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Differential patterns of brain activation between hoarding disorder and obsessive-compulsive disorder during executive performance

Published online by Cambridge University Press:  25 March 2019

Maria Suñol ,
Ignacio Martínez-Zalacaín ,
Maria Picó-Pérez ,
Clara López-Solà ,
Eva Real ,
Miquel Àngel Fullana ,
Jesús Pujol ,
Narcís Cardoner ,
José Manuel Menchón  and
Pino Alonso
...Show all authors
Maria Suñol
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Ignacio Martínez-Zalacaín
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Maria Picó-Pérez
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Clara López-Solà
Affiliation:
Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Mental Health, Corporació Sanitaria Parc Taulí-i3PT, Sabadell, Spain
Eva Real
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain
Miquel Àngel Fullana
Affiliation:
Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Psychiatry, Hospital Clínic-Institute of Neurosciences, Barcelona, Spain Department of Psychiatry and Legal Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain
Jesús Pujol
Affiliation:
Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain MRI Research Unit, Radiology Department, Hospital del Mar, Barcelona, Spain
Narcís Cardoner
Affiliation:
Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Mental Health, Corporació Sanitaria Parc Taulí-i3PT, Sabadell, Spain Department of Psychiatry and Legal Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain
José Manuel Menchón
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Pino Alonso
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Clinical Sciences, School of Medicine, University of Barcelona, Barcelona, Spain
Carles Soriano-Mas*
Affiliation:
Department of Psychiatry, Bellvitge University Hospital, Bellvitge Biomedical Research Institute – IDIBELL, Barcelona, Spain Carlos III Health Institute, Centro de Investigación Biomedica en Red de Salud Mental – CIBERSAM, Barcelona, Spain Department of Psychobiology and Methodology of Health Sciences, Universitat Autònoma de Barcelona, Barcelona, Spain
*
Author for correspondence: Carles Soriano-Mas, E-mail: [email protected]
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Abstract

Background

Preliminary evidence suggests that hoarding disorder (HD) and obsessive-compulsive disorder (OCD) may show distinct patterns of brain activation during executive performance, although results have been inconclusive regarding the specific neural correlates of their differential executive dysfunction. In the current study, we aim to evaluate differences in brain activation between patients with HD, OCD and healthy controls (HCs) during response inhibition, response switching and error processing.

Methods

We assessed 17 patients with HD, 18 patients with OCD and 19 HCs. Executive processing was assessed inside a magnetic resonance scanner by means of two variants of a cognitive control protocol (i.e. stop- and switch-signal tasks), which allowed for the assessment of the aforementioned executive domains.

Results

OCD patients performed similar to the HCs, differing only in the number of successful go trials in the switch-signal task. However, they showed an anomalous hyperactivation of the right rostral anterior cingulate cortex during error processing in the switch-signal task. Conversely, HD patients performed worse than OCD and HC participants in both tasks, showing an impulsive-like pattern of response (i.e. shorter reaction time and more commission errors). They also exhibited hyperactivation of the right lateral orbitofrontal cortex during successful response switching and abnormal deactivation of frontal regions during error processing in both tasks.

Conclusions

Our results support that patients with HD and OCD present dissimilar cognitive profiles, supported by distinct neural mechanisms. Specifically, while alterations in HD resemble an impulsive pattern of response, patients with OCD present increased error processing during response conflict protocols.

Keywords

Brain activationexecutive functionhoarding disorderneuroimagingobsessive-compulsive disorder
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 4 , March 2020 , pp. 666 - 673
Copyright
Copyright © Cambridge University Press 2019

