Elsevier

Brain and Cognition

Volume 146, December 2020, 105631
Brain and Cognition

The role of frontal-subcortical connectivity in the relation between coping styles and reactivity and downregulation of negative emotion

https://doi.org/10.1016/j.bandc.2020.105631Get rights and content

Highlights

  • Maladaptive coping styles were associated with depressive symptoms and trait anxiety.

  • Associations of coping and emotion were mediated by amygdala-frontal connectivity.

  • Coping styles were related to connectivity in top-down-control-related prefrontal regions.

  • Results suggest coping styles influence emotion regulation and related brain systems.

Abstract

Coping styles (CS) reflect individuals' habitual use of strategies for coping with negative events in daily life. Although research into coping has not reached consistent agreement about classifying coping strategies as either inherently adaptive or maladaptive, the influence of maladaptive CS on mental health is noticeable. CS might also be related to emotion regulation and associated brain systems. Participants (N = 165) completed measurements of CS, trait emotions including trait anxiety, depressive symptoms and happiness and then performed an emotion regulation task, in conjunction with functional MRI. Individual differences in maladaptive CS use were associated with higher trait negative emotionality and higher state reactivity of negative emotion. Concurrent bilateral amygdala-right middle frontal gyrus (MFG) connectivity during passive negative stimulus processing mediated the relation between maladaptive CS and negative emotion ratings. Psychophysiological interaction analyses showed that maladaptive and adaptive CS were linked to patterns of frontal-subcortical connectivity during state emotion regulation. These results suggest that maladaptive CS might be related to negative emotion processing and weaker spontaneous regulation and indicate that maladaptive CS is a risk factor in individual mental health.

Introduction

In response to academic, interpersonal and financial stressors, young adults use a variety of cognitive and behavioral strategies to cope (Folkman and Moskowitz, 2004, Legerstee et al., 2011, Litman, 2006). Coping styles (CS) reflect a generalized habitual preference for specific strategies in solving one's behavioral and emotional problems. It has been suggested that CS can be distinguished as either adaptive or maladaptive (Billings and Moos, 1981, Carver et al., 1989, Lazarus and Folkman, 1987). Maladaptive CS have been linked to psychopathology symptoms and suggested as risk factors for the development and persistence of psychopathology (Aldao et al., 2014, Aldao and Nolen-Hoeksema, 2010). For example, individuals with depression frequently report maladaptive use of rumination, which refers to repeatedly recalling negative emotional experiences. Negative self-views and depressive symptoms have also been linked to the use of self-blame or punishment, which refers to aggression toward oneself (Plaufcan et al., 2012, Vasconcelos et al., 2017). In contrast with maladaptive CS, adaptive CS include positive reappraisal—typically characterized as reinterpreting negative emotional events as positive or benign—and acceptance of emotions, which function as protective factors against psychopathology (Aldao et al., 2010, Matsumoto et al., 2008, Hofmann et al., 2010).

Inconsistent ideas have arisen regarding the tendency to classify coping strategies as universally adaptive or maladaptive; some empirical evidence shows that the effectiveness of coping strategies such as suppression and reappraisal on mental health is not uniform (Webb et al., 2012). More recent research has emphasized that coping efficacy may depend on fit between coping strategies and contextual demands (Aldao et al., 2015, Bonanno and Burton, 2013). Although there is no agreement on the effectiveness of adaptive CS on mental adjustment, it is noticeable that some maladaptive coping strategies are considered to have consistently negative effects on mental health. For example, cognitive reappraisal is effective only when the intensity of a negative stimulus is moderate (Sheppes et al., 2014), whereas rumination is highly correlated with depressive symptoms, regardless of emotional intensity (Aldao et al., 2010). Previous results also suggest that the various subtypes of maladaptive coping are positively correlated with one another, as are various specific forms of adaptive coping. For example, rumination and worry were highly correlated in participants with high depression levels and statistically mediated the relation between self-compassion and depression (Raes, 2010). Another example of maladaptive CS is catastrophic worry, which was coined by pain researchers to better understand the cognitive and emotional processes involved when individuals catastrophize about pain symptoms and anxiety (Flink et al., 2013). Adaptive and maladaptive coping strategies thus may load onto two latent factors and reflect coping style constructs that can then be used to predict emotional experiences and outcomes. One primary goal of this study was to investigate whether individual differences in composite factors for maladaptive and adaptive CS would be associated with emotional health at both the state and trait level.

