Language and social cognition, especially the ability to reason about mental states, known as theory of mind (ToM), are deeply related in development and everyday use. However, whether these cognitive faculties rely on distinct, overlapping, or the same mechanisms remains debated. Some evidence suggests that, by adulthood, language and ToM draw on largely distinct—though plausibly interacting—cortical networks. However, the broad topography of these networks is similar, and some have emphasized the importance of social content / communicative intent in the linguistic signal for eliciting responses in the language areas. Here, we combine the power of individual-subject functional localization with the naturalistic-cognition inter-subject correlation approach to illuminate the language–ToM relationship. Using functional magnetic resonance imaging (fMRI), we recorded neural activity as participants (n = 43) listened to stories and dialogues with mental state content (+linguistic, +ToM), viewed silent animations and live action films with mental state content but no language (−linguistic, +ToM), or listened to an expository text (+linguistic, −ToM). The ToM network robustly tracked stimuli rich in mental state information regardless of whether mental states were conveyed linguistically or non-linguistically, while tracking a +linguistic / −ToM stimulus only weakly. In contrast, the language network tracked linguistic stimuli more strongly than (a) non-linguistic stimuli, and than (b) the ToM network, and showed reliable tracking even for the linguistic condition devoid of mental state content. These findings suggest that in spite of their indisputably close links, language and ToM dissociate robustly in their neural substrates—and thus plausibly cognitive mechanisms—including during the processing of rich naturalistic materials.
Language and social cognition, especially the ability to reason about mental states, known as theory of mind (ToM), are deeply related in human development, everyday use, and possibly evolution. After all, language use is a communicative behavior, which is a kind of cooperative behavior, and cooperative behaviors are, in turn, a kind of social behavior (e.g., Grice, 1968, 1975; Sperber & Wilson, 1986). Construed this way, language can hardly be encapsulated from social cognition (cf. Fodor, 1983); it is subsumed within social cognition. Interpreting linguistic signals bears key parallels to the interpretation of other intentional behaviors (e.g., Grice, 1975; Sperber & Wilson, 1986). Communicative utterances, like other behaviors, are assumed to have goals, and conversation partners are assumed to pursue these goals rationally. Furthermore, everyday discourse appears to be dominated by information about other people (e.g., Dunbar et al., 1997), and the need to keep track of others’ social record has been proposed as a key driver of language evolution (e.g., Dunbar, 2004; Nowak & Highfield, 2011; Nowak & Sigmund, 2005; Sommerfeld et al., 2008). Lastly, evidence of others’ mental states conveyed through language is arguably richer and certainly more direct / less ambiguous than what can be inferred from non-linguistic intentional behavior alone: Trying to infer the beliefs guiding someone’s actions can be obviated by their telling you what those beliefs are.
In spite of this deep relationship, language processing and social cognitive processing appear to draw on distinct neural mechanisms. Language processing engages a network of left-lateralized brain regions in lateral frontal and temporal cortex. These regions support lexico-semantic processing (word meanings) and combinatorial morphosyntactic and semantic processing (e.g., Anderson et al., 2019; Bautista & Wilson, 2016; Blank et al., 2016; Fedorenko et al., 2010, 2012, 2016, 2020; Reddy & Wehbe, 2020). In contrast to their robust and consistent responses to linguistic stimuli, these regions do not respond to a wide range of non-linguistic cognitive processes, including arithmetic processing, music perception, executive function tasks, the processing of computer code (e.g., Amalric & Dehaene, 2018; Fedorenko et al., 2011; Ivanova, Srikant, et al., 2020; Liu et al., 2020; Monti et al., 2012), and—critically—perceptual and cognitive social stimuli and tasks (e.g., Jouravlev et al., 2019; Paunov, 2019; Paunov et al., 2022; Pritchett et al., 2018; see Fedorenko & Varley, 2016, for a review).
