Central and Peripheral Physiological Responses to Decision Making in Hoarding Disorder

Hannah C. Levy¹

Adam J. Naples^{2, 3}

Sarah Collett¹

James C. McPartland^{2, 3}

David F. Tolin^{1, 4}

¹Anxiety Disorders Center, Institute of Living, Hartford, CT, USA

²Yale Child Study Center, Yale School of Medicine, New Haven, CT, USA

³Center for Brain and Mind Health, Yale School of Medicine, New Haven, CT, USA

⁴Yale University School of Medicine

Author Note

Correspondence concerning this article should be addressed to Hannah Levy, Anxiety Disorders Center, Institute of Living/Hartford Hospital, 200 Retreat Avenue, Hartford, CT 06106. Tel.: 860-545-7847. Fax: 860-545-7105. Email: hannah.levy@hhchealth.org.

Author email addresses: Adam Naples, adam.naples@yale.edu; Sarah Collett, sarah.collett@hhchealth.org; James McPartland, james.mcpartland@yale.edu; David Tolin, david.tolin@hhchealth.org

Abstract

Individuals with hoarding disorder (HD) have difficulty parting with personal possessions, which leads to the accumulation of excessive clutter. According to a proposed biphasic neurobiological model, HD is characterized by blunted central and peripheral nervous system activity at rest and during neutral (non-discarding) decisions, and exaggerated activity during decision-making about discarding personal possessions. Here, we compared the error-related negativity (ERN) and psychophysiological responses (skin conductance, heart rate and heart rate variability, and end tidal CO₂) during neutral and discarding-related decisions in 26 individuals with HD, 37 control participants with anxiety disorders, and 28 healthy control participants without psychiatric diagnoses. We also compared alpha asymmetry between the HD and control groups during a baseline resting phase. Participants completed a series of Go/No Go decision-making tasks, one involving choosing certain shapes (neutral task) and the other involving choosing images of newspapers to imaginally “discard” (discarding task). Contrary to hypotheses, there were no group differences in the ERN or any psychophysiological measures. Alpha asymmetry at rest did not differ between groups. The findings suggest that the ERN and psychophysiological responses may not differ in individuals with HD during simulated discarding decisions relative to control participants, although the null results may be explained by methodological challenges in using Go/No Go tasks as discarding tasks. Future replication and extension of these results will be needed using ecologically valid discarding tasks.

Keywords : hoarding disorder; error-related negativity; psychophysiological responses; discarding

Central and Peripheral Physiological Responses to Decision Making in Hoarding Disorder

Hoarding disorder (HD) is characterized by difficulty discarding personal possessions, which leads to the accumulation of excessive clutter (American Psychiatric Association, 2013). HD is associated with significant functional impairment. Compared to patients with related mental health problems such as obsessive-compulsive disorder (OCD), patients with HD report significantly worse overall functioning and quality of life (Saxena et al., 2011). A systematic review similarly concluded that individuals with HD experience greater impairment in various domains of functioning relative to control groups (Ong et al., 2015).

Unfortunately, treatment options for HD are limited. Cognitive-behavioral therapy (CBT) is efficacious for HD (Steketee et al., 2010; Tolin et al., 2019), but results are modest. Meta-analytic research suggests that only 35% of patients with HD who receive CBT achieve clinically significant change (a measure of remission status) (Tolin et al., 2015). To address this problem, research has focused on identifying neurobiological mechanisms of HD that may inform novel treatment development. A proposed biphasic neurobiological model of HD (Tolin, 2023) posits that HD is characterized by blunted central nervous system (CNS) and peripheral nervous system (PNS) activity at rest or during neutral (non-discarding) tasks, and exaggerated CNS and PNS activity during decision-making about discarding personal possessions.