Previous findings have suggested that maladaptive CS play a more critical role in psychopathology than adaptive CS (Aldao et al., 2010, Aldao et al., 2014, Aldao and Nolen-Hoeksema, 2010). A potential explanation for this difference is that the utility of adaptive CS in emotion regulation might be context-dependent and require volitional action, whereas the frequent use of maladaptive CS might become an individual’s default and automatic method of coping with affective states (Aldao & Nolen-Hoeksema, 2012). Automatic responses and behavioral biases toward emotionally relevant stimuli would be elicited from the habitual use of maladaptive CS such as avoidance, worry and rumination (Dan et al., 2016, Klemanski et al., 2017, Schäfer et al., 2017). To test this conjecture, we investigated the relation between the two types of CS (maladaptive and adaptive) and measures of trait emotional health, such as anxiety, depression and happiness, separately.

In the current study, we measured individual CS by using a questionnaire that is designed to capture how people usually deal with their negative feelings and stressful events. Coping with stress is intimately related to emotion regulation (Zimmer-Gembeck et al., 2014). Emotion regulation mainly focuses on the use of emotion-focused coping regulatory strategies to increase, maintain or decrease emotional trajectories (Gross, 1998, Gross, 2002, Gross and Thompson, 2007). This regulatory process reflects individual state regulatory ability. Emotion regulation has also been conceptualized as cycles of perception-valuation–action (PVA) sequences, which can be either conscious or unconscious (Etkin et al., 2015, Gyurak and Etkin, 2014). Previous PVA sequences serve as an input for the next PVA sequence and influence how people perceive, valuate and act in response to the next emotional stimuli. Healthy adults show significant variability in their emotional responses, and also in their capacity for emotion regulation. Individual CS developed from the accumulation of previous PVA sequences might affect individual's state emotional reactivity and regulation. It has been suggested that young adults are still undergoing maturation of prefrontal regions, which mainly function to modulate behavioral control and emotional management (Akyurek, 2018). In the current study, we investigated the association of adaptive and maladaptive CS with the perception and regulation of negative emotions in a laboratory setting, as well as corresponding individual differences in their underlying brain processes.

Negative feelings, generated in the process of valuation, have been linked to activity in the amygdala, a region of the brain consistently showing involvement with key affective processes in the reactivity, processing, and regulation of emotional experiences (Delgado et al., 2008, Lapate et al., 2016, Simon et al., 2016). Consequently, we hypothesized that higher use of maladaptive CS would be associated with higher negative emotional reactivity and corresponding brain activity in the amygdala. Increasing the intensity of a negative emotion stimulus (e.g., sadness and anger) has been linked to greater activity in the ventral prefrontal cortex and anterior cingulate cortex, which may be interpreted as indicative of automatic regulation processes in reaction to negative emotions (Blair et al., 1999, Phan et al., 2002, Phillips et al., 2003). Therefore, we tested whether maladaptive CS would also be associated with changes in amygdala-seed functional connectivity (FC) during emotional reactivity, which might involve weaker automatic regulation and consequently influence individuals' negative emotional reactivity.

Although different types of CS may be related to different specific neural substrates, some brain systems are consistently implicated in various forms of emotion regulation. For instance, a core top-down control network has been shown to be independently recruited in regulatory processing of emotions. This network includes the bilateral inferior frontal gyrus (IFG), superior frontal gyrus (SFG), ventral prefrontal frontal cortex (vPFC), and dorsal PFC (Morawetz et al., 2017, Morawetz et al., 2017). The prefrontal cortex has been consistently implicated in the reprocessing, selecting and understanding of emotional information, cognitive and attentional control (Etkin et al., 2015, Li et al., 2020, Li et al., 2020, Rêgo et al., 2015), and inhibiting context-inappropriate responses (Ochsner et al., 2012, Poppe et al., 2018). In addition, the anterior cingulate cortex (ACC) has been shown to be involved in performance monitoring of emotional conflict (Inzlicht et al., 2015, Veroude et al., 2013). In addition to its activity being implicated in emotion regulation, connectivity between this top-down control network and subcortical regions is also important in emotion regulation and individual differences in regulatory success. One neuroimaging study revealed that top-down control systems recruited the dorsolateral ACC and ventrolateral PFC, which inhibited threat outputs from the amygdala under high cognitive load (Clarke & Johnstone, 2013). The successful regulation of anxiety has been linked to greater connectivity between the right amygdala and bilateral IFG, ventromedial PFC and ACC, which has been implicated in the control of prefrontal cortex sub-regions to reduce amygdala activation (Gold et al., 2015). In short, prefrontal-subcortical pathways could be considered essential neural circuitry in the effectiveness of downregulation. A synthetic review has suggested that the effects of different strategies on negative emotion downregulation were associated with prefrontal-amygdala connectivity strength (Ochsner et al., 2012). Therefore, we hypothesized that participants' habitual CS use would be associated with FC between frontal and subcortical regions and that these systems would also be related to individuals’ abilities to regulate state negative emotions.