On the other hand, attribution of mental states, such as beliefs, desires, and intentions, engages a network of brain regions in bilateral temporoparietal cortex and anterior and posterior regions along the cortical midline. These responses generalize across the type of mental state, its specific content or format (linguistic vs. pictorial), and the source of evidence for it (e.g., Castelli et al., 2000; Fletcher et al., 1995; Gallagher et al., 2000; Jacoby et al., 2016; Kandylaki et al., 2015; Ruby & Decety, 2003; Saxe & Kanwisher, 2003; Saxe, Schulz, & Jiang, 2006; Vogeley et al., 2001; see Koster-Hale & Saxe, 2013, for review). By adulthood, these regions, and especially the most selective component of the ToM network, the right temporoparietal junction (RTPJ), do not respond to social stimuli, like faces, voices, or biological motion (e.g., Deen et al., 2015), to general executive demands (e.g., Saxe, Schulz, & Jiang, 2006), to physical or broadly social attributes of agents, or to attribution of bodily sensations of pain and hunger (e.g., Bruneau et al., 2012; Jacoby et al., 2016; Saxe & Powell, 2006).
Investigations of developmental and acquired disorders have provided convergent support for the dissociability of language and ToM mechanisms. Some individuals with even severe aphasia appear to retain the capacity for mental state reasoning as long as nonverbal materials are used (e.g., Apperly et al., 2006; Varley & Siegal, 2000; Varley et al., 2001; Willems et al., 2011; see Fedorenko & Varley, 2016, for review). And at least some individuals with social, ToM-related impairments (e.g., some individuals with autism spectrum disorders) show preservation of lexical and syntactic linguistic abilities (e.g., Frith & Happé, 1994; Tager-Flusberg et al., 2005; Wilkinson, 1998).
Yet, given the deep relationship between language and ToM, ToM mechanisms must be engaged during language processing at least sometimes. When does this happen? The role of social-cognitive mechanisms in language comprehension—and thus the degree of segregation between social and linguistic mechanisms—can be examined with respect to two aspects of the linguistic signal. One concerns the role of mental state inference in language comprehension generally, whether or not the message content is about mental states. This question is at the core of the field of pragmatics, which aims to understand how communicative intent—a form of ToM inference—guides linguistic interpretation (e.g., Grice, 1957/1991, 1968, 1975). And the other relates to the use of language to express information about the mental states of agents, either directly or through descriptions of physical events, which prompt mental state attribution (e.g., Fletcher et al., 1995; Gallagher et al., 2000; Jacoby et al., 2016; Saxe & Kanwisher, 2003; Saxe, Schulz, & Jiang, 2006). In Figure 1, we schematically illustrate these different kinds of social-cognitive demands—understanding the communicative intent of the person generating the linguistic output and the processing of the linguistic content—across three common contexts for language processing.
Past work in cognitive neuroscience has investigated both of these ToM demands in language processing. Some studies have manipulated the difficulty of inferring the communicative intent of a speaker by examining paradigmatic cases of nonliteral language, from irony (e.g., Spotorno et al., 2012), to indirect speech (e.g., Feng et al., 2017; van Ackeren et al., 2012) and other forms of conversational implicature (e.g., Feng et al., 2021; Jang et al., 2013; see Hagoort & Levinson, 2014, for review). These studies have reported stronger responses in the ToM network for the critical, nonliteral stimuli compared to literal controls. However, delimiting the scope of pragmatic inference is a long-standing challenge, raising the question of whether it is possible to draw a boundary between decoded (literal) and inferred meaning, that is, between semantics and pragmatics (e.g., Jackendoff, 2009). The lack of clearly defined boundaries for the construct of pragmatics poses empirical challenges. For one, pragmatic inference need not be limited to linguistic communication: It can equally be present in other forms of cooperative information transfer between individuals, such as the interpretation of communicative gestures or, more relevant in the present context, understanding non-linguistic “stories” such as nonverbal animated or live-action films. At the same time, within the narrower context of linguistic communication, it is implausible that all forms of context-based inference of meaning recruit mental state reasoning (cf. Sperber & Wilson, 2002). Phenomena that require context-based inferences include not just the paradigmatic instances of nonliteral meaning, such as irony, indirect requests, hyperbole, and other conversational implicatures (Grice, 1975)—which do plausibly require ToM (at least often, if not necessarily)—but also relatively “low-level” and ubiquitous phenomena such as pronoun resolution, or lexical and syntactic disambiguation. Indeed, functional magnetic resonance imaging (fMRI) studies that have focused on the latter kinds of phenomena do not report ToM network engagement (e.g., Bahlmann et al., 2007; Hammer et al., 2011; January et al., 2009; Klepousniotou et al., 2014; Mason et al., 2003; McMillan et al., 2012; Rodd et al., 2005; Snijders et al., 2009).
