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An exploratory study of the neural mechanisms of decision making in compulsive hoarding

Published online by Cambridge University Press:  19 May 2008

D. F. Tolin ,
K. A. Kiehl ,
P. Worhunsky ,
G. A. Book  and
N. Maltby
D. F. Tolin*
Affiliation:
The Institute of Living/Hartford Hospital, Hartford, CT, USA Yale University School of Medicine, New Haven, CT, USA
K. A. Kiehl
Affiliation:
MIND Institute and University of New Mexico, NM, USA
P. Worhunsky
Affiliation:
The Institute of Living/Hartford Hospital, Hartford, CT, USA
G. A. Book
Affiliation:
The Institute of Living/Hartford Hospital, Hartford, CT, USA
N. Maltby
Affiliation:
The Institute of Living/Hartford Hospital, Hartford, CT, USA
*
*Address for correspondence: D. F. Tolin, Ph.D., Anxiety Disorders Center, The Institute of Living/Hartford Hospital, 200 Retreat Avenue, Hartford, CT 06106, USA. (Email: [email protected])
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Abstract

Background

Prior studies have suggested unique patterns of neural activity associated with compulsive hoarding. However, to date no studies have examined the process of making actual decisions about whether to keep or discard possessions in patients with hoarding symptoms. An increasing body of clinical data and experimental psychopathology research suggests that hoarding is associated with impaired decision making; therefore, it is important to understand the neural underpinnings of decision-making abnormalities in hoarding patients.

Method

Twelve adult patients diagnosed with compulsive hoarding, 17% of whom also met criteria for obsessive–compulsive disorder (OCD), and 12 matched healthy controls underwent functional magnetic resonance imaging (fMRI) while making decisions about whether or not to discard personal paper items (e.g. junk mail) brought to the laboratory as well as control items that did not belong to them. Items were either saved or destroyed following each decision.

Results

When deciding about whether to keep or discard personal possessions, compulsive hoarding participants displayed excessive hemodynamic activity in lateral orbitofrontal cortex and parahippocampal gyrus. Among hoarding participants, decisions to keep personal possessions were associated with greater activity in superior temporal gyrus, middle temporal gyrus, medial frontal gyrus, anterior cingulate cortex, precentral gyrus, and cerebellum than were decisions to discard personal possessions.

Conclusions

These results provide partial support for an emerging model of compulsive hoarding based on complications of the decision-making process. They also suggest that compulsive hoarding may be characterized by focal deficits in the processing of reward and changes in reward contingencies, particularly when these are perceived to be punishing.

Keywords

Decision-makingfMRIhoardingobsessive–compulsive disorder
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 2 , February 2009 , pp. 325 - 336
Copyright
Copyright © 2008 Cambridge University Press