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References

American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders, 5th Edn. Arlington, VA: American Psychiatric Publishing.Google Scholar
An, SK, Mataix-Cols, D, Lawrence, NS, Wooderson, S, Giampietro, V, Speckens, A, Brammer, MJ and Phillips, ML (2009) To discard or not to discard: the neural basis of hoarding symptoms in obsessive-compulsive disorder. Molecular Psychiatry 14, 318–331.CrossRefGoogle ScholarPubMed
Blom, RM, Samuels, JF, Grados, MA, Chen, Y, Bienvenu, OJ, Riddle, MA, Liang, KY, Brandt, J and Nestadt, G (2011) Cognitive functioning in compulsive hoarding. Journal of Anxiety Disorders 25, 1139–1144.CrossRefGoogle ScholarPubMed
Chamberlain, SR and Menzies, L (2009) Endophenotypes of obsessive-compulsive disorder: rationale, evidence and future potential. Expert Review of Neurotherapeutics 9, 1133–1146.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M and Williams, JBW (1996) Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). Washington, DC: American Psychiatric Press.Google Scholar
Foa, EB, Huppert, JD, Leiberg, S, Langner, R, Kichic, R, Hajcak, G and Salkovskis, PM (2002) The obsessive-compulsive inventory: development and validation of a short version. Psychological Assessment 14, 485–496.CrossRefGoogle ScholarPubMed
Frost, RO, Steketee, G and Grisham, J (2004) Measurement of compulsive hoarding: saving inventory-revised. Behaviour Research and Therapy 42, 1163–1182.CrossRefGoogle ScholarPubMed
Frost, RO, Steketee, G and Tolin, DF (2012) Diagnosis and assessment of hoarding disorder. Annual Review of Clinical Psychology 8, 219–242.CrossRefGoogle ScholarPubMed
Fullana, MA, Tortella-Feliu, M, Caseras, X, Andión, Ó, Torrubia, R and Mataix-Cols, D (2005) Psychometric properties of the Spanish version of the Obsessive-Compulsive Inventory-Revised in a non-clinical sample. Journal of Anxiety Disorders 19, 893–903.CrossRefGoogle Scholar
Goodman, WK, Price, LH, Rasmussen, SA, Mazure, C, Fleischmann, RL and Hill, CL (1989) The Yale-Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 1006–1111.CrossRefGoogle ScholarPubMed
Grisham, JR and Baldwin, PA (2015) Neuropsychological and neurophysiological insights into hoarding disorder. Neuropsychiatric Disease and Treatment 11, 951–962.CrossRefGoogle ScholarPubMed
Harkin, B, Miellet, S and Kessler, K (2012) What checkers actually check: an eye tracking study of inhibitory control and working memory. PLoS ONE 7, 1–11.CrossRefGoogle ScholarPubMed
Harrison, BJ, Pujol, J, Cardoner, N, Deus, J, Alonso, P, López-Solà, M, Contreras-Rodríguez, O, Real, E, Segalàs, C, Blanco-Hinojo, L, Menchon, JM and Soriano-Mas, C (2013) Brain corticostriatal systems and the major clinical symptom dimensions of obsessive-compulsive disorder. Biological Psychiatry 73, 321–328.CrossRefGoogle ScholarPubMed
Hedden, T and Gabrieli, JDE (2010) Shared and selective neural correlates of inhibition, facilitation, and shifting processes during executive control. Brain and Language 51, 421–431.Google ScholarPubMed
Hoffmann, S and Beste, C (2015) A perspective on neural and cognitive mechanisms of error commission. Frontiers in Behavioral Neuroscience 9, 1–16.CrossRefGoogle ScholarPubMed
Hough, CM, Luks, TL, Lai, K, Vigil, O, Guillory, S, Nongpiur, A, Fekri, SM, Kupferman, E, Mathalon, DH and Mathews, CA (2016) Comparison of brain activation patterns during executive function tasks in hoarding disorder and non-hoarding OCD. Psychiatry Research-Neuroimaging 255, 50–59.CrossRefGoogle ScholarPubMed
