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.