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References

Abramowitz, JS, Franklin, ME, Schwartz, SA, Furr, JM (2003). Symptom presentation and outcome of cognitive-behavioral therapy for obsessive-compulsive disorder. Journal of Consulting and Clinical Psychology 71, 1049–1057.CrossRefGoogle ScholarPubMed
Allman, JM, Hakeem, A, Erwin, JM, Nimchinsky, E, Hof, P (2001). The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Annals of the New York Academy of Sciences 935, 107–117.CrossRefGoogle ScholarPubMed
Anderson, SW, Damasio, H, Damasio, AR (2005). A neural basis for collecting behaviour in humans. Brain 128, 201–212.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, AR, Damasio, H, Anderson, SW (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, H, Tranel, D, Damasio, AR (1997). Deciding advantageously before knowing the advantageous strategy. Science 275, 1293–1295.CrossRefGoogle ScholarPubMed
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Science 4, 215–222.CrossRefGoogle ScholarPubMed
Calamari, JE, Wiegartz, PS, Riemann, BC, Cohen, RJ, Greer, A, Jacobi, DM, Jahn, SC, Carmin, C (2004). Obsessive-compulsive disorder subtypes: an attempted replication and extension of a symptom-based taxonomy. Behaviour Research and Therapy 42, 647–670.CrossRefGoogle ScholarPubMed
Carter, CS, Braver, TS, Barch, DM, Botvinick, M, Noll, D, Cohen, J (1998). Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280, 747–749.CrossRefGoogle ScholarPubMed
de Brabander, JM, de Bruin, JP, van Eden, CG (1991). Comparison of the effects of neonatal and adult medial prefrontal cortex lesions on food hoarding and spatial delayed alternation. Behavioral Brain Research 42, 67–75.CrossRefGoogle ScholarPubMed
Devinsky, O, Morrell, MJ, Vogt, BA (1995). Contributions of anterior cingulate cortex to behaviour. Brain 118, 279–306.CrossRefGoogle ScholarPubMed
du Boisgueheneuc, F, Levy, R, Volle, E, Seassau, M, Duffau, H, Kinkingnehun, S, Samson, Y, Zhang, S, Dubois, B (2006). Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129, 3315–3328.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1995). Structured Clinical Interview for DSM-IV Axis I Disorders – Patient Edition (SCID-I/P, version 2.0). Biometrics Research Department: New York.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (1997). Structured Clinical Interview for DSM-IV Personality Disorders (SCID-II). American Psychiatric Press, Inc.: Washington, DC.Google Scholar
Fitch, KE, Tolin, DF, Frost, RO, Steketee, G (2007). Compulsive hoarding: assessing insight. Presented at the Annual Meeting of the Association of Behavioral and Cognitive Therapies, Philadelphia, November, 2007.Google Scholar
Freire, L, Mangin, JF (2001). Motion correction algorithms may create spurious brain activations in the absence of subject motion. NeuroImage 14, 709–722.CrossRefGoogle ScholarPubMed
Freire, L, Roche, A, Mangin, JF (2002). What is the best similarity measure for motion correction in fMRI time series? IEEE Transactions on Medical Imaging 21, 470–484.CrossRefGoogle ScholarPubMed
Friston, KJ, Ashburner, J, Frith, CD, Poline, J-B, Heather, JD, Frackowiak, RSJ (1995). Spatial registration and normalization of images. Human Brain Mapping 2, 165–189.CrossRefGoogle Scholar
Frost, RO, Hartl, TL (1996). A cognitive-behavioral model of compulsive hoarding. Behaviour Research and Therapy 34, 341–350.CrossRefGoogle ScholarPubMed
Frost, RO, Kim, HJ, Morris, C, Bloss, C, Murray-Close, M, Steketee, G (1998). Hoarding, compulsive buying and reasons for saving. Behaviour Research and Therapy 36, 657–664.CrossRefGoogle ScholarPubMed
Frost, RO, Steketee, G, Grisham, J (2004). Measurement of compulsive hoarding: Saving Inventory – Revised. Behaviour Research and Therapy 42, 1163–1182.CrossRefGoogle ScholarPubMed
Frost, RO, Steketee, G, Tolin, DF, Brown, TA (2006). Comorbidity and diagnostic issues in compulsive hoarding. Presented to the Annual Meeting of the Anxiety Disorders Association of America, Miami, Florida, March 2006.Google Scholar
Frost, RO, Steketee, G, Williams, LF, Warren, R (2000). Mood, personality disorder symptoms and disability in obsessive compulsive hoarders: a comparison with clinical and nonclinical controls. Behaviour Research and Therapy 38, 1071–1081.CrossRefGoogle ScholarPubMed
Frost, RO, Tolin, DF (2008). Compulsive hoarding. In Clinical Handbook of Obsessive-Compulsive Disorder and Related Problems (ed.Taylor, S., Abramowitz and, J. S.McKay, D.), pp. 76–94. Johns Hopkins University Press: Baltimore.Google Scholar
Goldberg, II, Harel, M, Malach, R (2006). When the brain loses its self: prefrontal inactivation during sensorimotor processing. Neuron 50, 329–339.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.CrossRefGoogle ScholarPubMed
Grant, JE, Odlaug, BL, Wozniak, JR (2007). Neuropsychological functioning in kleptomania. Behaviour Research and Therapy 45, 1663–1670.CrossRefGoogle ScholarPubMed
Grisham, JR, Brown, TA, Savage, CR, Steketee, G, Barlow, DH (2007). Neuropsychological impairment associated with compulsive hoarding. Behaviour Research and Therapy 45, 1471–1483.CrossRefGoogle ScholarPubMed