In the current study, our main goal was to investigate the associations of maladaptive and adaptive CS with trait emotional health and state reactivity and downregulation of negative emotions assessed in a reappraisal strategy emotion regulation paradigm (Beauchamp et al., 2016, Paschke et al., 2016), as well as the potential neural correlates of both. First, we calculated individuals’ adaptive and maladaptive CS using a variety of self-report measures and used a two-factor solution to estimate latent variables for coping strategies (Aldao et al., 2010, Aldao et al., 2014). Second, we investigated the relation between the two CS factors and trait emotional health, including anxiety, depression and happiness. Third, we examined the associations of maladaptive CS use with negative emotional reactivity and its potential neural substrates. Finally, we investigated the associations of both maladaptive and adaptive CS with individuals’ performance on negative emotion downregulation. We expected that maladaptive CS would be more strongly associated with trait negative emotion, compared to adaptive coping. Furthermore, we expected high maladaptive CS to be related to higher state negative reactivity and decreased amygdala-PFC functional connectivity. During emotion regulation processing, we predicted that maladaptive CS would be linked to weaker PFC-seed connectivity and decreased success in downregulating negative emotions. In contrast, we anticipated adaptive CS would be linked to stronger FC between the PFC and subcortical areas and better downregulation abilities.

Section snippets

Participants

This study is part of an ongoing project to investigate the associations of brain structure and function with creativity and mental health (Chen et al., 2018, Chen et al., 2019, Li et al., 2020, Li et al., 2020). The fMRI task data used in the current study overlapped with data used in another published research paper (Yu et al., 2020). A previous similar fMRI study used NeuroPower analyses with false discovery rate correction for multiple comparisons to estimate sample size by using the map of

Factor analysis

Based on established scoring manuals, we reverse coded select items and computed subscale scores for each measure. We performed a factor analysis on the 15 subscales that represented different coping strategies, such as cognitive reappraisal, acceptance, rumination, punishment, worry and so on (165 participants, SI Appendix, TableS2). A parallel analysis implemented using Mplus recommended a two-factor solution in the exploratory factor analysis. We removed four items with low factor loadings

The association between adaptive and maladaptive CS and emotional health

The descriptive information for all behavioral variables is displayed in Table 1. Correlation analyses showed that adaptive and maladaptive CS were positively correlated (r = 0.281, p < 0.001), which is consistent with previous studies (Aldao et al., 2014, Aldao and Nolen-Hoeksema, 2012). To further validate the structure of and difference between the two factors, we investigated whether these two factors were associated with individual emotional health. Results showed that adaptive CS was

Discussion

The present study provides insight into whether a two-factor model of coping styles was associated with individual differences in trait negative emotion, reactivity and downregulation of negative emotions, as well as underlying patterns of neural activity and connectivity. Variation in the specific coping strategies that individuals reported using in daily life was highly related to one another, loading onto latent factors for maladaptive and adaptive CS. This two-factor model was further

Conclusion

In the present study, we found that maladaptive CS plays a critical role in emotional well-being, showing stronger associations with trait and state negative emotions, when compared to adaptive CS. Delineating the associations between CS and emotional well-being could help us better understand protective and risk factors for mental health and provide effective intervention. In addition, our current work provides support for theories that emphasize the importance of frontal-subcortical

Funding

This research was supported by the National Natural Science Foundation of China (31470981; 31571137; 31500885; 31600878; 31771231), Natural Science Foundation of Chongqing (cstc2015jcyjA10106). Scott Blain was supported by the National Science Foundation Graduate Research Fellowship Program (1348264).

CRediT authorship contribution statement

Xiaoqin Wang: Conceptualization, Investigation, Data curation, Formal analysis, Visualization, Writing - original draft. Scott D. Blain: Conceptualization, Methodology, Writing - review & editing. Dongtao Wei: Conceptualization. Wenjing Yang: Conceptualization, Writing - review & editing. Junyi Yang: Data curation. Kaixiang Zhuang: Methodology. Li He: Methodology. Colin G. DeYoung: Conceptualization, Methodology, Writing - review & editing. Jiang Qiu: Conceptualization, Investigation,

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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