In the present study, CM experiences—particularly emotional abuse—were found to be associated with increased likelihood TAF. Enhanced responses in the anterior insula and dACC, which are the two core hubs of SN, were associated with CM experiences and TAF tendency during the fMRI TAF task. To the best of our knowledge, this is the first study to demonstrate a link between neural correlates of TAF tendency and CM experiences.
Consistent with the findings of a previous study (Berman et al., 2013b), our study found a significant relationship between emotional abuse and TAF likelihood. Briefly, victims of emotional abuse may believe that certain negative thoughts cause or increase the likelihood of certain negative events. Although the evidence that directly links emotional abuse to TAF is limited, several studies including a meta-analysis have reported that the emotional type of CM has more negative effects on depressive symptoms (Gibb et al., 2007; Spertus et al., 2003; Humphreys et al., 2020). Furthermore, compared with healthy controls, people with depression exhibited higher total score of TAFS (Berle and Starcevic, 2005). Similar to TAF, ruminative cognitive style—a type of metacognition—acts as a moderator in the relationships between emotional abuse and depressive symptoms or emotional dysregulation (Li et al., 2020; Raes and Hermans, 2008). Our findings suggest that emotional abuse, increased metacognitive belief in the likelihood of negative events, and negative affect, such as depression or anxiety, may closely influence each other.
The current fMRI study revealed that the TAF task activated several brain regions, including the anterior insula, dACC, caudate, medial prefrontal cortex, precuneus, and amygdala. Although our previous fMRI study using the TAF task reported activation in the caudate, medial prefrontal cortex, precuneus, and anterior insula (Lee et al., 2019), the current TAF task activated a broader and greater number of brain regions. Our previous TAF task did not include neutral sentences as control stimuli, and the anticipated effects of the name phase were identified as a limitation (Lee et al., 2019). In the present study, the TAF task using neutral sentence stimuli demonstrated increased activity in brain regions. The present study therefore supports the reliability of the TAF task, and the current task was improved in this study with more acceptable contrast.
Furthermore, CM experiences were related to anterior insula activities during the TAF task. Our stimuli elicited interoceptive awareness of negative affect (e.g., serious injury from a car accident), prediction of self and other-related affects, and decision-making in uncertain context (e.g., I wish my mother would); there were pieces of evidence that the anterior insula could play central roles in these functions. First, increased activity in the anterior insular cortex is observed during high physiological arousal and awareness of changes in bodily states (Critchley, 2005). The insula computes an interceptive prediction error, which signals a mismatch between expected and actually experienced bodily arousal to a potentially aversive stimulus (Paulus and Stein, 2006). In the present study, increased anterior insular activation showed significant relationships with CM and anxiety scores, which was consistent with previous observations of increased insular activation in anxiety-prone individuals during emotion processing (Stein et al., 2007). Second, the anterior insula serves as the neural basis of empathy by performing predictive simulations of self- and other-related affects. In a previous study using TAF task, we found that the anterior insula was more active when thinking of a tragic accident happening to a loved one than when thinking of a neutral person (Lee et al., 2019). Third, when the anticipation involves uncertainty, the anterior insula’s response to aversive stimuli could be amplified in anxiety-prone subjects (Simmons et al., 2006). Taken together, we speculate that the hyper-reactivity of the insula may result in incorrect simulation and predictions about adverse events occurring, which in turn lead to maladaptive behaviors, such as avoidance, or drug use (Lin et al., 2016).
Regarding the large-scale network, the anterior insula and dACC were critical SN hubs (Seeley, 2019). Within SN, the anterior insula integrates the responses aroused by sensory, affective, and visceral systems (Menon and Uddin, 2010); moreover, dACC was closely related to response selection and conflict monitoring (Ide et al., 2013). These areas are also involved in determining the salience of stimuli and identifying the homeostatically relevant internal or external response (Menon, 2011). Notably, the SN coherence was increased on threatening stimuli (Carlson et al., 2013), and it was related to higher levels of anxiety (Seeley et al., 2007). In post-traumatic stress disorder, hyperactivity and hyperconnectivity of SN can be linked to increased threat detection (Akiki et al., 2017). Therefore, increased TAF tendency associated with CM experiences could be a result of sensitivity to threatening stimuli mediating SN. In the current study, ETISR-SF scores, particularly emotional abuse and TAFS likelihood, were significantly correlated to components of SN activities in the NegCP > NeuCP contrast, indicating high affective loads, but not in the NegNP > NeuNP contrast, indicating low affective loads. In a previous study, it was found that negative TAF activates more brain regions than positive TAF (Lee et al., 2021). Our findings therefore suggest that CM experiences increase negative affective loads, making TAF stimuli more salient.
TAF is representative of cognitive distortion related to OCD symptoms (Salkovskis, 1985), and previous studies have indicated that patients with OCD have an exaggerated TAF tendency (Berle and Starcevic, 2005; Shafran et al., 1996). However, our findings suggest some differences in the factors that contribute to a higher TAF tendency in patients with OCD versus CM victims. In case of OCD, increased activities and connectivities in the components of CSTC circuits during TAF stimuli exhibited associations with OCD symptoms during TAF stimuli (Lee et al., 2019; Lee et al., 2020). We found that OCD patients seem to attempt to avoid unpleasant affective stimuli elicited by negative TAF, in contrast to hypersensitive reactions to negative stimuli in CM victims. Both hyper-reactivity in patients with CM and avoidance in patients with OCD may have made them susceptible to TAF stimuli. Our past and current results suggest that staying within an acceptable range of emotional responses, e.g., feeling but not being overwhelmed, in order to adequately process the TAF stimuli.
This study has some limitations. First, this was a cross-sectional study, and CM experiences were compiled from participants’ memories. Thus, recall bias may have influenced our results. Second, our sample was relatively small, with only one institution. Therefore, our results cannot be generalized to the entire population. A multicenter study with a prospective design is required to confirm our preliminary results.