Central and Peripheral Physiological Responses to Decision Making in
Hoarding Disorder
Hannah C. Levy1
Adam J. Naples2, 3
Sarah Collett1
James C. McPartland2, 3
David F. Tolin1, 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.