We examined the function of the left vTPJ and lATL in sentence processing and social-semantic working memory. Two key findings indicate that these regions engage in sentence processing through social-semantic working memory: First, they are more sensitive to sentences than to word lists only if the sentences convey social meaning (Experiments 1 and 2); second, they show persistent social-semantic-selective activity after the linguistic stimuli disappeared (Experiments 3 and 4). Two additional findings also indicate that these regions are more tightly associated with social-semantic processing than with linguistic processing: they are sensitive to the socialness of nonlinguistic stimuli (Experiment 5) and are intrinsically more tightly connected with the social-semantic-processing areas than with the sentence-processing areas (Experiment 6). Taken together, our results provide converging evidence for the social-semantic-working-memory hypothesis of the left vTPJ and lATL and challenge the general-semantic and/or syntactic accounts for the neural activity of these regions in sentence processing.
Our results indicate that during sentence processing, the stronger neural responses of the left vTPJ and lATL to sentences than to word lists are selectively associated with social-semantic comprehension, which is likely due to more durable working memory for coherent social meanings than for incoherent ones in these regions. It is notable that without controlling for the socialness of the stimuli, the activation of these regions in sentence processing has consistently been reported in the literature (Humphries et al., 2006; Pallier et al., 2011; Malik-Moraleda et al., 2022; Zaccarella et al., 2017). Why is the activity of the left vTPJ and lATL so frequently observed in previous studies of sentence processing? There are at least two reasons. First, language use is a social behavior so that sentences are naturally dominated by social semantic information (Olson et al., 2013). For example, it has been found that approximately 2/3 of natural conversations are of social topics (Dunbar et al., 1997). Second, the left vTPJ and lATL are sensitive to the social meaning of a very broad range of concepts (Zhang et al., 2022). For example, they are even sensitive to the social meaning of nonliving objects (Lin et al., 2019). Therefore, the comprehension of the vast majority of our daily language may require the involvement of social-semantic working memory.
Our results provide an alternative explanation for the results of previous neuroimaging studies that compare sentences with fragmented linguistic stimuli. The stronger brain activity to sentences than to nonsentential stimuli was viewed as a classic neural signature for linguistic processing. It has been used for localizing the language network (Fedorenko et al., 2010; 2011; Labache et al., 2019; Malik-Moraleda et al., 2022), examining the linguistic functions of the brain networks defined by resting-state fMRI data processing (Branco et al., 2020), and revealing the recruitment of the occipital cortex of congenitally blind individuals in linguistic processing (Bedny et al., 2011). However, our results show that, without controlling for the socialness of the stimuli, this classic effect may reflect social-semantic working memory. Therefore, the previous findings on this effect should be interpreted with caution, and future language studies should consider social-semantic processing in language comprehension.
Our results indicate that the left vTPJ and lATL may connect language comprehension with social cognition through social-semantic working memory. Most previous studies on the relationship between language and social cognition focused on the ability of reasoning about mental states, which is known as Theory of Mind (ToM; de Villiers, 2007; Ferstl et al., 2008; Hagoort, 2019; Lin et al., 2018b; Paunov et al., 2022). The key regions supporting ToM are the right TPJ and dorsal medial prefrontal cortex (Saxe & Wexler 2005; Schurz et al., 2014), which are often engaged in the comprehension of stories and nonliteral meanings (Feng et al., 2021; Ferstl et al., 2008; Mar, 2011). We assume that in comparison with ToM, social-semantic working memory is a more general and basic social-cognitive component that connects language comprehension with social cognition: it is not specific to mental states but involved in the processing of a wide range of social concepts; it forms the basis of social-semantic manipulation and integration, which in turn supports higher-order social cognition such as ToM. Consistent with our view, in the field of social neuroscience, the left vTPJ and lATL are associated with not only ToM (Lewis et al., 2011; Samson et al., 2004) but also other social functions (Olson et al., 2013; Saxe & Wexler 2005; Wang et al., 2017); in the field of language comprehension, the left vTPJ and lATL are involved in not only comprehension of stories (Mar, 2011) and nonliteral meanings (Rapp et al., 2012) but also social-semantic comprehension of sentences (Zhang et al., 2021), phrases (Lin et al., 2020; Yang & Bi, 2022), and words (Lin et al., 2015; 2018a; 2019; Wang et al., 2019).
