Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

To discard or not to discard: the neural basis of hoarding symptoms in obsessive-compulsive disorder

Abstract

Preliminary neuroimaging studies suggest that patients with the ‘compulsive hoarding syndrome’ may be a neurobiologically distinct variant of obsessive-compulsive disorder (OCD) but further research is needed. A total of 29 OCD patients (13 with and 16 without prominent hoarding symptoms) and 21 healthy controls of both sexes participated in two functional magnetic resonance imaging experiments consisting of the provocation of hoarding-related and symptom-unrelated (aversive control) anxiety. In response to the hoarding-related (but not symptom-unrelated) anxiety provocation, OCD patients with prominent hoarding symptoms showed greater activation in bilateral anterior ventromedial prefrontal cortex (VMPFC) than patients without hoarding symptoms and healthy controls. In the entire patient group (n=29), provoked anxiety was positively correlated with activation in a frontolimbic network that included the anterior VMPFC, medial temporal structures, thalamus and sensorimotor cortex. Negative correlations were observed in the left dorsal anterior cingulate gyrus, bilateral temporal cortex, bilateral dorsolateral/medial prefrontal regions, basal ganglia and parieto-occipital regions. These results were independent from the effects of age, sex, level of education, state anxiety, depression, comorbidity and use of medication. The findings are consistent with the animal and lesion literature and several landmark clinical features of compulsive hoarding, particularly decision-making difficulties. Whether the results are generalizable to hoarders who do not meet criteria for OCD remains to be investigated.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Steketee G, Frost R . Compulsive hoarding: current status of the research. Clin Psychol Rev 2003; 23: 905–927.

    Article  Google Scholar 

  2. Mataix-Cols D, Rosario-Campos MC, Leckman JF . A multidimensional model of obsessive-compulsive disorder. Am J Psychiatry 2005; 162: 228–238.

    Article  Google Scholar 

  3. Samuels JF, Bienvenu III OJ, Pinto A, Fyer AJ, McCracken JT, Rauch SL et al. Hoarding in obsessive-compulsive disorder: resulting from the OCD collaborative genetics study. Behav Res Ther 2006; 45: 673–686.

    Article  Google Scholar 

  4. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR . Impairment of social and moral behavior related to early damage in the human prefrontal cortex. Nat Neurosci 1999; 2: 1032–1037.

    Article  CAS  Google Scholar 

  5. Cohen L, Angladette L, Benoit N, Pierrot-Deseilligny C . A man who borrowed cars. Lancet 1999; 353: 34.

    Article  CAS  Google Scholar 

  6. Hahm DS, Kang Y, Cheong SS, Na DL . A compulsive collecting behavior following an A-com aneurysm rupture. Neurology 2001; 56: 398–400.

    Article  CAS  Google Scholar 

  7. Ogai M, Iyo M, Mori N, Takei N . A right orbitofrontal region and OCD symptoms: a case report. Acta Psychiatr Scand 2005; 111: 74–77.

    Article  CAS  Google Scholar 

  8. Volle E, Beato R, Levy R, Dubois B . Forced collection after orbitofrontal damage. Neurology 2002; 58: 488–490.

    Article  CAS  Google Scholar 

  9. Anderson SW, Damasio H, Damasio AR . A neural basis for collecting behaviour in humans. Brain 2005; 128: 201–212.

    Article  Google Scholar 

  10. Blundell JE, Herberg LJ . Effectiveness of lateral hypothalamic stimulation, arousal, and food deprivation in the initiation of food hoarding behavior in naïve rats. Physiol Behav 1977; 18: 237–244.

    Article  Google Scholar 

  11. Kolb B . Studies on the caudate-putamen and dorsomedial thalamic nucleus of the rat: implications for mammalian frontal-lobe functions. Physiol Behav 1977; 18: 237–244.

    Article  CAS  Google Scholar 

  12. Stern CE, Passingham RE . The nucleus accumbens in monkeys (Macaca fascicularis): I. The organization of behavior. Behav Brain Res 1994; 61: 9–21.

    Article  CAS  Google Scholar 

  13. Mataix-Cols D, Cullen S, Lange K, Zelaya F, Andrew C, Amaro E et al. Neural correlates of anxiety associated with obsessive-compulsive symptom dimensions in normal volunteers. Biol Psychiatry 2003; 53: 482–493.

