Differential patterns of brain activation between hoarding disorder and obsessive-compulsive disorder during executive performance

Abstract

BackgroundPreliminary evidence suggests that hoarding disorder (HD) and obsessive-compulsive disorder (OCD) may show distinct patterns of brain activation during executive performance, although results have been inconclusive regarding the specific neural correlates of their differential executive dysfunction. In the current study, we aim to evaluate differences in brain activation between patients with HD, OCD and healthy controls (HCs) during response inhibition, response switching and error processing.MethodsWe assessed 17 patients with HD, 18 patients with OCD and 19 HCs. Executive processing was assessed inside a magnetic resonance scanner by means of two variants of a cognitive control protocol (i.e. stop- and switch-signal tasks), which allowed for the assessment of the aforementioned executive domains.ResultsOCD patients performed similar to the HCs, differing only in the number of successful go trials in the switch-signal task. However, they showed an anomalous hyperactivation of the right rostral anterior cingulate cortex during error processing in the switch-signal task. Conversely, HD patients performed worse than OCD and HC participants in both tasks, showing an impulsive-like pattern of response (i.e. shorter reaction time and more commission errors). They also exhibited hyperactivation of the right lateral orbitofrontal cortex during successful response switching and abnormal deactivation of frontal regions during error processing in both tasks.ConclusionsOur results support that patients with HD and OCD present dissimilar cognitive profiles, supported by distinct neural mechanisms. Specifically, while alterations in HD resemble an impulsive pattern of response, patients with OCD present increased error processing during response conflict protocols.

Abnormal white matter structure in hoarding disorder

“…A resting-state fMRI study also showed abnormal functional connectivity in the frontoparietal network in patients with HD (Levy et al, 2019). Therefore, decreased FA in the left SLF reflects alterations in WM in the frontoparietal network in these patients and may be associated with cognitive impairments, such as task-switching and inhibition, as shown in previous studies (Hough et al, 2016;Sunol et al, 2020).…”

“…The ATR is a corticothalamic and thalamocortical projection fiber bundle that connects the medial thalamic nuclei to the dlPFC, vlPFC, and OFC bilaterally via the ALIC and ACR (Jang and Yeo, 2014). Previous MRI studies have shown evidence of abnormal neural activity and volumetric changes in the dlPFC, vlPFC, OFC, and thalamus in patients with HD (An Hough et al, 2016;Levy et al, 2019Levy et al, , 2021Sunol et al, 2020;Tolin et al, 2009Tolin et al, , 2014Yamada et al, 2018). Patients with HD were found to have both WM tract alterations in the ATR and ALIC in the current study and abnormal neural activity in the PFC and thalamus according to preliminary research, which are anatomically connected by the ATR; therefore, patients with HD may have dysfunction in the frontothalamic circuit, which is thought to play an important role in executive functions, including working memory (Mamah et al, 2010), attention (Jagtap and Diwadkar, 2016), reward processing (Coenen et al, 2012), and decision-making (Sieveritz et al, 2019).…”

“…The third branch (SLF III) connects the intraparietal sulcus and inferior parietal lobule to the inferior frontal gyrus (BA 44,45,47)" (Thiebaut de Schotten et al, 2012). Previous MRI studies indicated that patients with HD showed different task-related or resting-state activation in these brain regions, including the precuneus and superior, middle, and inferior frontal gyri, which are connected by the SLF (Hough et al, 2016;Levy et al, 2019Levy et al, , 2021Stevens et al, 2020;Sunol et al, 2020;Tolin et al, 2009Tolin et al, , 2014. The SLF contributes to a broad range of cognitive functions, including visuospatial processing, attention, and working memory (Nakajima et al, 2020).…”

“…Functional magnetic resonance imaging (fMRI) has shown that patients with HD have abnormal activation in the left dorsolateral prefrontal cortex (dlPFC) and frontal pole cortex (FPC) and right precentral gyrus during the go/no go task (Tolin et al, 2014); furthermore, Hough et al found these patients showed greater activation in the bilateral orbitofrontal cortex (OFC), right ventrolateral prefrontal cortex (vlPFC), anterior cingulate cortex, and mid-posterior corpus callosum (Hough et al, 2016). During the stop-signal and switch-signal tasks, patients with HD showed greater activation in the right OFC during successful response switching and less activation in the right dlPFC, OFC, precentral gyrus, and bilateral dorsomedial prefrontal cortex during error processing (Sunol et al, 2020). Moreover, Levy et al found that their study participants with HD had abnormal functional activation in the bilateral dlPFC, OFC, FPC, medial and lateral temporal cortices, and amygdala during discarding decisions that provoked subjective distress (Levy et al, 2021).…”

Inhibitory control in obsessive compulsive disorder: A systematic review and activation likelihood estimation meta-analysis of functional magnetic resonance imaging studies

“…However, new studies have since been published, and existing ALE meta -analyses do not meet the current standards for type I error control ( Eickhoff et al, 2016 ). Moreover, several recent experiments have not found significant case-control differences during inhibitory control ( Hollestein et al, 2021 , Hough et al, 2016 , Pagliaccio et al, 2019 , Suñol et al, 2020 ) , and recent prominent publications have sparked serious concerns over the reliability and reproducibility of neuroimaging research ( Marek et al, 2022 , Poldrack et al, 2017 ). This raises the question of whether previous meta -analytical findings are replicable when integrating data from new studies while adhering to contemporary recommendations for conducting meta -analyses.…”