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The resilient brain: psychological resilience mediates the effect of amplitude of low-frequency fluctuations in orbitofrontal cortex on subjective well-being in young healthy adults
Abstract
Psychological resilience reflects the capacity to bounce back from stress, which plays an important role in health and well-being. However, less is known about the neural substrate for psychological resilience and the underlying mechanism for how psychological resilience enhances subjective well-being in the healthy brain. To investigate these issues, we employed fractional amplitude of low-frequency fluctuations (fALFF) measured with resting-state fMRI in 100 young healthy adults. The correlation analysis found that higher psychological resilience was related to lower fALFF in the left orbitofrontal cortex (OFC), which is involved in reward-related processing and emotion regulation. Furthermore, the mediation analysis indicated that psychological resilience acted as a full mediator of the association between the fALFF in left OFC and subjective well-being indicators (i.e. life satisfaction and hedonic balance). Importantly, these results remained significant after controlling for the effect of gray matter volume and regional homogeneity in the region. Overall, the present study provides the further evidence for functional neural substrates of psychological resilience and reveals a potential mechanism that psychological resilience mediates the effect of spontaneous brain activity on subjective well-being.
Keywords: resilience, subjective well-being, orbitofrontal cortex, amplitude of low-frequency fluctuations
Introduction
As an important personality trait, psychological resilience is defined as the capacity to bounce back from stress (Smith et al., 2010). It plays a protective role against disorders related to stress such as post-traumatic stress disorder (PTSD) (Agaibi and Wilson, 2005). Furthermore, psychological resilience is considered as a crucial concept in the field of positive psychology, and exhibits a beneficial effect on subjective well-being (Davydov et al., 2010; Hu et al., 2015). Subjective well-being reflects people’s cognitive (life satisfaction) and affective evaluations (hedonic balance) of their lives (Schimmack et al., 2002). A lot of research has found that psychological resilience is positively associated with hedonic balance and life satisfaction (Liu et al., 2012; Di Fabio and Palazzeschi, 2015; Kong et al., 2015d; Bajaj and Pande, 2016; Satici, 2016). In this study, we tried to investigate the neurobiological underpinnings of psychological resilience and the potential mechanism that how psychological resilience influences subjective well-being in the brain with resting-state fMRI (rs-fMRI).
Although psychological resilience is a hot topic in the field of positive psychology, limited work has used fMRI to explore the neurobiological underpinnings of resilience in healthy populations. For example, Waugh et al. (2008) used task-based fMRI (tfMRI) to probe this issue and found that, when facing with a threat, all of participants had prolonged activity in the insula to the aversive stimuli, but only low-resilient participants had prolonged activity in the insula to the neutral stimuli. Furthermore, Reynaud et al. (2013) found that high resilience was associated with increased activity in the amygdala and orbitofrontal cortex when responding to stress-related stimuli. However, these tfMRI results are limited to the regions that are activated by a certain task. Because psychological resilience is a complex construct, it should be related to different brain functions. Consistent with this view, evidence from studies on disorders related to stress has demonstrated that beyond the amygdala, insula and OFC, psychological resilience is also related to other regions within the prefrontal cortex (PFC) including anterior cingulate cortex (ACC) and medial PFC (mPFC) (Liberzon and Sripada, 2008; Milad et al., 2009; Sekiguchi et al., 2015).
