Functionally distinct language and Theory of Mind networks are synchronized at rest and during language comprehension

Abstract

Communication requires the abilities to generate and interpret utterances and to infer the beliefs, desires, and goals of others (“Theory of Mind”; ToM). These two abilities have been shown to dissociate: individuals with aphasia retain the ability to think about others’ mental states; and individuals with autism are impaired in social reasoning, but their basic language processing is often intact. In line with this evidence from brain disorders, functional MRI (fMRI) studies have shown that linguistic and ToM abilities recruit distinct sets of brain regions. And yet, language is a social tool that allows us to share thoughts with one another. Thus, the language and ToM brain networks must share information despite being implemented in distinct neural circuits. Here, we investigated potential interactions between these networks during naturalistic cognition using functional correlations in fMRI. The networks were functionally defined in individual participants, in terms of preference for sentences over nonwords for language, and for belief inference over physical-event processing for ToM, with both a verbal and a nonverbal paradigm. Although, across experiments, interregion correlations within each network were higher than between-network correlations, we also observed above-baseline synchronization of blood oxygenation level-dependent signal fluctuations between the two networks during rest and story comprehension. This synchronization was functionally specific: neither network was synchronized with the executive control network (functionally defined in terms of preference for a harder over easier version of an executive task). Thus, coordination between the language and ToM networks appears to be an inherent and specific characteristic of their functional architecture.NEW & NOTEWORTHY Humans differ from nonhuman primates in their abilities to communicate linguistically and to infer others’ mental states. Although linguistic and social abilities appear to be interlinked onto- and phylogenetically, they are dissociated in the adult human brain. Yet successful communication requires language and social reasoning to work in concert. Using functional MRI, we show that language regions are synchronized with social regions during rest and language comprehension, pointing to a possible mechanism for internetwork interaction.