Other studies have varied the amount of mental state content in verbal vignettes or stories (e.g., Ferstl & von Cramon, 2002; Saxe & Powell, 2006; for relevant behavioral evidence, see Bischetti et al., 2019; Lecce et al., 2019) and reported stronger activity in the ToM network for linguistic materials rich in mental state content. So, both kinds of demands appear capable of recruiting mental state reasoning, but delineating the conditions under which ToM mechanisms get engaged during linguistic processing remains an area of active investigation.
In the current study, we take a step back and re-examine the separability of linguistic and ToM mechanisms. Many studies to date have deliberately aimed to isolate the language or the ToM system rather than probe their relationship (cf. Braga et al., 2020; Deen et al., 2015; Paunov et al., 2019) and have relied on traditional experimentally controlled paradigms. As a result, we know that language and social cognition can dissociate, under appropriate experimental conditions. But do they, in fact, dissociate in everyday, naturalistic cognition? Paunov et al. (2019) recently used fMRI to examine inter-regional functional correlations within and between the language and ToM networks during naturalistic cognition paradigms, like story comprehension, and found that in spite of their dissociability (stronger within- than between-network correlations), the language and ToM networks also showed a significant amount of synchronization in their neural activity. These results point to some degree of functional integration between the networks. Furthermore, several prior studies have argued for the importance of social content / communicative intent in the linguistic signal for eliciting responses in the language areas (e.g., Mellem et al., 2016; Redcay et al., 2016). In line with current emphasis in the field on the importance of going beyond carefully controlled experimental materials in the testing of hypotheses about human cognitive architecture (e.g., Blank et al., 2014; Hasson et al., 2018; Huth et al., 2016), we use rich naturalistic materials. In contrast to Paunov et al. (2019), we rely on the inter-subject correlation (ISC) approach (e.g., Hasson et al., 2004, 2008), which allows us to not only examine the degree of dissociability and interaction between the networks, but also ask what aspects of the stimulus each network responds to by varying the format and content of the materials.
MATERIALS AND METHODS
Following Blank and Fedorenko (2017, 2020), we combine two powerful methodologies that have previously been productively applied separately in the domains of language and social cognition. In particular, we use functional localization (e.g., Brett et al., 2002; Fedorenko et al., 2010; Saxe, Brett, & Kanwisher, 2006) to identify the two networks of interest in individual subjects, and inter-subject correlations (e.g., Hasson et al., 2004, 2008) to examine the degree to which these networks “track” different stimulus features during the processing of rich naturalistic materials. Here, we highlight key strengths of each approach and consider their synergistic advantages in the context of our research goals.
Naturalistic paradigms have become a crucial complement to traditional, task-based studies in cognitive neuroscience. The obvious advantage of naturalistic paradigms is their high ecological validity: By giving up a measure of experimental control, it becomes possible to study cognition “in the wild” (Blank & Fedorenko, 2017; for general discussions, see, e.g., Nastase et al., 2020; Sonkusare et al., 2019). In particular, one can examine how coherent and structured mental representations are extracted from rich and noisy perceptual inputs, which is what happens in everyday cognition. This is in contrast to artificially isolating various features of these perceptual inputs, as is typically done in constrained experimental tasks. Naturalistic paradigms have been argued to elicit more reliable responses compared to traditional, task-based paradigms (Hasson et al., 2010), perhaps because they are generally more engaging, and can enable discoveries of functional relationships among brain regions and networks that are altogether missed in more constrained settings (e.g., Gallivan et al., 2009). Another advantage of naturalistic paradigms is their hypothesis-free nature. Through the use of naturalistic materials, researchers impose minimal design constraints to investigate the domain of interest in a manner that is maximally unbiased by prior theoretical assumptions. In effect, they are letting the data speak for itself.
