ORIGINAL ARTICLE Neural Mechanisms of Decision Making in Hoarding Disorder David F. Tolin, PhD; Michael C. Stevens, PhD; Anna L. Villavicencio, PhD; Melissa M. Norberg, PhD; Vince D. Calhoun, PhD; Randy O. Frost, PhD; Gail Steketee, PhD; Scott L. Rauch, MD; Godfrey D. Pearlson, MD Context: Hoarding disorder (HD), previously consid- actual real-time and binding decisions had to be made ered a subtype of obsessive-compulsive disorder (OCD), about whether to keep or discard possessions. has been proposed as a unique diagnostic entity in DSM-5. Current models of HD emphasize problems of decision- Results: Compared with participants with OCD and HC, making, attachment to possessions, and poor insight, participants with HD exhibited abnormal activity in the whereas previous neuroimaging studies have suggested anterior cingulate cortex and insula that was stimulus de- abnormalities in frontal brain regions. pendent. Specifically, when deciding about items that did not belong to them, patients with HD showed relatively Objective: To examine the neural mechanisms of im- lower activity in these brain regions. However, when de- paired decision making in HD in patients with well- ciding about items that belonged to them, these regions defined primary HD compared with patients with OCD showed excessive functional magnetic resonance imaging and healthy control subjects (HCs). signals compared with the other 2 groups. These differ- ences in neural function correlated significantly with Design: We compared neural activity among patients hoarding severity and self-ratings of indecisiveness and with HD, patients with OCD, and HCs during decisions “not just right” feelings among patients with HD and were to keep or discard personal possessions and control pos- unattributable to OCD or depressive symptoms. sessions from November 9, 2006, to August 13, 2010. Conclusions: Findings suggest a biphasic abnormality Setting: Private, not-for-profit hospital. in anterior cingulate cortex and insula function in pa- tients with HD related to problems in identifying the emo- Participants: A total of 107 adults (43 with HD, 31 with tional significance of a stimulus, generating appropriate OCD, and 33 HCs). emotional response, or regulating affective state during decision making. Main Outcome Measures: Neural activity as mea- sured by functional magnetic resonance imaging in which Arch Gen Psychiatry. 2012;69(8):832-841 URRENT MODELS OF tion,14,15 leading to resistance of attempts by hoarding disorder (HD)— others to intervene. Such impairments might defined as the excessive suggest abnormalities in frontal cortical re- acquisition of and inabil- gions and the anterior cingulate cortex ity to discard objects, re- (ACC), which are involved with executive sulting in debilitating clutter1—identify vari- functions, such as decision making and cat- Author Affiliations: The C 16-18 ous deficits in cognitive processes, as well egorization, and temporal regions that Institute of Living, Hartford, as maladaptive beliefs and behavioral pat- are associated with memory, categoriza- Connecticut (Drs Tolin, terns, as relevant underlying mecha- tion, and attachment of affective or moti- Stevens, Villavicencio, Norberg, 2-4 19,20 and Pearlson); Yale University nisms. Specific cognitive impairments vational significance to stimuli. School of Medicine, New noted in patients with HD include im- Four studies have used neuroimaging Haven, Connecticut (Drs Tolin, paired attention,5,6 impaired verbal and non- technology to examine regional brain func- Stevens, and Pearlson); The verbal recall,7 and impaired categorization tion associated with hoarding. Positron Mind Research Network and and decision-making ability.8,9 Maladap- emission tomography research reveals that The University of New Mexico, tive beliefs include perfectionism and fears patients with obsessive-compulsive dis- Albuquerque (Dr Calhoun); of making wrong decisions,10,11 fears of wast- order (OCD) with hoarding symptoms Smith College, Northampton, ing or losing important information,12 and have lower resting state glucose metabo- Massachusetts (Dr Frost); emotional or anthropomorphic attach- lism in the posterior cingulate and cu- Boston University, Boston, 13 Massachusetts (Dr Steketee); ment to possessions. The disorder is char- neus than do healthy control subjects and McLean Hospital and acterized by marked avoidance of decision (HCs) and lower glucose metabolism in Harvard Medical School, making about possessions. Patients with HD the dorsal ACC than do patients with OCD Belmont, Massachusetts are frequently characterized by poor in- without hoarding symptoms.21 Func- (Dr Rauch). sight about the severity of their condi- tional magnetic resonance imaging (fMRI) ARCH