42, 33–42.CrossRefGoogle ScholarPubMed
Beck, AT, Steer, RA (1993). Beck Anxiety Inventory. Harcourt Assessment Inc.: San Antonio.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Botvinick, M, Nystrom, LE, Fissell, K, Carter, CS, Cohen, JD (1999). Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179–181.Google Scholar
Botvinick, MM, Braver, TS, Barch, DM, Carter, CS, Cohen, JD (2001). Conflict monitoring and cognitive control. Psychological Review 108, 624–652.CrossRefGoogle ScholarPubMed
Brown, JW, Braver, TS (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science 307, 1118–1121.Google Scholar
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 & Anxiety 30, 39–46.Google Scholar
Crovitz, HF, Zener, K (1962). A group-test for assessing hand-and eye-dominance. American Journal of Psychology 75, 271–276.Google Scholar
Davies, PL, Segalowitz, SJ, Gavin, WJ (2004). Development of response-monitoring ERPs in 7- to 25-year-olds. Developmental Neuropsychology 25, 355–376.Google Scholar
de Bruijn, ER, Sabbe, BG, Hulstijn, W, Ruigt, GS, Verkes, RJ (2006). Effects of antipsychotic and antidepressant drugs on action monitoring in healthy volunteers. Brain Research 1105, 122–129.Google Scholar
Debener, S, Ullsperger, M, Siegel, M, Fiehler, K, von Cramon, DY, Engel, AK (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. Journal of Neuroscience 25, 11730–11737.Google Scholar
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, 1877–1887.Google Scholar
Endrass, T, Riesel, A, Kathmann, N, Buhlmann, U (2014). Performance monitoring in obsessive-compulsive disorder and social anxiety disorder. Journal of Abnormal Psychology 123, 705–714.Google Scholar
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, 257–263.CrossRefGoogle ScholarPubMed
Endrass, T, Ullsperger, M (2014). Specificity of performance monitoring changes in obsessive-compulsive disorder. Neuroscience & Biobehavioral Reviews 46, 124–138.Google Scholar
Eriksen, BA, Eriksen, CW (1974). Effects of noise letters upon the identification of a target letter in a nonsearch task. Attention, Perception & Psychophysics 16, 143–149.Google Scholar
Falkenstein, M, Hohnsbein, J, Hoormann, J, Blanke, L (1991). Effects of crossmodal divided attention on late ERP components. II. Error processing in choice reaction tasks. Electroencephalography and Clinical Neurophysiology 78, 447–455.Google Scholar
Falkenstein, M, Hoormann, J, Hohnsbein, J (2001). Changes of error-related ERPs with age. Experimental Brain Research 138, 258–262.Google Scholar
Fitzgerald, KD, Welsh, RC, Gehring, WJ, Abelson, JL, Himle, JA, Liberzon, I, Taylor, SF (2005). Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder. Biological Psychiatry 57, 287–294.Google Scholar
Friedman, D, Nessler, D, Cycowicz, YM, Horton, C (2009). Development of and change in cognitive control: a comparison of children, young adults, and older adults. Cognitive, Affective & Behavioral Neuroscience 9, 91–102.CrossRefGoogle ScholarPubMed
Frost, RO, Gross, RC (1993). The hoarding of possessions. Behavioral Research and Therapy 31, 367–381.CrossRefGoogle ScholarPubMed
Frost, RO, Steketee, G, Grisham, J (2004). Measurement of compulsive hoarding: saving inventory-revised. Behavioral Research & Therapy 42, 1163–1182.CrossRefGoogle ScholarPubMed
Gehring, WJ, Goss, B, Coles, MGH, Meyer, DE, Donchin, E (1993). A neural system for error detection and compensation. Psychological Science 4, 385–390.CrossRefGoogle Scholar
Gehring, WJ, Himle, J, Nisenson, LG (2000). Action-monitoring dysfunction in obsessive-compulsive disorder. Psychological Science 11, 1–6.CrossRefGoogle ScholarPubMed
Goodman, WK, Price, LH, Rasmussen, SA, Mazure, C, Fleischmann, RL, Hill, CL, Heninger, GR, Charney, DS (1989). The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 1006–1011.Google Scholar
Gratton, G, Coles, MG, Donchin, E (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology 55, 468–484.Google Scholar
Gratton, G, Coles, MG, Sirevaag, EJ, Eriksen, CW, Donchin, E (1988). Pre- and poststimulus activation of response channels: a psychophysiological analysis. Journal of Experimental Psychology: Human Perception and Performance 14, 331–344.Google Scholar
Grisham, JR, Frost, RO, Steketee, G, Kim, HJ, Hood, S (2006). Age of onset of compulsive hoarding. Journal of Anxiety Disorders 20, 675–686.Google Scholar
Grisham, JR, Norberg, MM, Williams, AD, Certoma, SP, Kadib, R (2010). Categorization and cognitive deficits in compulsive hoarding. Behavioral Research & Therapy 48, 866–872.Google Scholar