    Article  Google Scholar 

  14. Saxena S, Brody AL, Maidment KM, Smith EC, Zohrabi N, Katz E et al. Cerebral glucose metabolism in obsessive-compulsive hoarding. Am J Psychiatry 2004; 161: 1038–1048.

    Article  Google Scholar 

  15. Mataix-Cols D, Wooderson S, Lawrence N, Brammer MJ, Speckens A, Phillips ML . Distinct neural correlates of washing, checking and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry 2004; 164: 564–576.

    Article  Google Scholar 

  16. Goodman WK, Price LH, Rasmussen SA, Mazure C, Delgado P, Heninger GR et al. The Yale-Brown Obsessive Compulsive Scale (Y-BOCS). Part I: development, use and reliability. Arch Gen Psychiatry 1989; 46: 1006–1011.

    Article  CAS  Google Scholar 

  17. Frost RO, Steketee G, Grisham J . Measurement of compulsive hoarding: saving inventory-revised. Behav Res Ther 2004; 42: 31163–31182.

    Article  Google Scholar 

  18. Lawrence NS, Wooderson S, Mataix-Cols D, David R, Speckens A, Phillips ML . Decision making and set shifting impairments are associated with distinct symptom dimensions in obsessive-compulsive disorder. Neuropsychology 2006; 20: 409–419.

    Article  Google Scholar 

  19. Frost RO, Hartl T . A cognitive-behavioral model of compulsive hoarding. Behav Res Ther 1996; 34: 341–350.

    Article  CAS  Google Scholar 

  20. Mataix-Cols D, Lawrence NS, Wooderson S, Speckens A, Phillips ML . The Maudsley Obsessive-Compulsive Stimuli Set (MOCSS): validation of a standardized paradigm for symptom-specific provocation in obsessive-compulsive disorder (OCD). Submitted.

  21. First MB, Spitzer RL, Gibbon M, Williams JBW . Structured Clinical Interview for DSM-IV Axis I Disorders—Patient Edition. Biometrics Research Department of the New York State Psychiatric Institute: New York, 1995.

    Google Scholar 

  22. First MB, Gibbon M, Spitzer RL, Williams JBW, Smith Benjamin L . Structured Clinical Interview for DSM-IV Axis II Disorders—Patient Edition. Biometrics Research Department of the New York State Psychiatric Institute: New York, 1995.

    Google Scholar 

  23. Tortella-Feliu M, Fullana MA, Caseras X, Andion O, Torrubia R, Mataix-Cols D . Spanish version of the saving inventory-revised: adaptation, psychometric properties, and relationship to personality variables. Behav Modif 2006; 30: 693–712.

    Article  Google Scholar 

  24. Foa EB, Huppert JD, Leiberg S, Langner R, Kichic R, Hajcak G et al. The obsessive-compulsive inventory: development and validation of a short version. Psychol Assess 2002; 14: 485–496.

    Article  Google Scholar 

  25. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J . An inventory for measuring depression. Arch Gen Psychiatry 1961; 4: 561–571.

    Article  CAS  Google Scholar 

  26. Spielberger CD . Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press: Palo Alto, 1983.

    Google Scholar 

  27. Marks DF . Bibliography of research utilizing the Vividness of Visual Imagery Questionnaire. Percept Mot Skills 1989; 69: 707–718.

    Article  CAS  Google Scholar 

  28. Cromer KR, Schmidt NB, Murphy DL . Do traumatic events influence the clinical expression of compulsive hoarding? Behav Res Ther 2007; 45: 2581–2592.

    Article  Google Scholar 

  29. Lang PJ, Bradley MM, Cuthbert BN . International Affective Picture System (IAPS). NIMH Center for Study of Emotion and Attention: New York, 1997.

    Google Scholar 

  30. Ogawa S, Lee TM, Kay AR, Tank DW . Brain magnetic resonance imaging with contrast dependent blood oxygenation. Proc Natl Acad Sci USA 1990; 87: 8868–8872.

    Article  Google Scholar 

  31. Bullmore ET, Brammer M, Rabe-Hesketh S, Curtis V, Morris R, Williams SCR et al. Methods for the diagnosis and treatment of stimulus correlated motion in generic brain activation studies using fMRI. Hum Brain Mapp 1999; 7: 38–48.

