Effective emotion regulation is necessary for our daily social life. Essentially, various strategies can be employed to achieve successful emotion regulation, e.g., distraction, cognitive reappraisal, and expressive suppression (Webb et al., 2012; Morawetz et al., 2017b). Among these strategies, reappraisal, which entails the changing of the emotional value of stimuli that evokes emotions (Kanske et al., 2011; Webb et al., 2012), is the most frequently applied and studied strategy of emotion regulation (Wager et al., 2008; Kalisch, 2009; Ochsner et al., 2012; Buhle et al., 2014). Moreover, Gross and John (2003) developed a self-report Emotion Regulation Questionnaire (ERQ) to measure the dispositional use of two strategies, reappraisal (center on reinterpretation) and suppression. Assessment of this kind of personality habitude can reflect the utilization frequency of strategy, which may finally implicate the individual differences in abilities of emotion regulation. Also, more frequent use of reappraisal strategy has been demonstrated to be associated with better regulation of emotions, social interactions, and mental and physical health (Gross and John, 2003; Meyer et al., 2012; Hu et al., 2014; Picó-Pérez et al., 2018; Zaehringer et al., 2020).

The neural underpinnings related to reappraisal strategy have usually been evaluated by measurement of functional activation during experimental reappraisal tasks with functional magnetic resonance imaging (fMRI). The previous meta-analytic studies have shown that reappraisal recruits a widespread network that includes dorsomedial prefrontal cortex (DMPFC), dorsolateral prefrontal cortex (DLPFC)/superior frontal gyrus (SFG), ventrolateral prefrontal cortex (VLPFC)/inferior frontal gyrus (IFG), parietal lobes, temporal gyrus, and cingulate cortex (Phillips et al., 2008; Buhle et al., 2014; Kohn et al., 2014; Morawetz et al., 2017b). Importantly, the IFG/VLPFC is well known as a critical region for processes of selection and inhibition (Schulz et al., 2009; Kohn et al., 2014; Morawetz et al., 2017b), language (Ochsner et al., 2012; Messina et al., 2015), and social cognition (Kohn et al., 2014; Hartwigsen et al., 2019) in emotion regulation. In particular, the IFG has been observed with increased activation when multiple appropriate reinterpretations emerge and a choice must be made to achieve goal-directed behavior, as well as when required to inhibit goal-inappropriate reinterpretations (Morawetz et al., 2016; Braunstein et al., 2017).

Moreover, methods of IFG-based (with IFG serving as seed regions) functional connectivity have also been used to explore the neural correlations of reappraisal strategy in experimental settings. Morawetz et al. (2017a) defined left IFG as a seed region and examined effective connectivity between the seed region and the remaining brain regions, with reappraisal success scores as covariate. They have observed positive effective coupling between the left IFG and DLPFC, DMPFC, right middle temporal gyrus (MTG), and superior temporal gyrus (STG) during downregulation of emotion. Furthermore, in another study, Morawetz et al. (2016) found that the inhibitory effect on connectivity from IFG to DLPFC could facilitate successful reappraisal, deducing that the IFG may choose one from the many feasible goal-relevant reinterpretations actively maintained in the working memory (associated with DLPFC’s increased activity), and suppress the DLPFC as soon as the selection process is finished. On the other hand, Wager et al. (2008) found that the right IFG could effectively predict reappraisal success with some cortical and subcortical regions as mediators, such as DMPFC, SFG, inferior temporal gyrus (ITG), and subgenual anterior cingulate cortex (ACC).