However, naturalistic paradigms also come with an inherent analytic challenge: How do we make sense of data acquired without the typical constraints of standard hypothesis-driven modeling approaches? Hasson et al. (2004) pioneered an approach to tackle this challenge, known as the ISC approach (see Hasson et al., 2008, for an overview), which we adopt in the current study. The key insight behind the ISC approach is that we can model any given participant’s fMRI signal time series using another participant’s or other participants’ time series: If a voxel, brain region, or brain network “tracks” features of the stimulus during which a time series is obtained, then fMRI signal fluctuations will be stimulus-locked, resulting in similar time courses across participants (i.e., high inter-subject correlations).
ISCs have been used in several studies of narrative comprehension (e.g., Blank & Fedorenko, 2017, 2020; Honey et al., 2012; Lerner et al., 2011; Regev et al., 2013; Schmälzle et al., 2015; Silbert et al., 2014; Wilson et al., 2007), and whole-brain voxel-wise analyses have revealed high ISCs across large swaths of cortex that resemble the union of the language and ToM networks. On their own, these results might be taken as prima facie evidence for non-dissociability of language and ToM, given that the two networks appear to be jointly recruited. And insofar as the mental processes recruited in narrative comprehension recapitulate those used in everyday abstract cognition—an assumption that, we take it, partially justifies the interest in narratives in cognitive science and neuroscience (e.g., Finlayson & Winston, 2011; Willems et al., 2020)—the results may be taken to suggest the non-dissociability of language and ToM more generally.
However, it is difficult to draw inferences from these studies about the relative contributions of the language and ToM networks to narrative comprehension for two reasons. First, in whole-brain analyses, ISCs are computed on a voxel-wise basis: Individual brains are normalized to a stereotaxic template, and one-to-one voxel correspondence across individuals is then assumed in computing the ISCs. This approach is problematic because (i) inter-individual variability is well established in the high-level association cortex (e.g., Fischl et al., 2008; Frost & Goebel, 2012; Tahmasebi et al., 2012), so any given voxel may belong to functionally distinct regions across participants; and (ii) there is no independent criterion based on which an anatomical location can be interpreted as belonging to the language vs. the ToM network, thus necessitating reliance on the fallacious “reverse inference” (Poldrack, 2006) to interpret the resulting topography (see Fedorenko, 2021, for discussion). And second, traditional whole-brain analyses typically include all voxels that showed significant (above baseline) ISCs, thus potentially obscuring large differences in effect sizes (cf. Blank & Fedorenko, 2017; see Chen et al., 2017, for a general discussion of the importance of considering effect sizes in interpreting fMRI findings). Combining the ISC approach with individual-participant functional localization enables us to identify and directly compare the networks of interest (including with respect to effect sizes), as well as to relate the findings straightforwardly to the prior literature on the language and ToM networks. In the current study, we therefore identified the language and ToM networks using well-established functional localizers (Fedorenko et al., 2010; Saxe & Kanwisher, 2003), and then examined the degree of inter-subject synchronization in those regions during the processing of diverse naturalistic linguistic and non-linguistic conditions varying in the presence of mental state content. If the language and ToM networks are dissociable during naturalistic cognition, we would expect the language regions to track linguistic stimuli, including those that lack mental state content, and the ToM regions to track stimuli that have mental state content, including both linguistic and non-linguistic ones.
Overall Experimental Design and Statistical Analyses
Our overall design and analytic strategy were as follows: Participant-specific regions that responded more strongly during the reading of sentences compared with lists of nonwords were defined as regions of interest comprising the language network. Similarly, regions that responded more strongly to stories about others’ beliefs vs. stories about physical reality were defined as regions of interest comprising the ToM network (see the Stimuli and Procedure section for details). Whereas the precise anatomical locations of these regions were allowed to vary across participants, their overall topography was constrained by independently derived criteria to establish functional correspondence across brain regions of different participants (e.g., Fedorenko et al., 2010; Julian et al., 2012).