As indicated by previous social neuroscience studies, the representation of social concepts relies on fine-grained social-semantic dimensions that have distinct neural correlates (Tamir et al., 2016; Thornton & Mitchell, 2018). In Experiment 4, we examined the social-semantic working memory of two specific trait dimensions, i.e. dominance and trustworthiness. Only dominance could be decoded from the neural activity of the left vTPJ and lATL. This finding is consistent with the previous finding that dominance is the most salient and conserved across the trait-state divide according to neural representation (Thornton & Mitchell, 2018). It also indicates that the left vTPJ and lATL may not represent all kinds of social-semantic dimensions. Many regions outside the left vTPJ and lATL have been found to represent specific social-semantic subdimensions (Hassabis et al., 2014; Van Overwalle et al., 2015; Tamir et al., 2016; Thornton & Mitchell, 2018). It remains to be investigated whether these regions support working memory on specific social-semantic subdimensions.
The left vTPJ and lATL showed very similar results in the current study, indicating that they share similar functions. Similar functional profiles of these two regions have also been revealed in previous studies of social-semantic processing (Zhang et al., 2022), language processing (Lerner et al., 2011; Pallier et al., 2011), and RSFC (Amft et al., 2014). Nevertheless, some functional differences between them have also been indicated by the literature. It has been found that the left lATL is more stably involved in word-level social-semantic processing (Zahn et al., 2007; Zhang et al., 2021), while the left vTPJ is more sensitive to discourse-level social-semantic processing (Lin et al., 2018b; Zhang et al., 2021). Therefore, the left lATL and vTPJ may play greater roles in social concept retrieval and integration, respectively. In addition, the left vTPJ also plays a role in cross-modal social-semantic integration: it is sensitive to both speeches and gestures that convey the communicative intents (Redcay et al., 2016) and is especially sensitive to co-speech gestures (Weisberg et al., 2017).
The finding that the left vTPJ is involved in social-semantic working memory can be linked to the previous finding that several functional subdivisions of the left TPJ support working-memory processes. In the field of language processing, the left supramarginal and angular gyri have been found to buffer phonological and semantic information, respectively (Martin et al. 2021; Yue et al., 2019; Yue & Martin, 2021). In the field of social cognition, Meyer and Collier (2020) found that the bilateral dorsal TPJ is involved in working memory of mental states of specific individuals such as characters from a television show. These findings, together with ours, indicate that the left TPJ as a whole may play important roles in working memory, with its different subdivisions supporting working memory of different types of information.
Finally, it should be noted that both the left TPJ and ATL contain multiple functional subdivisions that support different cognitive functions (Graves et al., 2022; Huth et al., 2016; Lin et al., 2018a; 2020; Seghier, 2013; Wang et al., 2019; Zhang et al., 2022). Hung et al. (2020) identified 4 functional subregions of the ATL using meta-analytic approaches. Among these subregions, only the lATL is sensitive to social processing; the other subregions are differently sensitive to linguistic processing, visual sensory, auditory sensory, episodic memory, and emotion (see also Wang et al., 2019). Lin et al. (2020) investigated the neural correlates of phrase-level semantic combination using phrases of high and low socialness. They found that in the left TPJ, the region sensitive to social semantics is ventral to the region sensitive to phrase-level general semantic combination, with no overlap between the two regions. Therefore, although we found that the activation of the left vTPJ and lATL in sentence processing is selectively associated with social-semantic comprehension, some other brain areas of the TPJ and ATL might be involved in general-semantic and/or syntactic processes.
To conclude, we examined whether the sentence and social-semantic effects observed in the left vTPJ and lATL both reflect social-semantic working memory. We found that the stronger responses of these regions to sentences than to word lists are selectively associated with social-semantic comprehension and that these regions are involved in social-semantic working memory during and after sentence processing, which supports the social-semantic-working-memory hypothesis. Our findings provide novel insights into the function of the left vTPJ and lATL in language comprehension and indicate that these regions may connect language with social cognition through social-semantic working memory.