    Article  CAS  Google Scholar 

  32. Friman O, Borga M, Lundberg P, Knutsson H . Adaptive analysis of fMRI data. Neuroimage 2003; 19: 837–845.

    Article  Google Scholar 

  33. Bullmore ET, Long C, Suckling J, Fadili J, Calvert GA, Zelaya F et al. Coloured noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum Brain Mapp 2001; 12: 61–78.

    Article  CAS  Google Scholar 

  34. Talairach J, Tournoux P . Co-planar Stereotactic Atlas of the Human Brain. Thieme: Stuttgart, 1988.

    Google Scholar 

  35. Brammer M, Bullmore ET, Simmons A, Williams SCR, Grasby PM, Howard RJ et al. Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magn Reson Imaging 1997; 15: 763–770.

    Article  CAS  Google Scholar 

  36. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ . Global, voxel and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 1999; 18: 32–42.

    Article  CAS  Google Scholar 

  37. Rorden C, Brett M . Stereotaxic display of brain lesions. Behavioural Neurology 2000; 12: 191–200.

    Article  Google Scholar 

  38. Bechara A, Damasio AR . The somatic marker hypothesis: a neural theory of economic decision. Game Econ Behav 2005; 52: 336–372.

    Article  Google Scholar 

  39. Bechara A, Damasio AR, Damasio H, Anderson SW . Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 1994; 50: 7–15.

    Article  CAS  Google Scholar 

  40. Bechara A, Tranel D, Damasio H . Characterization of the decision-making deficit of patients with ventro-medial prefrontal cortex lesion. Brain 2000; 123: 2189–2202.

    Article  Google Scholar 

  41. Fukui T, Murai T, Fukuyama H, Hayashi T, Hanakawa T . Functional activity related to risk anticipation during performance of the Iowa Gambling Task. Neuroimage 2005; 24: 253–259.

    Article  Google Scholar 

  42. Northoff G, Grimm S, Boeker H, Schmidt C, Bermpohl F, Heinzel A et al. Affective judgment and beneficial decision making: ventromedial prefrontal activity correlates with performance in the Iowa Gambling Task. Hum Brain Mapp 2006; 27: 572–587.

    Article  Google Scholar 

  43. Clark L, Cools R, Robbins TW . The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn 2004; 55: 41–53.

    Article  CAS  Google Scholar 

  44. Kringelbach ML, Rolls ET . The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 2004; 72: 341–372.

    Article  Google Scholar 

  45. Kringelbach ML . The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 2005; 6: 691–702.

    Article  CAS  Google Scholar 

  46. Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR . A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J Neurosci 2000; 20: 2683–2690.

    Article  CAS  Google Scholar 

  47. Walton ME, Croxson PL, Behrens TE, Kennerley SW, Rushworth MF . Adaptive decision making and value in the anterior cingulate cortex. Neuroimage 2007; 36 (Suppl 2): T142–T154.

    Article  Google Scholar 

  48. Taylor SF, Liberzon I . Neural correlates of emotion regulation in psychopathology. Trends Cogn Sci 2007; 11: 413–418.

    Article  Google Scholar 

  49. van den Heuvel OA, Veltman DJ, Groenewegen HJ, Cath DC, van Balkom AJLM, van Hartskamp J et al. Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. Arch Gen Psychiatry 2005; 62: 301–310.

    Article  Google Scholar 

  50. Hartl TL, Frost RO, Allen GJ, Deckersbach T, Steketee G, Dufany SR et al. Actual and perceived memory deficits in individuals with compulsive hoarding. Depress Anxiety 2004; 20: 59–69.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the MRI team of the Institute of Psychiatry for their help with the design and MRI physics of this project and Dr Odile van den Heuvel for her helpful comments on an earlier draft. This study was funded by project grant no. 064846 from the Wellcome Trust, UK and a pilot grant from the South London and Maudsley NHS Trust.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to D Mataix-Cols.

Rights and permissions

Reprints and permissions

About this article

Cite this article

An, S., Mataix-Cols, D., Lawrence, N. et al. To discard or not to discard: the neural basis of hoarding symptoms in obsessive-compulsive disorder. Mol Psychiatry 14, 318–331 (2009). https://doi.org/10.1038/sj.mp.4002129

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.mp.4002129

Keywords

This article is cited by

Search

Quick links