Gur, RC, Ragland, JD, Mozley, LH, Mozley, PD, Smith, R, Alavi, A, Bilker, W, Gur, RE (1997). Lateralized changes in regional cerebral blood flow during performance of verbal and facial recognition tasks: correlations with performance and ‘effort’. Brain and Cognition 33, 388–414.CrossRefGoogle ScholarPubMed
Guy, W (1976). Assessment Manual for Psychopharmacology. U.S. Government Printing Office: Washington, DC.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurological and Neurosurgical Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Kiehl, KA, Liddle, PF, Hopfinger, JB (2000). Error processing and the rostral anterior cingulate: an event-related fMRI study. Psychophysiology 37, 216–223.CrossRefGoogle ScholarPubMed
Kolb, B (1977). Studies on the caudate-putamen and the dorsomedial thalamic nucleus of the rat: implications for mammalian frontal-lobe functions. Physiology and Behavior 18, 237–244.CrossRefGoogle ScholarPubMed
Kringelbach, ML (2005). The human orbitofrontal cortex: linking reward to hedonic experience. Nature Reviews Neuroscience 6, 691–702.CrossRefGoogle ScholarPubMed
Kringelbach, ML, Rolls, ET (2004). The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress in Neurobiology 72, 341–372.CrossRefGoogle ScholarPubMed
Lane, RD, Reiman, EM, Bradley, MM, Lang, PJ, Ahern, GL, Davidson, RJ, Schwartz, GE (1997). Neuroanatomical correlates of pleasant and unpleasant emotion. Neuropsychologia 35, 1437–1444.CrossRefGoogle ScholarPubMed
Lawrence, NS, Wooderson, S, Mataix-Cols, D, David, R, Speckens, A, Phillips, ML (2006). Decision making and set shifting impairments are associated with distinct symptom dimensions in obsessive-compulsive disorder. Neuropsychology 20, 409–419.CrossRefGoogle ScholarPubMed
Luchian, SA, McNally, RJ, Hooley, JM (2007). Cognitive aspects of nonclinical obsessive-compulsive hoarding. Behaviour Research and Therapy 45, 1657–1662.CrossRefGoogle ScholarPubMed
Maguire, EA, Mummery, CJ (1999). Differential modulation of a common memory retrieval network revealed by positron emission tomography. Hippocampus 9, 54–61.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mataix-Cols, D, Cullen, S, Lange, K, Zelaya, F, Andrew, C, Amaro, E, Brammer, MJ, Williams, SC, Speckens, A, Phillips, ML (2003). Neural correlates of anxiety associated with obsessive-compulsive symptom dimensions in normal volunteers. Biological Psychiatry 53, 482–493.CrossRefGoogle ScholarPubMed
Mataix-Cols, D, Marks, IM, Greist, JH, Kobak, KA, Baer, L (2002). Obsessive-compulsive symptom dimensions as predictors of compliance with and response to behaviour therapy: results from a controlled trial. Psychotherapy and Psychosomatics 71, 255–262.CrossRefGoogle ScholarPubMed
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, 564–576.CrossRefGoogle ScholarPubMed
Meunier, SA, Tolin, DF, Frost, RO, Steketee, G, Brady, RE (2006). Prevalence of hoarding symptoms across the anxiety disorders. Presented to the Annual Meeting of the Anxiety Disorders Association of America, Miami, FL, March 2006.Google Scholar
Mogenson, GJ, Wu, M (1988). Disruption of food hoarding by injections of procaine into mediodorsal thalamus, GABA into subpallidal region and haloperidol into accumbens. Brain Research Bulletin 20, 247–251.CrossRefGoogle ScholarPubMed
Northoff, G, Grimm, S, Boeker, H, Schmidt, C, Bermpohl, F, Heinzel, A, Hell, D, Boesiger, P (2006). Affective judgment and beneficial decision making: ventromedial prefrontal activity correlates with performance in the Iowa Gambling Task. Human Brain Mapping 27, 572–587.CrossRefGoogle ScholarPubMed
Polli, FE, Barton, JJ, Cain, MS, Thakkar, KN, Rauch, SL, Manoach, DS (2005). Rostral and dorsal anterior cingulate cortex make dissociable contributions during antisaccade error commission. Proceedings of the National Academy of Sciences of the United States of America 102, 15700–15705.CrossRefGoogle ScholarPubMed
Rolls, ET (2004). The functions of the orbitofrontal cortex. Brain and Cognition 55, 11–29.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Steketee, G, Frost, RO (2003). Compulsive hoarding: current status of the research. Clinical Psychology Review 23, 905–927.CrossRefGoogle ScholarPubMed
Steketee, G, Frost, RO, Kim, HJ (2001). Hoarding by elderly people. Health and Social Work 26, 176–184.Google Scholar
Steketee, G, Frost, RO, Kyrios, M (2003). Beliefs about possessions among compulsive hoarders. Cognitive Therapy and Research 27, 467–479.CrossRefGoogle Scholar
Tolin, DF, Brady, RE, Hannan, SE (2008). Obsessional beliefs and symptoms of obsessive-compulsive disorder in a clinical sample. Journal of Psychopathology and Behavioral Assessment 30, 31–42.CrossRefGoogle Scholar
Tolin, DF, Frost, RO, Steketee, G, Gray, KD, Fitch, KE (2007). The economic and social burden of compulsive hoarding. Psychiatry Research. doi: 10.1016/j.psychres.2007.08.008.Google Scholar
Wincze, JP, Steketee, G, Frost, RO (2007). Categorization in compulsive hoarding. Behaviour Research and Therapy 45, 63–72.CrossRefGoogle ScholarPubMed
Wu, KD, Watson, D (2005). Hoarding and its relation to obsessive-compulsive disorder. Behaviour Research and Therapy 43, 897–921.CrossRefGoogle ScholarPubMed
Yonelinas, AP, Hopfinger, JB, Buonocore, MH, Kroll, NE, Baynes, K (2001). Hippocampal, parahippocampal and occipital-temporal contributions to associative and item recognition memory: an fMRI study. Neuroreport 12, 359–363.CrossRefGoogle ScholarPubMed