In the current study, we found that the empathy scores of abstinent alcohol subjects were significantly lower than healthy controls. Moreover, functional connectivity from the DMN to the SMN, the CON, and the Occipital network were predictive for empathy scores in healthy subjects. However, no comparable predictive models were observed in the abstinence group. Instead, the identified connectivity fingerprints underlying empathy of healthy controls could be generalized to predict the empathy ability of the abstinence group. The current findings imply that the neural networks underlying empathy may be disrupted by long-term alcohol use, and their function do not ‘normalize’ even after abstinence from drinking. Furthermore, the impaired degree may vary greatly among abstinent alcoholic individuals. The large inter-individual variation could lead to the failure of using rs-FC to identify predictive models for the abstinence group.
We found that in healthy controls baseline connectivity from the DMN to the SMN and to the Occipital network contributed to the prediction of their empathy. According to former research, the SMN is not only responsible for perceptual processing of overt movements, but this network is also implicated in accurate inference of the intentions and emotions underlying those movements.(Jacquet and Avenanti, 2015; Paracampo et al., 2017; Tamietto et al., 2015; Tidoni et al., 2013; Urgesi et al., 2014; Valchev et al., 2016; Wood et al., 2016) For example, Paracampo and his colleagues, combining transcranial magnetic stimulation (TMS) with an empathic accuracy task, found that TMS over sensorimotor regions disrupted the ability to infer amusement authenticity from observed smiles,(Paracampo et al., 2017) providing direct evidence for the involvement of the SMN in empathy processes. Regarding the Occipital network, its role (e.g., occipital face area, OFA) in emotional facial recognition has been acknowledged as well.(Duchaine and Yovel, 2015; Pitcher et al., 2011; Wang et al., 2020) The Occipital network extracts static features from faces, which could help us identify the underlying emotions in facial expressions.(Duchaine and Yovel, 2015; Wang et al., 2020) The above findings suggest that the SMN and Occipital network are not only responsible for sensory and motor functions, but also acting as key neural substrates of social cognition. The DMN, characterized by the process of self-reference and conceiving the perspectives of others, has been directly linked to empathy.(Andrews-Hanna, 2012; Buckner et al., 2008; Christoff et al., 2016) Compared to a medium-empathy healthy group, the low-empathy healthy group showed lower functional connectivity in the DMN.(S. J. Kim et al., 2017) In another study, emotional empathy scores were found to be correlated with DMN connectivity.(Bilevicius et al., 2018) Taken together, the current results indicate that functional connectivity between higher-level cognitive networks (e.g., DMN) and lower-level perceptual networks (e.g., SMN and visual) may be crucial for the process of inferring another's mental or affective state.
Empathy of healthy individuals can be reliably predicted by the functional connectivity between the DMN and CON. The CON, as described in former studies, plays an important role in the awareness of salient external stimuli and the facilitation of access to the appropriate cognitive resources.(Cai et al., 2016; Chen et al., 2013; Menon, 2011) It is possible that people with high levels of empathy ability are more sensitive to salient stimuli and they could be more able to put social information in their proper context. In line with the above assumption, CON connectivity has been associated with emotional empathy.(Bilevicius et al., 2018) A recent meta-analysis showed that CON and DMN activation are implicated in cognitive and affective empathy,(Kogler et al., 2020) substantiating the involvement of the DMN and CON in empathic processes. Furthermore, functional couplings between the DMN and the CON are crucial for attention control, working memory, decision making, and other higher-level cognitive functions.(Cai et al., 2016; Chen et al., 2013; Cocchi et al., 2013; Menon, 2011; Shen et al., 2018) Here, we found that this internetwork connectivity was predictive for empathy, supporting the crucial role of the DMN and CON in higher-level cognitive functions, including empathic ability.
Of note, our results highlight that the individual empathy scores of the abstinence group cannot be predicted by whole brain rs-FC using CPM. Instead, the predictive model for healthy controls could be generalized to the abstinence group. A possible explanation is that neural networks accounting for empathy may be disrupted even after alcohol abstinence and the damaged degree varies greatly among abstinent individuals. To test the abovementioned hypothesis, we used graph theory(Armstrong et al., 2016; Khazaee et al., 2015; Suo et al., 2015; Ye et al., 2015) analysis to investigate the disruption of neural networks in alcohol abstinence. The results show lower local and global network efficiency in abstinent alcoholics (see Supplemental Material), indicating that neural networks are disrupted in the abstinence group. In support of this assumption, abnormal functional connectivity in the DMN, CON, and SMN was observed in abstinent alcoholics when compared to healthy controls.(Müller-Oehring et al., 2015; Vergara et al., 2017; Weiland et al., 2014) Taken together, neural networks contributing to empathy may not ‘normalize’ their functions even after alcohol abstinence. Furthermore, the impaired degree may vary greatly among abstinent individuals, because the variances of empathy scores of abstinence group were higher than healthy controls (F(1,104) = 5.701, p = 0.019). The large individual variation could lead to the failure of using whole brain rs-FC to identify predictive model of empathy in the abstinence group.
There are some limitations to our study. First, the length of sobriety is unclear, which is lacking in the database. Second, our study is the cross-sectional design. Future research needs to explore the causality. Therefore, longitudinal studies are needed to assess the dynamics of empathy and related activity of the brain during the progression from alcohol addiction to abstinence.
In conclusion, individual differences in functional connectivity between large-scale neural networks contribute to variability in empathy abilities in healthy controls. However, such predictive models were not observed in the abstinence group. Further studies are needed to investigate functional connectivity-based predictive model for abstinence-related empathy. The current findings may facilitate the development of effective therapies focusing on the rehabilitation of social cognition in alcohol abstinence.