The Neural Correlates of Compulsive Hoarding

The previous two posts described the emergence of compulsive collecting behavior (of Toy Bullets and Televisions) following damage to the orbitofrontal cortex. Although these unusual case reports do appear in the neurological literature, compulsive hoarding or collecting is much more common in psychiatric settings, as a disorder that may occur as a symptom of OCD (or as a separate diagnosis). In fact, in their new paper, Pertusa and colleagues (2008) ask the question, Compulsive Hoarding: OCD Symptom, Distinct Clinical Syndrome, or Both? [Both¹]. Earlier studies have come to similar conclusions (e.g., Grisham et al., 2005).



A recent neuroimaging study (An et al., 2008) used a symptom provocation procedure to examine the neural correlates of hoarding. The research participants were restricted to individuals with obsessive-compulsive disorder; those hoarders without an OCD diagnosis were excluded. Thus, two groups of OCD patients (those with and without hoarding symptoms) were compared to demographically matched controls while viewing three types of pictures [the figure is my completely fabricated rendition of possible exemplars²].

(1) neutral or mildly positive - 150 color pictures rated as low in disgust and anxiety. Examples included furniture, nature scenes, urban landscapes, household items, pets, families. The pictures were obtained from the International Affective Picture System.

(2) aversive control - 50 color pictures of scenes rated as highly disgusting and anxiety-provoking by healthy subjects were also obtained from the IAPS. These included scenes of mutilated bodies/wounds, small animals (snakes, spiders, cockroaches and rats) and body products.

(3) commonly hoarded objects - 50 color pictures that included items such as old magazines/newspapers, empty food containers, clothes and toys. These pictures were rated by several patients (not in the fMRI study) to ensure that they would be anxiety-provoking.

The pictures were presented in alternating blocks of neutral and emotional. Participants were instructed to

imagine being in a particular situation while looking at the scenes they were about to see (for example, for hoarding: ‘Imagine that these objects belong to you and that you must throw them away forever;’ for aversive control: ‘Imagine that you must come into contact with what is shown in the pictures’). After each set of pictures were presented, another prerecorded sound file of the question ‘How anxious do you feel?’ was played and the subjects rated their subjective anxiety on a Likert-style scale (0 = no anxiety to 8 = extreme anxiety).

Not surprisingly, the OCD-hoarders rated the hoarding pictures as more anxiety-provoking than did the other two groups. However, the aversive control pictures were rated as equivalently yucky by all three groups.

What did the fMRI results show? From the previous neurological case studies, one would expect differences in the orbitofrontal cortex of the OCD-hoarding group, relative to the non-hoarding and control participants. And indeed, when viewing the provocative stacks of magazines and empty food containers,

OCD patients with prominent hoarding symptoms showed greater activation in bilateral anterior ventromedial prefrontal cortex (VMPFC) than patients without hoarding symptoms and healthy controls.

Figure 2A (An et al., 2008). Brain regions significantly more activated in hoarders than in non-hoarders and controls (shown in red) during symptom provocation. The functional data are superimposed on a high-resolution anatomical template using the MRIcro software. The left side of the brain appears on the right side of the image. The box plots depict the percent change in blood oxygen level dependent (BOLD) response in each group. In each box plot, the horizontal lines represent the group median, the box represents the quartiles and the whiskers the extreme values in each group.

In contrast, when comparing the disgusting aversive pictures to neutral pictures, the activated regions in the hoarding OCD patients were more similar to those that were seen in the non-hoarding OCD patients and the healthy control participants. However, the hoarders did show less activation in the cerebellum and visual areas than the controls (and the non-hoarders showed more).

The authors suggest that

The brain regions associated with compulsive hoarding in this study are anatomically very close to those associated with hoarding behaviors ... in human lesion studies. Although it is plausible that hoarding behaviors caused by brain lesions may be phenomenologically and etiologically distinct from obsessive-compulsive hoarding, our results seem to suggest that they share similar neural substrates.

[Although the regions are missing in the human lesion patients, and overactive in the OCD hoarding patients...]


For more information on compulsive hoarding:

The Anxiety Disorders Center at Hartford Hospital - Compulsive Hoarding

Department of Psychiatry, UCSD - WHAT IS COMPULSIVE HOARDING?

Understanding Compulsive Hoarding - from the Children of Compulsive Hoarders website, which features a wealth of information, videos, and support for families.

Several months ago, Mind Hacks reviewed the short documentary film, Possessed, which is about four people with compulsive hoarding disorder. The filmmaker, Martin Hampton, is currently working on a follow-up project about people's personal experiences with OCD.


News stories:

New York Times - A Clutter Too Deep for Mere Bins and Shelves

ABC News - The Tortured Lives of People Who Can't Throw Things Out

Discover magazine - The Psychology of . . . Hoarding


Footnotes

¹ Both, say Pertusa et al.:

Overall, the phenomenology of hoarding behavior was similar in the two hoarding groups [OCD with Hoarding, Hoarding only]. The majority of participants in both groups reported hoarding common items as a result of their emotional and/or intrinsic value. However, approximately one-fourth of participants in the compulsive hoarding with OCD group showed a different psychopathological profile, which was characterized by the hoarding of bizarre items and the presence of other obsessions and compulsions related to their hoarding, such as fear of catastrophic consequences, the need to perform checking rituals, and the need to perform mental compulsions before discarding any item. ... In most individuals, compulsive hoarding appears to be a syndrome separate from OCD, which is associated with substantial levels of disability and social isolation. However, in other individuals, compulsive hoarding may be considered a symptom of OCD and has unique clinical features.

² I decided to use a moldy slice of bread, rather than a mutilated body part, so as not to offend the sensibilities of the more delicate reader.

References

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 DOI: 10.1038/sj.mp.4002129

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.

Grisham JR, Brown TA, Liverant GI, Campbell-Sills L. (2005). The distinctiveness of compulsive hoarding from obsessive-compulsive disorder. J Anxiety Disord. 19:767-79.

Pertusa A, Fullana MA, Singh S, Alonso P, Menchón JM, Mataix-Cols D. (2008). Compulsive Hoarding: OCD Symptom, Distinct Clinical Syndrome, or Both? Am J Psychiatry. May 15. [Epub ahead of print].