title: Emotional Interference Inhibition − A Neural Mechanism Linking Behavior and Resilience
Creators: name: Dietrich, Anya
Publisher: name: UNSPECIFIED
Year: 2023

description: Background All living organisms in complex environments are frequently and inevitably exposed to various emotional stimuli during stressful life events, which have the potential to induce stress or specific emotional states. These emotions can drive them to excel or disastrously interfere with the course of their lives. Consequently, the adequate and beneficial processing of these stimuli is vital for survival. As an evolutionary adaptive process, reoccurring threatening and emotional stimuli are processed automatically, reflexively, preferably and prioritized (James, 1890; Tooby and Cosmides, 1990). As a result, neural processing resources are directed towards emotional stimuli at the expenses of other non-emotional processing or activities (Öhman et al., 2001), such as goal-directed cognitive processes. However, these processes can be equally important for survival as they guarantee, for example the satisfaction of basic needs, such as foraging or mating, as well as adaption to changing conditions, solving of problems, making decisions, planning, or the fostering of social cooperation. The delicate balance and optimal integration of emotional and cognitive processing are essential for optimal functioning. This oftentimes requires shielding of the cognitive process from an emotional interference. Emotional interference inhibition refers to the capacity to effectively suppress the disruptive impact of interfering emotional stimuli. Unfortunately, its failure is often associated with mental health disorders, such as in anxiety or depressive disorders or in post-traumatic stress disorder (Etkin and Schatzberg, 2011; Zetsche and Joormann, 2011; Kronhaus et al., 2006; Bremner et al., 2004). On the other hand, when emotional interference inhibition functions effectively, it can contribute to mental well-being and promote resilience (Kalisch et al., 2015). Resilience is a complex and multidimensional concept referring to the ability to maintain mental health in the face of life adversity such as trauma or stress by adapting, recovering, bouncing back, or even thriving (Seery et al., 2010; Kalisch et al., 2015). Importantly, resilience does not revolve around avoiding or eradicating negative life experiences or stressors. Instead, resilience emphasizes the significance of adequately processing these events, enabling individuals to engage in beneficial thoughts and behaviors to cope effectively. Therefore, in recent years, research studies focused more and more on investigating the mediating neurobiological mechanisms. Among those, one neurobiological resilience mechanism that has gained significant attention is emotional interference inhibition (Kalisch et al., 2015). Nevertheless, despite the growing interest in emotional interference inhibition, many questions still remain unanswered. The current work seeks to shed light on the following unresolved questions: Which Cognitive Inhibitory Subcomponent is Vulnerable to Emotional Interferences? The first study (The Impact of Emotional Interference on the Subcomponents of Cognitive Inhibitory Processes) of the current work investigated the impact of emotional interference on various subcomponents of cognitive inhibitory processes. The impact of emotions on cognitive inhibitory processes is particularly relevant, as these processes are essential for goal pursuit and overall well-being, and have been found to be overlapping though separable (Stahl et al., 2014). However, the extent to which different subcomponents of cognitive inhibitory processes are susceptible to emotional interference remains unclear. In this study, we investigated the vulnerability of cognitive inhibitory subcomponents to emotional interference using a systematic behavioral test battery including an emotional Flanker task, an emotional Stop Signal task, an emotional Recent Probes task, and a Cognitive Emotion Regulation task in a large cohort of healthy participants (N = 121). These tasks address several cognitive inhibitory subcomponents such as stimulus interference inhibition, proactive interference inhibition, response inhibition, and behavioral inhibition. Our results revealed that some subcomponents of cognitive inhibitory processes exhibited emotion-cognition interaction effects, indicating varying degrees of susceptibility to emotional interferences. Among these subcomponents, stimulus interference inhibition emerged as a particularly vulnerable and critical process, displaying clear interaction effects between emotion and cognition. This finding highlights the importance of inhibiting interfering emotional stimuli for goal-pursuit and well-being, which can be particularly relevant in the context of mental health disorders such as major depression, bipolar disorder, and post-traumatic stress disorder. Furthermore, our study demonstrated that emotional interference significantly affected behavioral performance, as evidenced by slower reaction times and lower accuracies in tasks involving emotional stimuli compared to neutral stimuli. Emotions interfered significantly with cognitive inhibitory processes in various tasks, including the Flanker task, Recent Probes task, and Cognitive Emotion Regulation task. However, the Stop Signal task did not exhibit significant emotion-cognition interaction effects, suggesting that certain subcomponents may be less vulnerable to emotional interference. However, the only task with clear emotion-cognition interaction effects associated with inhibitory control was the Flanker task. These findings contribute to our understanding of the complex interplay between emotion and cognition, highlighting the differential vulnerability of cognitive inhibitory subcomponents to emotional interference. Specifically, the identification of stimulus interference inhibition as a particularly susceptible subcomponent emphasizes its clinical relevance and underscores the importance of targeting this process in interventions aimed at improving emotional interference inhibition for well-being and mental health. Future research should explore the underlying neural mechanisms and generalize these findings to different populations and mental health disorders. What are the Neural Correlates of Emotional Interference Inhibition? The second study (Neural Mechanisms of Emotional Interference Inhibition) delved into the neurophysiological mechanisms underlying emotional interference inhibition in the brain, as it is