Discussion
The aim of this study was to compare CNS activity, measured with ERN and alpha asymmetry, and PNS activity, measured by HRV, HR, ETCO2, SCL, and SCR, during simulated discarding decisions and emotionally neutral decisions in individuals with HD, anxious control participants, and healthy control participants. Contrary to hypotheses, there were no significant group differences on any CNS or PNS measures for neutral or discarding decisions. The ERN during the simulated discarding task was not associated with hoarding symptoms. We offer some potential explanations for these null findings below.
As described above, we had initially intended to use a simulated discarding task that had been used in prior research on the ERN (Baldwin, Whitford, & Grisham, 2016). However, we had to modify the original task to increase its difficulty and obtain more errors to reliably measure the ERN, and we may have unintentionally ended up with more of a visual detection task (participants had to distinguish between newspapers that did and did not have pictures on them) rather than a discarding-related decision-making task. Prior studies that have found exaggerated activity in frontal brain regions and excessive psychophysiological activation during discarding decisions have used more ecologically valid tasks that likely were more emotionally salient for those with HD, including sorting and discarding personal possessions or imagined personal possessions (Levy, Nett, & Tolin, 2019; Stevens et al., 2020; Tolin et al., 2012). On the other hand, the task itself would not explain why the neutral (non-discarding) task also showed no group differences for CNS or PNS activity. Prior studies have found decreased activity in frontal regions during neutral (non-discarding) error processing tasks (Mathews et al., 2016; Sunol et al., 2019) and during tasks involving discarding others’ possessions (Tolin et al., 2012). By contrast, Hough et al. (2016) reported greater activity in frontal regions during error processing, making it challenging to draw conclusions about CNS processes during decision-making in HD.
Alternatively, it is possible that our use of EEG hampered our ability to detect HD-related abnormalities. As described above, the most reliable evidence of exaggerated CNS activity during discarding decisions comes from fMRI research (Stevens et al., 2020; Tolin et al., 2012). The major advantage of EEG relative to fMRI is the ability to assess moment-to-moment changes in brain activity, which is not possible in fMRI due to the delayed BOLD signal. However, the ERN occurs at a very specific time following commission of an error [approximately 50 milliseconds after the error; for a review, see Olvet and Hajcak (2008)], so the tasks must be timed exactly to capture the effect. Discarding tasks involving real possessions, by nature, cannot be timed this precisely, making it challenging to design an ecologically valid discarding task that is also accurate for measuring the ERN.
We also did not find evidence of greater right vs. left alpha asymmetry during a baseline resting period in HD relative to the anxious and healthy control groups. To our knowledge, this study is the first to assess alpha asymmetry in individuals with HD. Prior research has shown that depression, which is commonly comorbid with HD, is characterized by right lateralized alpha asymmetry (Coan & Allen, 2004; Kemp et al., 2010), although it should be noted that a meta-analysis did not find alpha asymmetry differences between patients with major depressive disorder and healthy controls (van der Vinne et al., 2017). We were surprised by this finding, particularly because patients with HD commonly engage in avoidance behaviors (particularly discarding their possessions) and they experience social impairment often characterized by withdrawal from significant others. Alpha asymmetry has previously been linked to avoidance/withdrawal motivation (Coan, Allen, & Harmon-Jones, 2001). On the other hand, other mental health disorders characterized by avoidance that are often comorbid with HD, including anxiety-related disorders, have not consistently shown significantly right lateralized alpha asymmetry (Harrewijn, Van der Molen, & Westenberg, 2016; Kemp et al., 2010; Smith, Zambrano-Vazquez, & Allen, 2016). Based on the results of the current study, alpha asymmetry may not be a fruitful biomarker for future study in HD.
Future investigations of CNS and PNS responses to decision-making in HD may require more ecologically valid discarding tasks. Although this may be challenging due to the barriers we described above, a potential avenue for future research is the use of virtual reality technology, which was tested and showed promise in terms of treatment acceptability and enhancing motivation for change in reducing clutter (Chasson et al., 2020). In this work, participants were immersed in a virtual reality environment that depicted rooms in their own homes. It is possible that a virtual reality environment would preserve the ecological validity of a discarding task but also allow the individual discarding decisions to be timed accurately enough to measure the ERN.
In addition to the methodological challenges described above, the current study had other limitations. First, the study was conducted during the COVID-19 pandemic, when recruitment for in-laboratory studies was particularly difficult. Because we were attempting to recruit individuals with HD, who are typically older, we suspect that many prospective participants declined the study due to discomfort about attending an in-person appointment. We also faced unexpected data loss due to equipment malfunctions, which further reduced our sample size and statistical power. It should be noted that the effect sizes we obtained in the current study were so small (ranging from η2p = 0.00-0.06) that it would have taken very large samples to detect these effects; we thus do not have reason to suspect that a larger sample would have greatly changed the results of the current study. Furthermore, our a priori power analysis indicated that our sample was large enough to detect at least a medium effect (see above). Our sample was also limited in terms of racial diversity. Second, despite our efforts to match the control groups to the HD group for age and sex, we ended up with age differences and had to control for age in the study analyses. To ensure that covarying age did not undermine our statistical power, we re-ran the study analyses excluding the covariate and found similar results for the ERN and psychophysiological activity. Nevertheless, matching for age across comparison groups is an important consideration for EEG research, given normative changes in neural activity that are associated with aging (Daselaar et al., 2015; Meyer, 2017; Raz et al., 2005; Rodrigue & Raz, 2004; Walhovd et al., 2011).
Further clarification of the neurobiology of HD is hoped to point to novel biological mechanisms that could be targeted in intervention development. As an example, a recent study in undergraduate students found that a single-session cognitive-behavioral intervention focused on reducing error sensitivity decreased the ERN, particularly for those with the highest baseline ERN (Meyer et al., 2020). It will also be important to further test the proposed neurobiological model of HD (Tolin, 2023). One particular area that remains to be studied pertains to the hypoactivity observed at rest (Saxena et al., 2004) and in neutral (non-discarding) tasks (Mathews et al., 2016; Sunol et al., 2019) among individuals with HD. It is unclear whether this hypoactivity is a critical or causal mechanism of HD or simply a side effect of HD symptoms. We look forward to future work that addresses these questions.