Some evidence points to a baseline under-engagement of CNS processes in individuals with HD. An early positron emission tomography (PET) study, which predates the DSM-5 diagnosis of HD, found that OCD patients with prominent hoarding symptoms exhibited significantly lower activity in posterior cingulate gyrus and cuneus relative to healthy control participants during a task-free resting state (Saxena et al., 2004). A more recent functional magnetic resonance imaging (fMRI) study (Sunol et al., 2019) found that individuals with HD demonstrated decreased activity in dorsolateral prefrontal cortex (dlPFC), dorsomedial prefrontal cortex (dmPFC), and precentral gyrus during error processing in a Go/No Go task relative to individuals with OCD and healthy control participants, though orbitofrontal cortex (OFC) activity was enhanced. Other fMRI research has similarly shown attenuated activity in frontal regions, including the anterior cingulate cortex (ACC) and insula, during emotionally-neutral decision-making in HD participants relative to clinical and nonclinical control groups (Stevens et al., 2020; Tolin et al., 2012). In contrast to these results, it should be noted that Hough et al. (2016) reported greater activation of frontal regions (ACC and dlPFC) during an emotionally neutral (non-discarding) Go/No Go task in participants with HD, compared to healthy controls and individuals with OCD.

Conversely, when making emotionally salient decisions about discarding personal possessions during fMRI, relative to healthy control participants and those with OCD, individuals with HD demonstrate excessive activity in the ACC and insula (Stevens et al., 2020; Tolin et al., 2012). Further evidence of exaggerated responding comes from studies of PNS response. When making personally relevant decisions about discarding their own possessions vs. when deciding whether to discard matched control items (“experimenter owned” possessions, which were items donated by study staff), participants with HD demonstrated greater heart rate, greater skin conductance, and increased hyperventilation as indicated by lower end tidal CO₂ (ETCO₂) (Levy, Nett, & Tolin, 2019).

The present study aimed to expand on these prior studies, which collectively suggest a biphasic abnormality, by measuring CNS and PNS activity during a neutral task and during a simulated decision-making task about possessions. For CNS measurement, we used electroencephalography (EEG) because it captures ongoing neural activity with a temporal resolution that is superior to fMRI, thus allowing us to examine moment-to-moment changes in brain activity that may be specific to discarding decisions. We focused first on error-related negativity (ERN), a negative event-related potential that is generated by the ACC when an individual detects that they have made an error, or when an error is likely. Consistent with prior studies of CNS responses (Stevens et al., 2020; Sunol et al., 2019; Tolin et al., 2012), during non-discarding-related tasks, the ERN is significantly lower in individuals with HD relative to individuals with OCD and healthy control participants (Baldwin et al., 2019; Mathews et al., 2016). In a sample of undergraduate student participants, hoarding symptoms predicted greater ERN amplitudes for discarding-related decisions but not emotionally neutral decisions (Baldwin, Whitford, & Grisham, 2016). We predicted that individuals with HD would demonstrate greater ERN during discarding decisions, and lower ERN during emotionally neutral decisions, compared to anxious and healthy control groups, and that the ERN during simulated discarding decisions would predict the severity of HD symptoms.

We also assessed resting state alpha asymmetry, or the difference between left and right alpha wave activity in the frontal regions of the brain. Relatively greater left vs. right alpha activity is commonly associated with approach motivation (Harmon-Jones, Peterson, & Harris, 2009; Harmon-Jones et al., 2004), whereas relatively greater right vs. left alpha is thought to reflect withdrawal/avoidance motivation (Coan, Allen, & Harmon-Jones, 2001). Consistent with these results, greater right alpha is associated with psychiatric conditions that are characterized by withdrawal and avoidance, such as depression [for a review, see Coan and Allen (2004)]. We are not aware of any prior research assessing alpha asymmetry in patients with HD; however, based on evidence from related psychiatric conditions such as depression, we predicted that the HD group would demonstrate greater right vs. left alpha asymmetry during the baseline resting period.

For PNS activity, we compared psychophysiological responses among HD participants and the control groups. Specifically, we measured ETCO₂, heart rate (HR) and heart rate variability (HRV), and skin conductance. Thus, this study expands the findings of Levy, Nett and Tolin (2019) who did not use a control group. We predicted that the HD group would demonstrate greater psychophysiological activation for simulated discarding decisions, and lower psychophysiological activity during emotionally neutral decisions, relative to the control groups.