Grundler, TO, Cavanagh, JF, Figueroa, CM, Frank, MJ, Allen, JJ (2009). Task-related dissociation in ERN amplitude as a function of obsessive-compulsive symptoms. Neuropsychologia 47, 1978–1987.CrossRefGoogle ScholarPubMed
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, 116–123.Google Scholar
Hall, BJ, Tolin, DF, Frost, RO, Steketee, G (2013). An exploration of comorbid symptoms and clinical correlates of clinically significant hoarding symptoms. Depression & Anxiety 30, 67–76.Google Scholar
Hammer, A, Kordon, A, Heldmann, M, Zurowski, B, Munte, TF (2009). Brain potentials of conflict and error-likelihood following errorful and errorless learning in obsessive-compulsive disorder. PLoS ONE 4, e6553.CrossRefGoogle ScholarPubMed
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 & Adolescent Psychiatry 51, 902–910.Google Scholar
Holroyd, CB, Coles, MG (2002). The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychological Review 109, 679–709.CrossRefGoogle ScholarPubMed
Iervolino, AC, Perroud, N, Fullana, MA, Guipponi, M, Cherkas, L, Collier, DA, Mataix-Cols, D (2009). Prevalence and heritability of compulsive hoarding: a twin study. American Journal of Psychiatry 166, 1156–1161.Google Scholar
Johannes, S, Wieringa, BM, Nager, W, Rada, D, Dengler, R, Emrich, HM, Munte, TF, Dietrich, DE (2001). Discrepant target detection and action monitoring in obsessive-compulsive disorder. Psychiatry Research 108, 101–110.Google Scholar
Kaczkurkin, AN (2013). The effect of manipulating task difficulty on error-related negativity in individuals with obsessive-compulsive symptoms. Biological Psychology 93, 122–131.Google Scholar
Kim, HJ, Steketee, G, Frost, RO (2001). Hoarding by elderly people. Health & Social Work 26, 176–184.Google Scholar
Klawohn, J, Riesel, A, Grutzmann, R, Kathmann, N, Endrass, T (2014). Performance monitoring in obsessive-compulsive disorder: a temporo-spatial principal component analysis. Cognitive, Affective & Behavioral Neuroscience 14, 983–995.Google Scholar
Leonowicz, Z, Karvanen, J, Shishkin, SL (2005). Trimmed estimators for robust averaging of event-related potentials. Journal of Neuroscience Methods 142, 17–26.Google Scholar
Luk, CH, Wallis, JD (2013). Choice coding in frontal cortex during stimulus-guided or action-guided decision-making. Journal of Neuroscience 33, 1864–1871.Google Scholar
Maltby, N, Tolin, DF, Worhunsky, P, O'Keefe, TM, Kiehl, KA (2005). Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder: an event-related fMRI study. Neuroimage 24, 495–503.Google Scholar
Mataix-Cols, D, Billotti, D, Fernandez de la Cruz, L, Nordsletten, AE (2012). The London field trial for hoarding disorder. Psychological Medicine 43, 837–847.Google Scholar
Mathews, CA, Nievergelt, CM, Azzam, A, Garrido, H, Chavira, DA, Wessel, J, Bagnarello, M, Reus, VI, Schork, NJ (2007). Heritability and clinical features of multigenerational families with obsessive-compulsive disorder and hoarding. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics 144, 174–182.Google Scholar
Mathews, CA, Perez, VB, Delucchi, KL, Mathalon, DH (2012). Error-related negativity in individuals with obsessive-compulsive symptoms: toward an understanding of hoarding behaviors. Biological Psychology 89, 487–494.Google Scholar
Meyer, A, Riesel, A, Hajcak Proudfit, G (2013). Reliability of the ERN across multiple tasks as a function of increasing errors. Psychophysiology 50, 1220–1225.Google Scholar
Morein-Zamir, S, Papmeyer, M, Pertusa, A, Chamberlain, SR, Fineberg, NA, Sahakian, BJ, Mataix-Cols, D, Robbins, TW (2014). The profile of executive function in OCD hoarders and hoarding disorder. Psychiatry Research 215, 659–667.CrossRefGoogle ScholarPubMed
Nieuwenhuis, S, Nielen, MM, Mol, N, Hajcak, G, Veltman, DJ (2005). Performance monitoring in obsessive-compulsive disorder. Psychiatry Research 134, 111–122.Google Scholar
Nieuwenhuis, S, Ridderinkhof, KR, Talsma, D, Coles, MG, Holroyd, CB, Kok, A, van der Molen, MW (2002). A computational account of altered error processing in older age: dopamine and the error-related negativity. Cognitive, Affective & Behavioral Neuroscience 2, 19–36.Google Scholar
Olvet, DM, Hajcak, G (2009). The stability of error-related brain activity with increasing trials. Psychophysiology 46, 957–961.Google Scholar
Perez, VB, Ford, JM, Roach, BJ, Woods, SW, McGlashan, TH, Srihari, VH, Loewy, RL, Vinogradov, S, Mathalon, DH (2012). Error monitoring dysfunction across the illness course of schizophrenia. Journal of Abnormal Psychology 121, 372–387.Google Scholar
