Neural Mechanisms of Decision Making in Hoarding Disorder

Abstract

Context Hoarding disorder (HD), previously considered a subtype of obsessive-compulsive disorder (OCD), has been proposed as a unique diagnostic entity in DSM-5. Current models of HD emphasize problems of decision-making, attachment to possessions, and poor insight, whereas previous neuroimaging studies have suggested abnormalities in frontal brain regions. Objective To examine the neural mechanisms of impaired decision making in HD in patients with well-defined primary HD compared with patients with OCD and healthy control subjects (HCs). Design We compared neural activity among patients with HD, patients with OCD, and HCs during decisions to keep or discard personal possessions and control possessions from November 9, 2006, to August 13, 2010. Setting Private, not-for-profit hospital. Participants A total of 107 adults (43 with HD, 31 with OCD, and 33 HCs). Main Outcome Measures Neural activity as measured by functional magnetic resonance imaging in which actual real-time and binding decisions had to be made about whether to keep or discard possessions. Results Compared with participants with OCD and HC, participants with HD exhibited abnormal activity in the anterior cingulate cortex and insula that was stimulus dependent. Specifically, when deciding about items that did not belong to them, patients with HD showed relatively lower activity in these brain regions. However, when deciding about items that belonged to them, these regions showed excessive functional magnetic resonance imaging signals compared with the other 2 groups. These differences in neural function correlated significantly with hoarding severity and self-ratings of indecisiveness and “not just right” feelings among patients with HD and were unattributable to OCD or depressive symptoms. Conclusions Findings suggest a biphasic abnormality in anterior cingulate cortex and insula function in patients with HD related to problems in identifying the emotional significance of a stimulus, generating appropriate emotional response, or regulating affective state during decision making.

The Relationship between Hoarding Symptoms, Intolerance of Uncertainty, and Error-Related Negativity

“…The finding that hoarding symptoms predict ERN only on possession-related errors may support the notion of a possession-sensitive 'error-warning system' in hoarding individuals (Tolin et al 2012b) and the proposition that fear of error when discarding may have a neurological basis (Mathews et al 2012(Mathews et al , 2015. The extent to which an individual's tolerance for uncertainty affects this system, however, remains unclear.…”

“…It is possible that error-monitoring in hoarding individuals becomes exaggerated during discarding decisions partially due to the uncertain fate of the object, or uncertainty regarding the future utility or value of the discarded possession. If so, our current findings may help account for why ACC activity in hoarding individuals correlates with a nagging need for certainty when discarding (Tolin et al 2012b) and is greatest when they refuse to discard their possessions (Tolin et al 2009). Of course, this proposition is speculative and the present data should be viewed as the beginning of a complex examination of the overlap between these processes.…”

“…In hoarding individuals, hemodynamic ACC activity during discarding positively correlates with Bnot just right^feel-ings (Tolin et al 2012b) -a nagging psychological need for complete certainty and control (Rasmussen and Eisen 1992). In addition, this ACC activity appears greatest when these individuals refuse to discard, over and above successful discarding (Tolin et al 2009), suggesting that discarding is avoided when ACC is most active.…”

“…Abnormal hemodynamic activity in the anterior cingulate cortex (ACC) of some hoarding individuals appears to be modulated by whether or not they are dealing with their possessions or novel objects (Tolin et al 2009;Tolin et al 2012a;Tolin et al 2012b). Event-related potential (ERP) evidence suggests that error detection processes associated with ACC activity may be abnormal in OCD-related hoarding and HD (Mathews et al 2012;Mathews et al 2015;Riesel et al 2014).…”

“…Some hemodynamic studies show preliminary evidence of an association between these processes. Broadly speaking, IU appears directly related to increased hemodynamic activity in the insula when faced with emotional ambiguity (Simmons et al 2008); a brain area adjacent to the ACC that is also implicated in hoarding (Tolin et al 2012a;Tolin et al 2012b). More specifically, recent research has found a direct association between the amplitude of the ERN and an individual's tolerance for uncertainty (Jackson et al 2016).…”