The relationship between EEG theta/beta ratio and response inhibition in autogenous and reactive obsessions

Obsessive-Compulsive Disorder (OCD) is characterized by dysfunction within underlying inhibitory processes which is thought to represent the obsessions and compulsions seen throughout OCD (Chamberlain et al., 2005). This dysfunction has been demonstrated throughout various inhibitory tasks such as the Stroop, go/no-go, flanker, and stop-signal tasks (Bannon et al., 2002; Enright and Beech, 1993; Mar et al., 2022; Richter et al., 2012). Furthermore, a meta-analysis investigating the role of inhibitory deficits in various psychopathologies determined that OCD was the most strongly associated with inhibitory deficits (Lipszyc and Schachar, 2010). However, research investigating the neural underpinnings of these inhibitory deficits within OCD have been inconsistent, specifically for inhibition-related electrophysiological findings such as the P3 and N2 event-related potentials (see Perera et al., 2019 for a review). This may be due to the heterogenous nature of OCD which presents differently across individuals (McKay et al., 2004). Accordingly, recent neuroimaging work has started to examine inhibitory deficits associated with different OCD subtypes using clinical samples diagnosed with OCD (Fan et al., 2016, 2023; Xia et al., 2020), such as the Autogenous-Reactive Obsession (AO-RO) OCD subtyping taxonomy (Lee and Kwon, 2003).

The AO-RO taxonomy proposed by Lee and Kwon (2003) categorized obsessions into two subtypes (Lee et al., 2005a, 2009; Lee and Telch, 2010; Yucens et al., 2024). AO are repetitive thoughts or urges (e.g., sexual, aggressive, religious) that are perceived as repulsive, distressing, and threatening due to their presence or intrusions in the mind. In contrast, RO are repetitive thoughts that arise in response to destressing external stimuli or triggers perceived as threats needing correction (e.g., suspected germs, accidents, disarrangement; Lee and Kwon, 2003). Although more clinical replications are warranted, previous research with the AO-RO taxonomy has demonstrated the validity of this subtype model within OCD patients (Lee et al., 2005b, 2005c; Yucens et al., 2024). To further investigate AO-RO neurocognitive differences Fan et al. (2016) investigated inhibitory deficits for OCD patients, categorized into AO or RO groups based on their primary obsessional presentation, compared to healthy controls. On the emotional stroop task (measuring interference inhibition through attentional control), AO's, compared to RO's and healthy controls, demonstrated inhibitory deficits on the P2 (measuring stimulus detection in the presence of conflict or interference; Finke et al., 2011) and N450 (measuring inhibitory efficiency; West and Alain, 2000) event-related potentials (Fan et al., 2016). Additionally, on the stop-signal task (measuring action cancellation), both AO's and RO's, compared to the healthy controls, demonstrated inhibitory deficits on the stop-P3 (reflecting the inhibition of motor response; Gajewski and Falkenstein, 2013) event-related potential (Fan et al., 2016). These findings were also congruent with recent resting-state fMRI findings from OCD patients that suggest AO is primarily associated with deficits in inhibition regions relating to top-down cognitive and attentional control compared to RO and healthy controls (Fan et al., 2023; Xia et al., 2020). Collectively, these results demonstrate the potential utility of the AO-RO taxonomy in further characterizing the electrophysiological indices of inhibitory deficits associated with OCD.

Various EEG analytic methods have been previously explored to characterize OCD including event-related potentials (e.g., Fan et al., 2016; Perera et al., 2023a; Raggi et al., 2021), oscillatory power (e.g., Boo et al., 2023; Dell'Acqua et al., 2023; Suzuki et al., 2023), phase coherence (e.g., Perera et al., 2023b; Suzuki et al., 2023), and connectivity analyses (e.g., Perera et al., 2023a; Smith et al., 2020). However, previous electrophysiological work has demonstrated that frequency band power ratios have high test-retest reliability within individuals (Angelidis et al., 2016). Specifically, the ratio between theta and beta (Theta/Beta ratio; TBR) power has been shown to index cognitive and attentional control in healthy adults (Angelidis et al., 2016; Putman et al., 2010, 2014). Furthermore, it has been shown to be sensitive to changes in stress, sleep apnea, attention-deficit/hyperactive disorder (ADHD), and executive dysfunction in Lewy body disease (Arns et al., 2013; Baik et al., 2022; Li et al., 2022; Wen and Aris, 2020). Given the connection between OCD and inhibitory processes that require cognitive and attentional control, TBR may function as a reliable index of the inhibitory deficits seen within OCD using the AO-RO taxonomy.

To date, EEG markers of inhibitory deficits within OCD have been inconsistent across studies. However, the AO-RO taxonomy may contribute to addressing these heterogenous findings as suggested by previous work (Fan et al., 2016, 2023; Xia et al., 2020). TBR demonstrates potential to function as a reliable biomarker that may discriminate the inhibitory deficits seen within AO and RO. Thus, the principal aim of the present study was to examine if TBR can function as a neural correlate to further characterize distinguishable inhibitory differences within OCD using the AO-RO taxonomy. Given that OCD is driven by inefficient and excessive cognitive control systems, it is predicted that elevated TBR will index this abnormality (Clarke et al., 2019; McLoughlin et al., 2022; Wen and Aris, 2020). This was investigated within two tasks of inhibition (i.e., interference and action cancellation) to examine TBR more broadly within relevant inhibitory processes. Therefore, we hypothesize that, in contrast to RO severity, AO severity will be predominantly associated with elevated TBR during inhibitory processing, reflecting AO's abnormal top-down cognitive and attentional control during inhibitory processing.

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