Recent evidence has shown that the formation of intrinsic resting-state functional architecture is influenced by repeated task-based co-activation within a network (Mackey et al., 2013; Guerra-Carrillo et al., 2014; Uchida et al., 2014), suggesting a close correspondence between task-specific brain activation and intrinsic brain connectivity, which is reflected by resting-state functional connectivity (rsFC). In essence, Smith et al. (2009) compared task-based activation networks derived from a large database of functional imaging studies with the covarying networks from 36 subjects’ resting fMRI data, and found that these task-related networks closely matched the networks when at resting state. Intriguingly, another study using a sample of 4- to 18-year-old healthy participants found that task-related functional connectivity could even predict rsFC of up to 2 years after the initial experimental task (Gabard-Durnam et al., 2016). Thus, it seems possible that recurring activation caused by a specific task may share an association with resting-state connectivity pattern, and this may also apply to the emotion regulation domain with IFG-based functional connectivity during the reappraisal task. Besides, one study demonstrated that activation of IFG in reappraisal task is positively correlated with the frequency of dispositional reappraisal in daily life (Grecucci et al., 2013). Consequently, it can be assumed that the reappraisal task and dispositional reappraisal may share a similar IFG-based functional connectivity pattern. However, since no study has examined the association between dispositional use of reappraisal strategy and rsFC with IFG seed regions, it is uncertain whether IFG-based rsFC could also facilitate habitual reappraisal, thus resulting in better emotion regulation, although previous evidence indicates that both left and right IFG show associations with DMPFC and temporal gyrus during the performance of a reappraisal task. Nevertheless, it remains unknown whether the functional connectivity pattern of the left IFG seed concerning habitual reappraisal is the same as that of the right IFG seed.

Moreover, neural efficiency supposes that more adept individuals optimally use the functional connectivity to undertake minute neural processing and, hence, display diminished neural activity alongside the performance facilitation (Neubauer and Fink, 2009; Di Domenico et al., 2015; Curtin et al., 2019). It is anticipated that the higher the scores of dispositional reappraisal, the more frequent the use of reappraisal, and the better the ability of emotion regulation. Presumably, the neural efficiency may also be suitable for dispositional reappraisal, a daily used specific strategy of emotion regulation, with a changeable connectivity pattern along with a variation of reappraisal scores. However, there is no evidence supporting how the individual difference in frequency of reappraisal use may affect functional connectivity during the resting state. Considering the aforementioned close association between rsFC and task-related functional connectivity, we asked another question: Could it be possible that the IFG-based rsFC pattern vary with the level of frequency of dispositional reappraisal?

Therefore, in an endeavor to answer the questions raised, the present study applied seed-based rsFC analysis and prediction analysis with an aim of (1) examining whether IFG-based rsFC is related to individual dispositional use of reappraisal; (2) investigating whether habitual reappraisal related rsFC pattern of the left IFG is the same as that of the right IFG; (3) exploring whether IFG-based rsFC is specific to the frequency level of the use of dispositional reappraisal. Based on the limited evidence mentioned above, we hypothesized that dispositional use of reappraisal would be positively correlated with IFG-based rsFC and that the rsFC pattern of the left IFG and that of the right IFG would be very similar, with both showing associations with DMPFC and temporal gyrus. Moreover, according to the theory of neural efficiency (Neubauer and Fink, 2009; Di Domenico et al., 2015; Curtin et al., 2019), the individual differences in dispositional reappraisal may be associated with the difference in the IFG-based rsFC pattern, with a higher level of dispositional reappraisal corresponding to a less IFG-based rsFC.

Previous studies have emphasized the key functional role of IFG in collaboration with other regions in emotional regulation task-based functional connectivity, while the present study constitutes the first investigation into the associations between rsFC patterns of bilateral IFG and the dispositional use of reappraisal. Interestingly, we observed that medium dispositional use of reappraisal was positively related to IFG-based rsFC. Specifically, the medium habitual use of reappraisal was associated with a significant positive coupling between: (1) bilateral IFG and temporal gyrus; (2) left IFG and bilateral SPL, MCC, left IPL, and right insula; and (3) right IFG and DMPFC/ACC. However, no significant correlation emerged between left or right IFG-related rsFC and the high dispositional reappraisal use. The predictive analyses also showed that both left and right IFG-related rsFC could effectively and separately predict for individual reappraisal scores in MRG. However, IFG-related rsFC of sMRG had no significant predictive power for reappraisal scores of HRG.