considered a general neurobiological resilience mechanism. Building upon the findings of the first study, which identified stimulus interference inhibition as particularly vulnerable to emotional interferences, this study aimed at investigating the neural activity derived from the electroencephalography (EEG) recordings of the same emotional Flanker task employed in a large cohort of healthy participants (N=121). By pairing the large cohort with state-of-the-art EEG/FEM beamforming, we obtained high temporal and fMRI-equivalent spatial resolution. Spatially, emotion and cognition processing overlapped in the right inferior frontal gyrus (rIFG), specifically in pars triangularis. Temporally, emotion and cognition processing overlapped during the transition from emotional to cognitive processing, with a stronger interaction in β-band power leading to worse behavioral performance. Despite functionally segregated subdivisions in rIFG, frequency-specific information flowed extensively within IFG and top-down to visual areas (V2, Precuneus) — explaining the behavioral interference effect. Thus, for the first time, we here show the neural mechanisms of emotional interference inhibition in space, time, frequency, and information transfer with high temporal and spatial resolution, revealing a central role for β-band activity in rIFG. Moreover, our results support the idea that rIFG plays a broad role in both inhibitory control and emotional interference inhibition, as it is a site of convergence in both processes. Furthermore, our results have potential clinical implications for understanding dysfunctional emotion-cognition interaction and emotional interference inhibition in psychiatric disorders, e.g., major depression and substance use disorder, in which patients have difficulties in regulating emotions and executing inhibitory control. What is the Association of Emotional Interference Inhibition and Resilience? The third study (Emotional Interference inhibition and Resilience) aimed to explore the relationship between resilience and emotional interference inhibition, a cognitive process involved in regulating emotions and cognitive performance. The Longitudinal Resilience Assessment (LORA) study employed a large cohort of participants (N = 1139) across a wide age range, monitoring their naturally occurring life stressors and mental health outcomes over time. Psychophysical measures of emotional interference inhibition, including reaction time and accuracy, were obtained through an emotional Flanker task in accordance with study 1 (The Impact of Emotional Interference on the Subcomponents of Cognitive Inhibitory Processes) and study 2 (Emotional Interference inhibition and Resilience). Emotional interference inhibition in the domain of stimulus interference inhibition predicted prospective individual resilience. In agreement with Study 1, the results showed that emotional interference had a significant impact on behavioral performance, with negative emotional stimuli negatively affecting accuracy and reaction time, indicating the disruptive effects of emotional interference on cognitive performance. Notably, resilient individuals exhibited better emotional interference inhibition, particularly in the domain of stimulus interference inhibition as measured by reaction time. This suggests that resilient individuals have more cognitive resources and are better able to manage emotional interference during demanding cognitive tasks. Furthermore, the findings highlight the importance of stimulus interference inhibition as a critical factor for resilience outcomes and suggest its potential as a target for interventions aimed at enhancing resilience. Understanding the relationship between emotional interference inhibition and resilience is crucial for developing effective strategies to promote mental health and well-being in the face of life adversity. Future research should explore the potential of stimulus interference inhibition as an intervention target to enhance resilience. Conclusio The current work contributes significantly to the understanding of the complex interplay of emotion and cognition by investigating the neural mechanisms of emotional interference inhibition and its association to behavior and resilience. Three studies were presented that contribute to the understanding of emotional interference inhibition in general and its function as a neurobiological resilience mechanism. Stimulus interference inhibition, which is closely related to the processing of interfering cognitive or emotional visual stimuli, is a particularly vulnerable inhibitory subcomponent. This is in line with Stahl et al. (2014) supporting a certain separability of cognitive inhibitory subcomponents. It suggests that proficient cognitive inhibition fosters emotional interference inhibition, possibly by requiring fewer processing resources or by overall better inhibitory processing. The early inhibition of irrelevant stimuli before processing them at higher-order levels aligns with the idea that affective or threatening stimuli are processed bottom-up and reflexively (James, 1890; Tooby and Cosmides, 1990). It further indicates that early stages of the processing hierarchy are specifically vulnerable to emotional interferences, whereas later stages forward interferences once they are incorporated, even though this might elicit faulty responses. Furthermore, we identified, transient emotional interference inhibition in the right inferior frontal gyrus (rIFG), particularly in pars triangularis. Our findings suggest that IFG serves as a general inhibitor of emotional and non-emotional processes. It influences stimulus processing and thereby potentially stimulus interference inhibition through top-down modulations. Additionally, the activity of IFG is associated to behavior and resilience, thereby supporting the idea of Kalisch et al. (2015) that emotional interference inhibition is a resilience mechanism. Especially as resilient individuals exhibit better emotional interference inhibition, indicating enhanced cognitive resources. In conclusion, our findings suggest that individuals with higher levels of resilience demonstrate enhanced capacity to employ emotional interference inhibition and that emotional interference inhibition is executed by IFG shaping stimulus processing and thereby critically determining the percept that preconditions behavioral responses and appraisals or reappraisals and thereby shape resilience. These findings have valuable implications for fostering resilience, promoting well-being, and improving mental health outcomes.