Kringelbach, ML and Rolls, ET (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress in Neurobiology 72, 341–372.CrossRefGoogle ScholarPubMed
Maltby, N, Tolin, DF, Worhunsky, P, O'Keefe, TM and Kiehl, KA (2005) Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder: an event-related fMRI study. NeuroImage 24, 495–503.CrossRefGoogle Scholar
Mataix-Cols, D, Wooderson, S, Lawrence, N, Brammer, MJ, Speckens, A and Phillips, ML (2004) Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Archives of General Psychiatry 61, 564–576.CrossRefGoogle ScholarPubMed
Mathews, CA, Perez, VB, Roach, BJ, Fekri, S, Vigil, O, Kupferman, E and Mathalon, DH (2016) Error-related brain activity dissociates hoarding disorder from obsessive-compulsive disorder. Psychological Medicine 46, 367–379.CrossRefGoogle ScholarPubMed
McClure, EB, Treland, JE, Snow, J, Schmajuk, M, Dickstein, DP, Towbin, KE, Charney, DS, Pine, DS and Leibenluft, E (2005) Deficits in social cognition and response flexibility in pediatric bipolar disorder. American Journal of Psychiatry 162, 1644–1651.CrossRefGoogle ScholarPubMed
Melcher, T, Falkai, P and Gruber, O (2008) Functional brain abnormalities in psychiatric disorders: neural mechanisms to detect and resolve cognitive conflict and interference. Brain Research Reviews 59, 96–124.CrossRefGoogle ScholarPubMed
Menzies, L, Chamberlain, SR, Laird, AR, Thelen, SM, Sahakian, BJ and Bullmore, ET (2008) Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neuroscience and Biobehavioral Reviews 32, 525–549.CrossRefGoogle ScholarPubMed
Nichols, TE and Holmes, AP (2002) Non parametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping 15, 1–25.CrossRefGoogle ScholarPubMed
Nordsletten, AE, de la Cruz, LF, Pertusa, A, Reichenberg, A, Hatch, SL and Mataix-Cols, D (2013) The Structured Interview for Hoarding Disorder (SIHD): development, usage and further validation. Journal of Obsessive Compulsive and Related Disorders 2, 346–350.CrossRefGoogle Scholar
Norman, LJ, Carlisi, C, Lukito, S, Hart, H, Mataix-Cols, D, Radua, J and Rubia, K (2016) Structural and functional brain abnormalities in attention-deficit/hyperactivity disorder and obsessive-compulsive disorder: a comparative meta-analysis. JAMA Psychiatry 73, 815–825.CrossRefGoogle ScholarPubMed
Norman, LJ, Taylor, SF, Liu, Y, Radua, J, Chye, Y, De Wit, SJ, Huyser, C, Karahanoglu, FI, Luks, T, Manoach, D, Mathews, C, Rubia, K, Suo, C, van den Heuvel, OA, Yücel, M and Fitzgerald, K (2018) Error processing and inhibitory control in obsessive-compulsive disorder: a meta-analysis using statistical parametric maps. Biological Psychiatry. pii: S0006-3223 (18)32022-5. ISSN 0006-3223. (https://doi.org/10.1016/j.biopsych.2018.11.010) Accessed 13 March 2019. [Epub ahead of print].Google ScholarPubMed
Pertusa, A, Frost, RO and Mataix-Cols, D (2010) When hoarding is a symptom of OCD: a case series and implications for DSM-V. Behaviour Research and Therapy 48, 1012–1020.CrossRefGoogle ScholarPubMed
Sal y Rosas, HJ, Vega-Dienstmaier, JM, Mazzotti, G, Vidal, H, Guimas, B, Adrianzén, C and Vivar, R (2002) Validación de una versión en español de la Escala Yale-Brown para el Trastorno Obsesivo-Compulsivo. Actas Españolas de Psiquiatría 30, 30–35.Google Scholar
Saxena, S, Brody, AL, Maidment, KM, Smith, EC, Zohrabi, N, Katz, E, Baker, SK and Baxter, LR (2004) Cerebral glucose metabolism in obsessive-compulsive hoarding. American Journal of Psychiatry 161, 1038–1048.CrossRefGoogle ScholarPubMed
