Deficits in physiological and self-conscious emotional response to errors in hoarding disorder
Introduction
Hoarding disorder (HD) is a highly impairing and distressing psychiatric disorder that poses a significant public health burden (Tolin et al., 2008). The prevalence of HD, estimated at 2–4% (Samuels et al., 2008), is higher than those of many other psychiatric disorders of adulthood (e.g., schizophrenia and bipolar disorder (McGrath et al., 2008, Kessler et al., 2005), and increases with age, beginning around age 35, reaching > 6% among adults over age 55 (Cath et al., 2017, Samuels et al., 2008). It can be expected that the public health burden of this disorder will continue to grow due to increased global life expectancy(Collaborators, 2016). However, in part because HD was not formally recognized as a separate psychiatric illness until 2013, research into its causes, prognosis, and treatment still lags behind that of other psychiatric disorders.
Although the pathophysiology of HD is not yet well understood, multiple theories about the fundamental causes of HD have been developed over the past two decades. Perhaps the best known of these is the cognitive-behavioral model of HD, developed by Frost and colleagues (Frost and Hartl, 1996, Steketee et al., 2003) which posits that HD arises from four core deficits: (1) information processing deficits (specifically decision-making, categorization/organization, and memory functions), (2) problematic emotional attachments (or more specifically, highly emotional [abnormal] attachments to items), (3) behavioral avoidance, and (4) erroneous beliefs about the nature (value or replaceability) of possessions (Frost and Hartl, 1996). Frost et al. postulated that these deficits are not mutually exclusive, but rather overlap and interact to create hoarding behaviors. For example, difficulty discarding may represent an avoidance behavior arising from indecisiveness and fear of making an error that serves to prevent or delay negative consequences, including negative emotions, that may arise from discarding an object that may be wanted later.
Subsequent studies have supported the hypothesis that hoarding behaviors are associated with strong negative and positive emotions. For example, positive emotions, such as happiness and pride, have been associated with excessive acquiring (Wheaton et al., 2011, Timpano et al., 2014, Steketee and David, 2011), while negative emotions such as anger, fear and sadness have been associated with the inability to discard (Fernández de la Cruz et al., 2013). Increased emotional reactivity and intense emotional reactions have been reported in a study of individuals who self-identified as having problematic hoarding when imagining both acquiring and discarding (Shaw et al., 2015). A study using a sample of college students also found that higher levels of hoarding symptoms were associated with a greater tendency towards impulsivity during negative mood states (Timpano and Schmidt, 2013). However, to date, all the work on emotional reactivity in HD has relied on self-report measures, and to our knowledge, emotional reactivity in individuals with HD has not been quantified using multi-modal approaches. Despite some initial work suggesting that individuals with HD may avoid unpleasant emotions (Ayers et al., 2014) (Wheaton et al., 2011) and report having a lower tolerance for distressing situations in general (Timpano et al., 2014), it is still unclear if the reported increase in emotional reactivity occurs beyond hoarding-related scenarios.
More work has been done on the hypothesis that hoarding behaviors are related to indecision and a fear of making errors. Studies of decision-making as a neuropsychological construct (assessed by tools such as the Iowa Gambling Task) have been equivocal (Steketee et al., 2003, Frost and Gross, 1993, Mackin et al., 20112016). In previous studies examining error commission on continuous performance tasks (such as the Sustained Attention to Response Task, the Stop Signal Reaction Time Task and Go/No-Go) hoarding participant's mean number of errors were slightly higher and reaction time slower than control groups, although these differences were not statistically significant (Blom et al., 2011, Grisham et al., 2010). To date, current studies examining neuropsychological functioning in respect to decision-making, error commission and inhibitory control have yet to find clear indications of abnormalities in performance in HD samples.
Although the neuropsychological studies are equivocal, neuroimaging and neurophysiological studies suggest that HD may be characterized by more specific deficits in error processing. For example, recent work by Mathews et al. (2015) using electrophysiological approaches demonstrated that the error-related negativity (ERN), a pre-conscious event related potential that is thought to represent a mismatch between intended and actual responses (e.g. errors) on response conflict tasks, was hypoactive in individuals with HD compared to age-matched healthy controls and to individuals with OCD. Similarly, two neuroimaging studies using functional MRI (fMRI) found different patterns of neural activity in HD compared with healthy controls and participants with OCD during error processing, despite similar rates of error commission. One study found hypoactivity in the middle frontal gyrus and hyperactivity in the right precentral gyrus during error commission (Tolin et al., 2014) and the other showed hyperactivity in orbitofrontal cortex (OFC), insula and striatum compared to healthy controls, and hyperactivity in the striatum and ventrolateral prefrontal cortex compared to individuals with OCD (Hough et al., 2016). It is notable that in these studies, there were no significant differences in the number of errors made by individuals with HD compared to those with OCD or healthy controls; rather, the pre-conscious processing of errors was abnormal.
These studies suggest that abnormalities in error processing are a core feature of HD, although further research is needed to explore which aspects of error processing (e.g., conscious vs. unconscious processing of errors) are disrupted and how these deficits are related to experiential avoidance, emotional reactivity and ultimately, to hoarding behaviors. As noted above, much of the work on emotional reactivity in HD has been done in the context of imagined or real discarding tasks, and not in the context of emotionally neutral behavioral tasks that are designed to elicit errors but not emotional responses. The present study sought to objectively explore emotional responses to errors on a simple behavioral task in HD by examining physiological responses and emotional facial expressions during error commission, and to compare these emotional responses to behavioral performance (number of errors committed, reaction time) as well as to self-reports of performance and emotional reactions to errors. We hypothesized that, in comparison to healthy controls, individuals with HD would: (1) have similar responses in the number of errors committed and reaction times during a simple behavioral response task, but would over-report the number of errors committed and endorse more negative emotional responses to errors on self-report, and (2) have normal autonomic functioning at baseline but would show enhanced physiological response and more negative facial expression during error commission.
Section snippets
Participants
Fifty-seven participants were recruited for this study, including 25 individuals with HD and 32 age-matched healthy controls (HC). HC were recruited from two ongoing research studies of neuropsychiatric disorders at UCSF: HC under age 60 were recruited from the control sample for research studies of HD, OCD, and depression at the OCD and Anxiety Clinic at UCSF, and HC ages 50 and older were recruited from the control sample for studies of dementia at the Memory and Aging Center (MAC) at UCSF.
Demographics
There were no differences in gender, age, medication rates or executive function as measured by the NAB between participant groups. HD participants were significantly less educated and more depressed than HC participants (Table 1). Of the nine individuals of our sample on medication (15.8% of the total sample), the majority were taking prescribed stimulants or anti-depressants with one person on mood stabilizers and two on combinations of anti-depressants and mood stabilizers.
Behavioral data
There were
Discussion
In this study, we examined error processing and emotional reactivity in the context of error commission on a simple, non-emotional behavioral task in individuals with HD compared with healthy controls. As expected, we found that individuals with HD had similar behavioral responses when compared to HC, including correction of errors, reaction times, and post-error slowing, although HD participants made on average 2 more errors out of 40 trials than did healthy controls. All participants also
Acknowledgments and disclosures
This work was supported by NIH grant R21 MH087748, NIH/NIA grant R01 AG030688, NIH/NIA grant P50 AG023501, NIH/NIA grant P01 AG019724, and the Hillbloom Network Program.
Authors Jessica J. Zakrzewski, MRes; Samir Datta, BA; Carole Scherling, PhD; Krystal Nizar, MD, PhD; Ofilio Vigil, MS; Howard Rosen, MD; Carol A. Mathews, MD all have no financial disclosures to declare.
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