Hoarding disorder (HD) is characterized by difficulty discarding or parting with possessions, and, in most cases, excessively acquiring objects, resulting in clutter that disrupts use of living spaces and impacts various aspects of life in affected individuals (American Psychiatric Association, 2013; Frost et al., 2009). It is relatively common, affecting around 2.5 % of the general population (American Psychiatric Association, 2022; Postlethwaite et al., 2019). People with HD may experience lower social functioning and have a higher likelihood of marital and employment difficulties (Chou et al., 2020; van Roessel et al., 2023). Clutter associated with HD can lead to health and safety risks, impacting neighbors via fire hazards and pest infestations (Frost et al., 2000; Tolin et al., 2008; Wilbram et al., 2008). Despite the detrimental impact of HD, our current understanding of the neural mechanisms driving HD symptoms is limited. There are no FDA-approved treatments for HD, and our knowledge of how current behavioral therapies affect behavioral performance and neural circuits is insufficient.

Cognitive control may be a promising target for study in HD. Cognitive control involves employing executive functions to guide appropriate actions aimed at achieving a specific goal (Badre, 2008; Kouneiher et al., 2009; Miller, 2000), and it is involved in managing and regulating cognitive processes such as attention, decision-making, working memory, and inhibitory control (Breukelaar et al., 2017; Minzenberg et al., 2009; Niendam et al., 2012). Prior studies have examined different aspects of cognitive performance in HD (Woody et al., 2014). Specifically, the hoarding symptoms of overvaluing of objects and difficulty discarding possessions may be a result of impairments in decision-making, categorization, and attention. Woody et al. (2014) surveyed the literature and reported that while there are some areas of cognitive performance that show replicated deficits (e.g., planning decisions, visuospatial learning, sustained attention), other areas showed mixed results and required further study, including concept formation, visuospatial processing, and inhibitory control.

The anterior cingulate cortex (ACC) and bilateral insula are major nodes in the cognitive control circuit involved in inhibitory control, conflict monitoring, and decision-making (Bush et al., 2000; Hanlon et al., 2016; Velanova et al., 2008). Higher activity in the ACC and the insula has been linked with error processing and inhibitory control (Velanova et al., 2008). Consistent with this, greater activity is observed in the ACC and bilateral insula during errors of commission on tasks requiring inhibitory control (Ghahremani et al., 2015; Ramautar et al., 2006). Furthermore, increased activity in both the ACC and insula is a common feature across psychiatric disorders characterized by impaired inhibitory control (Fitzgerald et al., 2005; Hanlon et al., 2016).

In hoarding disorder, findings regarding ACC and insula activity during tasks requiring inhibitory control are mixed. Increased ACC activation has been noted in HD participants during commission errors in the GoNoGo task (Hough et al., 2016). However, these findings are inconsistent with a prior study that reported no significant differences between HD participants and controls (Tolin et al., 2014b). Taken together, these studies indicate that the ACC and insula are regions of interest when studying HD, and understanding how they change during therapeutic interventions will help build on the existing literature.

Meta-analyses have shown that cognitive behavioral therapy (CBT) is an effective treatment for HD (Mathews et al., 2018; Moulding et al., 2017; Rodgers et al., 2021; Tolin et al., 2019). The Buried in Treasures (BIT) workshop is a skills-based group using CBT principles. We and others have previously reported on the clinical effects of BIT on HD (Frost et al., 2012) including our recent study showing that BIT+ (a therapy that combines BIT sessions with in-home uncluttering sessions) significantly reduced HD symptoms in all subscales of the SI-R (Wheaton et al., 2024). However, it is still unknown whether the BIT+ intervention may modulate the cognitive control circuit as an underlying neural mechanism for its therapeutic effects.

Previous neuroimaging studies have shown increased activity in the ACC and insula when individuals with HD make decisions about keeping or discarding personal possessions versus non-personal items (Tolin et al., 2012). Building on this, Tolin et al. (2023) investigated how CBT modulates activity in key brain regions of interest (ROIs) implicated in HD-related neurobiological impairments. In this study, participants were scanned while making simulated decisions about acquiring and discarding objects. The results revealed activity changes in the dorsal anterior cingulate cortex. However, despite these neural changes, there was no evidence that these alterations directly mediated improvements in HD symptoms. Other examinations of neural activity in regions of the cognitive control circuit during an inhibitory control-evoked task revealed that ACC hyperactivity was associated with inhibitory control impairments (Hough et al., 2016). However, no data were provided regarding the effects of CBT in this context. Building on these findings, our study aimed to examine how CBT modulates activity in regions of the cognitive control circuit within a neutral context, specifically focusing on inhibitory control rather than decision-making, as explored by Tolin et al. (2023).

To gain a deeper understanding on inhibitory control impairments in adults with HD and to examine whether BIT+ could modulate the cognitive control circuit, this study focused on examining activation within the ACC and insula both at baseline and following BIT+ sessions, during a functional magnetic resonance imaging (fMRI) GoNoGo task. Specifically, we examined the inhibitory control deficits in HD as compared to healthy controls (HC) at baseline, and we investigated whether changes in right insula, left insula and ACC activity were linked to the effects of BIT+ in adults with HD. To do so, we obtained estimates of blood-oxygen-level-dependent (BOLD)signal magnitude during incorrect NoGo trials , both before and after 18 weeks of BIT+ treatment. We hypothesized that HD participants will show higher activity in the insula and ACC compared to HC at baseline. Further, we hypothesized that this hyperactivity would be normalized in patients whose hoarding symptoms responded to BIT+ treatment; therefore, we would observe an association between lower activation of the ACC and insula with symptom improvement measured by the SI-R total and SI-R acquisitions scales after BIT+.

The observed difficulty in individuals with HD to suppress urges to save items or excessively acquire possessions led us to hypothesize that these behaviors stem from impairments in inhibitory control. Based on this, we predicted that participants in the HD group would demonstrate a higher frequency of commission errors (indicative of lapses in inhibitory control) when compared to HC. Furthermore, we anticipated that participation in BIT+ treatment would result in a reduction in commission errors among individuals with HD, reflecting potential improvements in inhibitory control. Given that deficits in attention are commonly reported in HD (Grisham et al., 2010; Hartl et al., 2005), we extended our investigation to explore baseline attention deficits. Specifically, we assessed whether the HD group exhibited increased errors of omission, which could indicate difficulties in sustaining attention. This dual focus, which integrates behavioral assessments with neuroimaging, has the potential to reveal neural changes associated with the response to behavioral therapy. Such findings could enhance our understanding of the neural mechanisms underlying HD symptoms and inform the development of more effective interventions. These advancements could not only refine behavioral therapies but also support the design of targeted pharmacological treatments or neurostimulation-based approaches, offering a multifaceted strategy to address HD more comprehensively.