Although psychological resilience has been defined as a dynamic process (Lutha and Cicchetti, 2000; Masten, 2001; Waugh and Koster, 2015), it has also often been considered as a stable trait (Jacelon, 1997; Waugh et al., 2011; Waaktaar and Torgersen, 2012), so its neural underpinnings might be related to the overall brain function under task-free conditions, which can be investigated by using the rs-fMRI based on measurements of low-frequency fluctuations (LFFs, 0.01–0.10 Hz) in the BOLD signal (Fox and Raichle, 2007; Biswal, 2012). Two increasingly popular measures of LFFs [e.g. regional homogeneity (ReHo) and fractional amplitude of low-frequency fluctuations (fALFF)] reflect local properties of spontaneous brain activity, but they characterize different aspects of the regional spontaneous activity. ReHo measures the temporal synchronization of the BOLD fluctuations in a given region (i.e. short range connectivity) that may reflect the interaction and integration among local voxels (Zang et al., 2004), whereas fALFF measures the amplitude of the BOLD fluctuations of each voxel (i.e. spontaneous brain activity intensity) (Zou et al., 2008). Importantly, the ReHo/fALFF measures have been used to identify the neural marker of mental disorders (Cheng et al., 2012; Dutta et al., 2014; Liu et al., 2014) and uncover the neural basis of individual differences in behavior in normal populations (Tian et al., 2012; Zou et al., 2013; Kong et al., 2015c, 2016a,b, 2018; Xiang et al., 2016). In addition, previous studies have found that the ReHo/fALFF could successfully predict task-evoked activations and behavioral performance (Mennes et al., 2011; Yuan et al., 2013; Zou et al., 2013). Therefore, these two measures can provide a useful tool to investigate neural correlates of psychological resilience.
Recently, Kong et al. (2015d) used the ReHo measure to explore neural correlates of trait resilience, and found that higher ReHo in the ACC and insula within salience network was associated with lower trait resilience. However, as Kong et al. (2015d) mentioned, this study failed to find an association of resilience with other PFC regions such as OFC, which has been demonstrated in studies on disorders related to stress, as well as studies on healthy populations (Liberzon and Sripada, 2008; Reynaud et al., 2013; Sekiguchi et al., 2015). Because both fALFF and ReHo reflect different aspects of the regional spontaneous activity (An et al., 2013; Tian et al., 2016; Zhao et al., 2016), so we wondered whether the association of psychological resilience with other PFC regions, especially OFC can be seen by using the measures on neuronal activity magnitude (i.e. fALFF). Recently, Wang et al. (2017) found a negative association between higher fALFF in the OFC and trait hope, which is a highly related construct to psychological resilience (Lloyd and Hastings, 2009; Satici, 2016). Thus, we speculated that the fALFF in the OFC could be negatively associated with psychological resilience.
Moreover, as we mentioned previously, behavioral studies have demonstrated that psychological resilience exhibits a beneficial effect on subjective well-being (Bajaj and Pande, 2016; Satici, 2016). Importantly, some regions with the PFC related to psychological resilience (e.g. OFC and ACC) are also found to be implicated in subjective well-being (Van Reekum et al., 2007; Kong et al., 2015a,c,d, 2016a;). Notably, Kong et al. (2015d) revealed that the ReHo in the ACC related to trait resilience could significantly predict the cognitive component of subjective well-being (i.e. life satisfaction), indicating that the ACC is an important site supporting the link between cognitive well-being and psychological resilience. However, there’re still several problems needing further research. On one hand, as mentioned earlier, this study did not find any association of other PFC subregions, especially OFC with psychological resilience and life satisfaction (Liberzon and Sripada, 2008; Reynaud et al., 2013; Sekiguchi et al., 2015; Kong et al, 2015c). On the other hand, this study focused on only the cognitive component of subjective well-being, but it is generally known that subjective well-being includes a cognitive component (i.e. life satisfaction) and an emotional component (i.e. hedonic balance).
To explore these issues, we used a standard instrument to measure psychological resilience in a sample of young healthy adults (N = 100). Then, we conducted a correlation analysis to investigate the relationship of psychological resilience with the fALFF across the brain. Based on previous neuroimaging studies on resilience, we speculated that the fALFF in the OFC would be negatively associated with psychological resilience. Finally, we conducted a mediation analysis to examine how the fALFF in these regions related to resilience, especially the OFC, affects two components of subjective well-being (e.g. hedonic balance and life satisfaction) through resilience. Based on previous behavioral and neuroimaging studies on resilience and well-being, we speculated that psychological resilience would mediate the relationship of the fALFF in the OFC with two components of subjective well-being.
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