Activity in these two sets of brain regions was recorded with fMRI while participants listened to or watched a series of naturalistic stimuli, as detailed below. For each region in each network, our critical dependent variable was the strength of the correlation between each participant’s time series and the average time series from the rest of the participants. The group-averaged ISC in each region was tested for significance via a permutation test of the time series data. For our critical analysis, all individual ISC values were modeled using a linear mixed-effects (LME) regression with participant, brain region, and stimulus (what we call “condition” below) as random effects.
Forty-seven native English speakers (age 19–48, M = 24.5, SD = 5.08; 30 female) from MIT and the surrounding Boston community participated for payment. Forty participants were right-handed, as determined by the Edinburgh handedness inventory (Oldfield, 1971) or by self-report (n = 1). All seven left-handed participants showed typical left lateralization in the language localizer task described below (see Willems et al., 2014, for arguments to include left handers in cognitive neuroscience research). Four participants were excluded from the analyses due to poor quality of the localizer data (2 for ToM localizer, 1 for language localizer, and 1 for both), with the exclusion criterion defined as fewer than 100 suprathreshold voxels (at the p < 0.001 uncorrected whole-brain threshold) across the respective network’s masks (see below), bringing the number of participants included in the critical analyses to 43. All participants gave informed written consent in accordance with the requirements of MIT’s Committee on the Use of Humans as Experimental Subjects (COUHES).
Stimuli and Procedure
Each participant completed a language localizer, a ToM localizer, a localizer for the domain-general MD system (used in a replication analysis, as described below), and a subset, or all, of the critical naturalistic stimuli (“conditions”) (between 1 and 7) due to scan duration constraints (18 participants completed all 7 conditions of interest, 1 participant completed 6 conditions, 10 participants completed 5 conditions, 1 participant completed 4 conditions, 1 participant completed 3 conditions, 7 participants completed 2 conditions, and 5 participants completed 1 condition). Each condition was presented to between 28 and 32 participants (see Table 1). Each stimulus, lasting ∼5–7 min (see Table 1 for precise durations), was preceded and followed by fixation (16 s and 32 s, respectively). Finally, 10 participants performed a resting state scan, used in one of the reality-check analyses, as described below. For the language localizer, 36/43 participants completed it in the same session as the critical conditions, the remaining 7 participants completed it in an earlier session. Similarly, for the ToM and MD localizers, 37/43 participants completed them in the same session as the critical conditions, the remaining 6 participants completed them in an earlier session. We will now describe the localizers and the critical experiment in more detail.
|Condition .||Duration .||N .|
|Story||5 m 16 s||31|
|Audio play||6 m 14 s||29|
|Dialogue||5 m 35 s||28|
|Animated short film||5 m 48 s||32|
|Live action movie clip||6 m 10 s||30|
|Intentional shapes animation||4 m 50 s||30|
|Expository text||7 m 6 s||28|
|−Lang −ToM (control)|
|Resting state||5 m 0 s||10|
|Condition .||Duration .||N .|
|Story||5 m 16 s||31|
|Audio play||6 m 14 s||29|
|Dialogue||5 m 35 s||28|
|Animated short film||5 m 48 s||32|
|Live action movie clip||6 m 10 s||30|
|Intentional shapes animation||4 m 50 s||30|
|Expository text||7 m 6 s||28|
|−Lang −ToM (control)|
|Resting state||5 m 0 s||10|
Language localizer task
The task used to localize the language network is described in detail in Fedorenko et al. (2010) and targets brain regions that support high-level language processing. Briefly, we used a reading task contrasting sentences and lists of unconnected, pronounceable nonwords (Figure 2) in a blocked design with a counterbalanced condition order across runs. Stimuli were presented one word / nonword at a time. Participants read the materials passively (we included a button-pressing task at the end of each trial, to help participants remain alert). As discussed in the introduction, this localizer is robust to task manipulations (e.g., Fedorenko et al., 2010; Ivanova, Siegelman, et al., 2020; Scott et al., 2017). Moreover, this localizer identifies the same regions that are localized with a broader contrast, between listening to natural speech and its acoustically degraded version (Ayyash et al., 2022; Scott et al., 2017). All participants completed two runs, each lasting 358 s and consisting of 8 blocks per condition and 5 fixation blocks. (A version of this localizer is available from https://evlab.mit.edu/funcloc/.)