In line with our hypotheses, the associations of both left and right IFG with temporal gyrus were linked to the habitual use of reappraisal. Particularly, using the reappraisal strategy altered the emotional value of stimuli by manipulating the conceptual knowledge and creating opposite interpretations. This suggests that the involvement of the semantic process is a core part of emotion regulation. Evidently, the semantic system plays a critical role in the storage and controlled retrieval of conceptual knowledge (Binder et al., 2009), contributing to representations of relevant emotional information from emotional experiences (Neumann and Lozo, 2012). Specifically, the temporal gyrus, which has often been observed with enhanced activation in reappraisal task (Goldin et al., 2008; Kanske et al., 2011; Dörfel et al., 2014), is usually considered as part of semantic system (Binder et al., 2009) and plays a role in both the storage and the strategic retrieval of semantic knowledge (Davey et al., 2016). Recent evidence on functional connectivity between IFG and MTG at both task (Zhang et al., 2019) and resting-state contexts (Kohn et al., 2014; Davey et al., 2016) indicates that the cooperation between IFG and MTG makes strategic access of semantic information possible. Similarly, the present study also revealed strong functional connectivity between IFG and temporal gyrus, alongside a positive correlation with medium habitual use of reappraisal, perhaps supporting the capacity to potentially engage and sustain semantic retrieval, in line with goal-driven control of subjective emotional feelings.

Inconsistent with our preliminary expectation, only the right IFG displayed an association with DMPFC. The DMPFC has generally been proved to be involved in semantic and self-reflective processes (Olsson and Ochsner, 2008; Binder et al., 2009), and has repeatedly been observed to be significantly activated in the reappraisal tasks (Kanske et al., 2011; Buhle et al., 2014; Morawetz et al., 2017a, 2016). In particular, DMPFC is implicated with the elaboration of the affective meaning of stimuli and representation of value information concerning mental states (Ochsner et al., 2012; Dixon et al., 2017). Thus, the right IFG, with a close connection with DMPFC, may facilitate the evaluation of the changing mental states, in relation to outcomes of appropriate or inappropriate interpretations of emotional stimuli. Besides, with a correlation with medium habitual reappraisal use, right IFG-based rsFC also showed a strong link with ACC. Recent evidence suggests that ACC constitutes a core part of the neural circuitry of valuation (Amemori and Graybiel, 2012; Bartra et al., 2013; Clithero and Rangel, 2013), playing an important role in evaluating interoceptive signals based on self-referential and conceptual emotion knowledge (Dixon et al., 2017). The evaluation role of ACC may thus facilitate a better understanding of subjective emotional feelings, by assigning conceptual meaning to these bodily sensations. Notably, through interaction with ACC, DMPFC contributes to the maintenance of mental representations of an individual’s feelings active in affective working memory (Lane et al., 2015) and may subsequently transfer these internal state information to IFG via a feed-forward mechanism (Phillips et al., 2008). Therefore, it is highly plausible that the right IFG (roles in selecting appropriate or inhibiting inappropriate interpretations from semantic memory) strongly connects with DMPFC and ACC (roles in perceiving and evaluating subjective emotional feelings), exhibiting correspondingly more frequent reappraisal skill, to achieve goal-directed emotional states.

Furthermore, as indicated above, we also observed a positive correlation between medium dispositional use of reappraisal and connectivity of left IFG with bilateral SPL, MCC, left IPL, and right insula during resting state. Consistent with the previous findings on the activation of parietal lobes in reappraisal task (Buhle et al., 2014; Morawetz et al., 2017b), our study also found an association between habitual use of reappraisal and co-activation of left IFG and parietal lobes (including SPL and IPL), which usually engage in the attention control process (Luks et al., 2007; Hutchinson et al., 2014; Salo et al., 2017; Sang et al., 2017; Wang et al., 2020). More importantly, it is documented that the parietal lobes and prefrontal gyrus engage in cognitive control by exerting influence on the temporal regions to change the semantic and perceptual representations, so as to facilitate the selection of appropriate behaviors, and the inhibition of maladaptive habitual actions (Buhle et al., 2014; Dixon, 2015). Similarly, MCC has also been found to be strongly involved in the allocation of attention to emotional information and action monitoring (McRae et al., 2008; Kragel et al., 2018). Indeed, the cognitive function of MCC in performance monitoring may help guide the changing emotional responses through reappraisal strategy in an intended way (Ochsner et al., 2012). Moreover, MCC also combines with the insula, which contains bodily information and sensations (including interoceptive representation of emotions) (Craig, 2009; Lane et al., 2015), to project the affective information to the neighboring IFG/VLPFC (Craig, 2009; Kohn et al., 2014), indicating a motivation to IFG to select an appropriate response in the final stage. During this process, IFG may work in concert with the parietal lobes and temporal gyrus to focus attention on the subjective feelings and select appropriate interpretation to obtain a desirable emotional state.