Pertusa, A, Fullana, MA, Singh, S, Alonso, P, Menchon, JM, Mataix-Cols, D (2008). Compulsive hoarding: OCD symptom, distinct clinical syndrome, or both? American Journal of Psychiatry 165, 1289–1298.Google Scholar
Pitman, RK (1987). A cybernetic model of obsessive-compulsive psychopathology. Comprehensive Psychiatry 28, 334–343.Google Scholar
Pontifex, MB, Scudder, MR, Brown, ML, O'Leary, KC, Wu, CT, Themanson, JR, Hillman, CH (2010). On the number of trials necessary for stabilization of error-related brain activity across the life span. Psychophysiology 47, 767–773.Google ScholarPubMed
Ridderinkhof, KR, Ullsperger, M, Crone, EA, Nieuwenhuis, S (2004). The role of the medial frontal cortex in cognitive control. Science 306, 443–447.Google Scholar
Riesel, A, Endrass, T, Auerbach, LA, Kathmann, N (2015a). Overactive performance monitoring as an endophenotype for obsessive-compulsive disorder: evidence from a treatment study. American Journal of Psychiatry 172, 665–673.Google Scholar
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, 317–324.CrossRefGoogle ScholarPubMed
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, 707–717.Google Scholar
Riesel, A, Richter, A, Kaufmann, C, Kathmann, N, Endrass, T (2015b). Performance monitoring in obsessive-compulsive undergraduates: effects of task difficulty. Brain and Cognition 98, 35–42.Google Scholar
Riesel, A, Weinberg, A, Endrass, T, Meyer, A, Hajcak, G (2013). The ERN is the ERN is the ERN? Convergent validity of error-related brain activity across different tasks. Biological Psychology 93, 377–385.CrossRefGoogle ScholarPubMed
Rotge, JY, Guehl, D, Dilharreguy, B, Cuny, E, Tignol, J, Bioulac, B, Allard, M, Burbaud, P, Aouizerate, B (2008). Provocation of obsessive-compulsive symptoms: a quantitative voxel-based meta-analysis of functional neuroimaging studies. Journal of Psychiatry Neuroscience 33, 405–412.Google Scholar
Santesso, DL, Segalowitz, SJ (2008). Developmental differences in error-related ERPs in middle- to late-adolescent males. Developmental Psychology 44, 205–217.CrossRefGoogle ScholarPubMed
Santesso, DL, Segalowitz, SJ, Schmidt, LA (2006). Error-related electrocortical responses are enhanced in children with obsessive-compulsive behaviors. Developmental Neuropsychology 29, 431–445.CrossRefGoogle ScholarPubMed
Saxena, S (2007). Is compulsive hoarding a genetically and neurobiologically discrete syndrome? Implications for diagnostic classification. American Journal of Psychiatry 164, 380–384.Google Scholar
Saxena, S, Brody, AL, Maidment, KM, Baxter, LR Jr. (2007). Paroxetine treatment of compulsive hoarding. Journal of Psychiatric Research 41, 481–487.Google Scholar
Saxena, S, Brody, AL, Maidment, KM, Smith, EC, Zohrabi, N, Katz, E, Baker, SK, Baxter, LR Jr. (2004). Cerebral glucose metabolism in obsessive-compulsive hoarding. American Journal of Psychiatry 161, 1038–1048.Google Scholar
Spitzer, RL, Williams, JB, Gibbon, M, First, MB (1992). The Structured Clinical Interview for DSM-III-R (SCID). I: history, rationale, and description. Archives in General Psychiatry 49, 624–629.CrossRefGoogle ScholarPubMed
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 5, 913–920.Google Scholar
Tolin, DF, Frost, RO, Steketee, G (2007). An open trial of cognitive-behavioral therapy for compulsive hoarding. Behavioral Research & Therapy 45, 1461–1470.CrossRefGoogle ScholarPubMed
Tolin, DF, Stevens, MC, Villavicencio, AL, Norberg, MM, Calhoun, VD, Frost, RO, Steketee, G, Rauch, SL, Pearlson, GD (2012). Neural mechanisms of decision making in hoarding disorder. Archives of General Psychiatry 69, 832–841.Google Scholar
Tolin, DF, Witt, ST, Stevens, MC (2014). Hoarding disorder and obsessive-compulsive disorder show different patterns of neural activity during response inhibition. Psychiatry Research 221, 142–148.Google Scholar
Ursu, S, Stenger, VA, Shear, MK, Jones, MR, Carter, CS (2003). Overactive action monitoring in obsessive-compulsive disorder: evidence from functional magnetic resonance imaging. Psychological Science 14, 347–353.Google Scholar
van Veen, V, Carter, CS (2002). The anterior cingulate as a conflict monitor: fMRI and ERP studies. Physiology & Behavior 77, 477–482.Google Scholar
Weinberg, A, Dieterich, R, Riesel, A (2015). Error-related brain activity in the age of RDoC: a review of the literature. International Journal of Psychophysiology. Published online: 4 March 2015. doi: 10.1016/j.ijpsycho.2015.02.029.Google Scholar
Yeung, N, Botvinick, MM, Cohen, JD (2004). The neural basis of error detection: conflict monitoring and the error-related negativity. Psychological Review 111, 931–959.Google Scholar
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