ToM localizer task
The task used to localize the ToM network is described in detail in Saxe and Kanwisher (2003) and targets brain regions that support reasoning about others’ mental states. Briefly, the task was based on the classic false belief paradigm (Wimmer & Perner, 1983), and contrasted verbal vignettes about false beliefs (e.g., a protagonist has a false belief about an object’s location; the critical condition) and linguistically matched vignettes about false physical states (physical representations depicting outdated scenes, e.g., a photograph showing an object that has since been removed; the control condition) (Figure 2) in a long-event-related design with a counterbalanced order across runs (when multiple runs were administered). Stimuli were presented one at a time. Participants read these vignettes and answered a true / false comprehension question after each one. Forty-one participants completed two runs and two completed one run due to time limitations, each lasting 262 s and consisting of 5 vignettes per condition. (A version of this localizer is available from https://saxelab.mit.edu/use-our-efficient-false-belief-localizer.)
An alternative, nonverbal ToM localizer task
One of the naturalistic conditions in this study (an animated short film, Partly cloudy; Reher & Sohn, 2009; see next section) has been previously used as a nonverbal ToM localizer (Jacoby et al., 2016; see also Richardson et al., 2018). To that end, it has been coded into mental, physical, social, and pain segments, and the regions defined by the mental > pain contrast have been validated against the traditional ToM localizer described above (see Jacoby et al., 2016, for details). Examples of mental content include a character falsely believing they have been abandoned by a companion, and a character observing others interacting happily after experiencing pain (4 events, 44 s total). Following a reviewer’s suggestion, we used this localizer as an alternative ToM localizer in some of the analyses. We used the mental > physical contrast rather than mental > pain to maintain conceptual similarity with the verbal localizer’s false belief > false physical contrast. The activations obtained with the two different control conditions were qualitatively similar. Examples of physical content include a wide shot of clouds and birds flying (3 events, 22 s total). The main goal was to ensure that the language–ToM dissociation is not due to an overly narrow definition of theory of mind in terms of false beliefs, implicit in the use of this particular type of mental state attribution in the standard, verbal localizer. Notably, many previous studies have shown that the ToM network defined with the false belief localizer responds to a wide range of mental state content besides (false) beliefs, including intentions, sources of evidence about others’ minds, emotional pain, and the “minds” of group agents (e.g., Bruneau et al., 2012; Jenkins et al., 2014; Koster-Hale et al., 2014; Young & Saxe, 2008). Nevertheless, analyses that use the nonverbal ToM localizer should confirm that the results of the present study generalize beyond a particular way of localizing the ToM network.
MD localizer task (used in a replication analysis, as described below)
The task used to localize the MD network is described in detail in Fedorenko et al. (2011) and targets brain regions that support goal-directed effortful behaviors (e.g., Duncan, 2010, 2013). Briefly, we used a spatial working-memory task contrasting a harder version with an easier version (Supplemental Figure A1; Supporting Information can be found at https://doi.org/10.1162/nol_a_00071) in a blocked design with a counterbalanced condition order across runs (when multiple runs were administered). On each trial, participants saw a 3 × 4 grid and kept track of eight (hard version) or four (easy version) randomly generated locations that were sequentially flashed two at a time or one at a time, respectively. Then participants indicated their memory for these locations in a two-alternative, forced-choice paradigm via a button press, and received feedback. Of the 32 participants included in the replication analysis (i.e., non-overlapping with those used in the original study in Blank & Fedorenko, 2017), 23 participants completed two runs of the localizer, and 9 completed one run, each lasting 448 s and consisting of 6 blocks per condition and 4 fixation blocks.