Shin, NY, Lee, TY, Kim, E and Kwon, JS (2014) Cognitive functioning in obsessive-compulsive disorder: a meta-analysis. Psychological Medicine 44, 1121–1130.CrossRefGoogle ScholarPubMed
Smith, SM and Nichols, TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage 44, 83–98.CrossRefGoogle ScholarPubMed
Snyder, HR, Kaiser, RH, Warren, SL, Heller, W, Hall, F and Hospital, M (2015) Obsessive-compulsive disorder is associated with broad impairments in executive function: a meta-analysis. Clinical Psychological Science 3, 301–330.CrossRefGoogle ScholarPubMed
Stalnaker, TA, Cooch, NK and Schoenbaum, G (2015) What the orbitofrontal cortex does not do. Nature Neuroscience 18, 620–627.CrossRefGoogle ScholarPubMed
Taylor, SF, Stern, ER and Gehring, WJ (2007) Neural systems for error monitoring: recent findings and theoretical perspectives. The Neuroscientist 13, 160–172.CrossRefGoogle ScholarPubMed
Timpano, KR, Rasmussen, J, Exner, C, Rief, W, Schmidt, NB and Wilhelm, S (2013) Hoarding and the multi-faceted construct of impulsivity: a cross-cultural investigation. Journal of Psychiatric Research 47, 363–370.CrossRefGoogle ScholarPubMed
Tolin, DF, Frost, RO, Steketee, G and Fitch, KE (2008) Family burden of compulsive hoarding: results of an internet survey. Behaviour Research and Therapy 46, 334–344.CrossRefGoogle ScholarPubMed
Tolin, DF, Kiehl, KA, Worhunsky, P, Book, GA and Maltby, N (2009) An exploratory study of the neural mechanisms of decision making in compulsive hoarding. Psychological Medicine 39, 325–336.CrossRefGoogle ScholarPubMed
Tolin, DF, Stevens, MC, Villavicencio, AL, Norberg, MM, Calhoun, VD, Frost, RO, Steketee, G, Rauch, SL and Pearlson, GD (2012) Neural mechanisms of decision making in hoarding disorder. Archives of General Psychiatry 69, 832–841.CrossRefGoogle ScholarPubMed
Tolin, DF, Witt, ST and Stevens, MC (2014) Hoarding disorder and obsessive-compulsive disorder show different patterns of neural activity during response inhibition. Psychiatry Research-Neuroimaging 221, 142–148.CrossRefGoogle ScholarPubMed
Tortella-Feliu, M, Fullana, MA, Caseras, X, Andión, Ó, Torrubia, R and Mataix-Cols, D (2006) Spanish version of the savings inventory-revised: adaptation, psychometric properties, and relationship to personality variables. Behavior Modification 30, 693–712.CrossRefGoogle ScholarPubMed
Ursu, S, Stenger, VA, Shear, MK, Jones, MR, Carter, CS, Katherine Shear, M, Jones, MR, Carter, CS, Shear, MK, Jones, MR and Carter, CS (2003) Obsessive-compulsive disorder: evidence from functional magnetic resonance imaging. Psychological Science 14, 347–353.CrossRefGoogle ScholarPubMed
van den Heuvel, OA, van Wingen, G, Soriano-Mas, C, Alonso, P, Chamberlain, SR, Nakamae, T, Denys, D, Goudriaan, AE and Veltman, DJ (2016) Brain circuitry of compulsivity. European Neuropsychopharmacology 26, 810–827.CrossRefGoogle ScholarPubMed
Wu, KD and Watson, D (2005) Hoarding and its relation to obsessive-compulsive disorder. Behaviour Research and Therapy 43, 897–921.CrossRefGoogle ScholarPubMed
Yücel, M, Harrison, B, Wood, S, Fornito, A, Wellard, R, Pujol, J, Clarke, K, Phillips, M, Kyrios, M, Velakoulis, D and Pantelis, C (2007) Functional and biochemical alterations of the medial frontal cortex in obsessive-compulsive disorder. Archives of General Psychiatry 64, 946–955.CrossRefGoogle ScholarPubMed
Zhang, R, Geng, X and Lee, TMC (2017) Large-scale functional neural network correlates of response inhibition: an fMRI meta-analysis. Brain Structure and Function 222, 3973–3990.CrossRefGoogle ScholarPubMed
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