As initially anticipated, we did not observe a significant correlation between left or right IFG-related rsFC and the high dispositional reappraisal use. More so, the IFG-related rsFC pattern of MRG could not effectively predict for reappraisal scores of HRG. This supports the neural efficiency view, that the more adept the skill, the lesser the neural connectivity, but the more enhanced the performance becomes (Neubauer and Fink, 2009; Di Domenico et al., 2015; Curtin et al., 2019). However, there is a conspicuous lack of evidence on trait emotion regulation with reappraisal disposition to support our findings. Nevertheless, some promising evidence from cognitive training provides a potential explanation. For example, Vartanian et al. (2013) proved that working memory training can augment performance on divergent thinking task and lead to lower activation in the prefrontal gyrus (VLPFC and DLPFC) in adult participants, while Motes et al. (2018) found that cognitive training results in a faster processing speed along with reduced activation in the prefrontal gyrus in elderly participants. Therefore, it is possible that individuals with high-frequency daily use of reappraisal strategy, possess a more adept skill of emotion regulation, and recruit less functional connectivity between IFG and other regions in the resting state. On the other hand, the limited sample size in HRG may also be a potential reason to explain the non-significant results of both the association between rsFC and reappraisal scores, and the correlation in the internal cross-validation analysis. If so, future study should bring into consideration the sample size factor to ascertain whether the IFG-based rsFC pattern is linked to the variation of frequency level of dispositional use of reappraisal.

Overall, previous studies have emphasized the important role of the IFG in cooperation with other brain regions in task-based functional connectivity, in the selection and inhibition processes of emotional regulation. The present study expands on these findings by explicitly investigating how patterns of functional connectivity between IFG and other brain regions change during resting state, and how these changes may be linked to individuals’ habitual reappraisal use. Specifically, besides coupling with temporal gyrus in the function of general semantic control, we found that the left IFG, along with SPL, MCC, left IPL and right insula, predominantly engages in monitoring the emotional performance (cognitive control of emotion), while the right IFG, coupling with DMPFC and ACC, predominantly engages in representation of mental states (evaluation of emotion).

Despite the important contributions of our study, there are several limitations needed to be noted. Firstly, as mentioned above, the sample size of HRG is relatively smaller than that of the MRG. Possibly, there may be some other potential intrinsic functional connectivity patterns recruited by individuals with higher emotion regulation capacity. To fully understand the neural substrates of emotion regulation, more participants with a higher ability of emotion regulation need to be included in future studies. Secondly, the present study only recruited healthy participants. Although the neural association observed in these participants may provide potential neural evidence for clinical practice, the dispositional reappraisal use may show a different association with the resting-state networks in the context of emotional dysregulation. Therefore, future studies should consider a comparative analysis of the relevance of habitual strategy use and regulation networks, between patients with emotional disorders and healthy populations, to improve the clinical understanding and intervention. Finally, although we have not observed a significant association between IFG-based rsFC and suppression scores, which is also a personality trait of emotion regulation, it may exist in other potential functional hubs and neural substrates relevant to the dispositional use of the suppression strategy. Thus, future studies should explore the potential neural mechanism underlying trait suppression in both healthy and clinical populations.

In conclusion, the present study investigated the intrinsic neural underpinnings of dispositional reappraisal employing the IFG-based function connectivity approach during resting state. Our findings demonstrate that the medium dispositional reappraisal use relies on the cooperation of the functional hubs of the bilateral IFG and other regions within the emotion regulation cortex. These findings may explain how individuals cope with emotional events in daily life, as well as applied in clinical intervention for emotion-regulation-related disorders.

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

The studies involving human participants were reviewed and approved by the Local Committee for the Protection of Human Subjects of the University of Electronic Science and Technology of China. Written informed consent to participate in this study was provided by the participants.

WL, JZ, ZJ, and LL conceived and designed the experiments. WL performed the experiments. WL and KX analyzed the data. WL wrote the main manuscript text. RN revised the manuscript. All authors reviewed the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.