GEN PSYCHIATRY/ VOL 69 (NO. 8), AUG 2012 WWW.ARCHGENPSYCHIATRY.COM 832 ©2012 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 reveals that patients with OCD (mostly patients with OCD moderate symptom severity as evidenced by a Clinician’s Global without hoarding symptoms) asked to imagine discard- Impression rating of moderately ill or above, and had at least 1 year ing an item experience greater activity in the left precen- of symptom duration. The HD or OCD participants were excluded tral gyrus and right medial orbitofrontal cortex (OFC) if they had a history of psychotic disorder, neurologic disorder, sub- than do HCs,22 and patients with OCD with hoarding stance abuse, or serious suicidal ideation. Healthy controls were excluded if they met criteria for a current or past Axis I or Axis II symptoms experience greater activation in the ventro- disorder, had a history of neurologic disorders, or were taking psy- medial prefrontal cortex than do patients with OCD with- chiatric medications. Participants who were unsuitable for fMRI 23 out hoarding symptoms and HCs using the same task. (eg,thosewithsevereclaustrophobia,pregnancy,ormetalimplants) During actual decision making about real possessions, were excluded. patients with HD experience greater activity in the left lateral OFC and parahippocampal gyrus than do HCs.24 Thus, results to date implicate frontal and temporal OUTCOME MEASURES regions thought to underlie problems of decision mak- Demographic information, including self-reported race and eth- ing, attachment, reward processing, impulse control, self- nicity, was collected via questionnaire. The HD diagnoses were awareness, and emotion regulation. However, substan- made using the Hoarding Rating Scale–Interview,29 a semi- tial differences in population and methods across these structured interview that assesses the severity of clutter, ac- studies preclude clear generalization of conclusions. The quisition, difficulty discarding, distress, and impairment, each objective of the present study is to provide a clearer ex- on a 0- to 8-point scale. Other psychiatric diagnoses were as- amination of the neural mechanisms of impaired deci- certained using the Anxiety Disorders Interview Schedule for sion making that are specific to HD. Unlike previous DSM-IV.27 Severity of HD was assessed using the Saving Inven- 30 research, the present study recruited patients with well- tory–Revised, a 23-item questionnaire. Nonhoarding OCD se- defined primary HD and compared them with patients verity was assessed using the Obsessive Compulsive Inventory– Revised (OCI-R),31 an 18-item self-report measure. For use in with OCD and HCs using a unique fMRI task in which analysis of covariance, a total OCI-R score was calculated that actual, real-time, and binding decisions had to be made omitted the 3 hoarding items. Depression severity was as- about whether to keep or discard possessions. We pre- sessed using the Hamilton Rating Scale for Depression (HRSD),32 dicted that, compared with patients with OCD and HCs, a 17-item semistructured interview. The Structured Interview patients with HD would experience increased hemody- Guide for the HRSD33 was used for administration. Global im- namic activity in the frontal and temporal cortical re- pressions of illness severity were recorded using the Clini- gions, including the ventromedial prefrontal cortex, OFC, cian’s Global Impression28 scale. A series of visual analog scales ACC, and parahippocampal gyrus, when deciding whether (VASs) were constructed for the present study. For each VAS, to discard their own possessions. No such differences were an emotion label and numeric scale (0-100) were presented on predicted when participants were deciding whether to the computer screen. The emotions to be rated included anxi- ety, indecisiveness, sadness, and “not just right” feelings. discard control items that did not belong to them. We further predicted that fMRI measures in the aforemen- tioned regions of interest (ROIs) would reveal a unique STUDY MATERIALS relationship to hoarding symptom severity, indepen- dent of severity of OCD or depressive symptoms. For the decision-making task, we selected 2 different sets of stimuli. The first set was paper items (eg, junk mail and news- papers) that belonged to the participants. Participants were in- METHODS structed to bring to the scanner session paper items from their homes without sorting them first. We refer to these items as participant’s possessions (PPs). The second set of stimuli was STUDY PARTICIPANTS comparable paper items that did not belong to the participant. For each participant, we selected items that were roughly the Forty-three patients with HD, 31 patients with OCD, and 33 HCs same amount, size,