The critical naturalistic task
In the main experiment, each participant listened to (over scanner-safe Sensimetrics headphones) and/or watched a set of naturalistic stimuli (varying between 4 min 50 s and 7 min 6 s in duration). Four of the conditions used linguistic materials: (i) a story (Elvis from the Natural Stories corpus; Futrell et al., 2021); (ii) an audio play (a segment from an HBO miniseries, “Bad News” (audio only) from Angels in America; Kushner & Nichols, 2003); (iii) a naturalistic dialogue—a casual unscripted conversation between two female friends (recorded by JG); and (iv) a non-narrative expository text (a text about trees adapted from “Tree”; Wikipedia, n.d.) (recorded by JG). The first three of the linguistic conditions were rich in mental state content; the fourth was meaningful naturalistic discourse with little/no mental state content (see below for additional discussion). The three remaining conditions were videos with no linguistic content: (i) an animated short film (Partly Cloudy from Pixar; Reher & Sohn, 2009); (ii) a clip from a live action film (“Falling Asleep in Church”; Mr. Bean Official, 2009); and (iii) a custom-created Heider and Simmel style animation (Heider & Simmel, 1944) consisting of simple geometric shapes moving in ways so as to suggest intentional interactions designed to tell a story (e.g., a shape gets locked up inside a space, another shape goes on a quest to get help to release it, etc.). All three non-linguistic conditions were rich in mental state content. (Five additional conditions—included for some participants in another study—are of no interest to the current study.) All the materials are available on OSF (except in cases where copyright issues prevent us from doing so): https://osf.io/prghx/. In the resting state scan, used for one of our reality-check analyses, as described below, participants were instructed to close their eyes and let their mind wander but to remain awake while resting in the scanner for 5 min (the scanner lights were dimmed and the projector was turned off).
It is important to note that although we classify these naturalistic conditions into “types” in a binary way (i.e., either involving ToM or not, and either involving language or not), this should not be taken to suggest that there cannot be gradation within each category. Indeed, given the richness of the stimuli, there almost certainly is, at least for the ToM dimension. However, we do not pursue this question further given the small number of stimuli within each category, and their complexity. Another challenge is coding the materials, especially for mental state content. In particular, linguistically mediated mental state attribution often proceeds not from explicit mentions of mental states but from action descriptions, and in nonverbal settings ToM attribution proceeds exclusively from action observation. As a result, it is difficult to specify, especially in complex naturalistic materials, when mental state attribution is prompted. Conversely, ToM vocabulary need not lead to stronger mental state attribution (e.g., “Alan thinks that this is a nice house” vs. “Alan says that this is a nice house”; presumably, a mental state is ascribed to Alan in both cases). Thus, we do not attempt to quantify degrees of mental state attribution beyond the overall presence or (near-)absence of mental state content.
Another important point to acknowledge is that there may be a certain degree of “contamination” across categories. Specifically, as discussed in the Introduction, the −ToM condition (expository text) plausibly involves some degree of pragmatic inference, and such texts have previously been shown to elicit responses in parts of the ToM network (e.g., Ferstl & von Cramon, 2002; Jacoby & Fedorenko, 2020). In the case of language, even though binary classification is relatively straightforward (linguistic input is either present or not), one might argue that the language network may nevertheless be recruited to some extent owing to the communicative nature or rich semantics of the non-linguistic stimuli. Although prior work suggests that nonverbal communication does not recruit the language network (e.g., Deen et al., 2015; Jouravlev et al., 2019; Pritchett et al., 2018), some studies have found the language network is activated during the processing of visual event semantics (e.g., Ivanova et al., 2021). Critically for present purposes, however, to the extent that there is contamination in either direction, it should work against finding a language–ToM dissociation; i.e., our results might underestimate the true degree of dissociation. The rich and graded nature of the stimuli might help account for some results inconsistent with a complete dissociation, and we return to this question in the Discussion.
Data Acquisition and Preprocessing
Whole-brain structural and functional data were collected on a whole-body 3 Tesla Siemens Trio scanner with a 32-channel head coil at the Athinoula A. Martinos Imaging Center at the McGovern Institute for Brain Research at MIT. T1-weighted structural images were collected in 176 axial slices with 1 mm isotropic voxels [repetition time (TR) = 2,530 ms; echo time (TE) = 3.48 ms]. Functional, blood oxygenation level-dependent (BOLD) data were acquired using an echo-planar imaging (EPI) sequence with a 90° flip angle and using GRAPPA (generalized auto-calibrating partially parallel acquisitions) with an acceleration factor of 2; the following parameters were used: 31 4-mm-thick near-axial slices acquired in an interleaved order (with 10% distance factor), with an in-plane resolution of 2.1 × 2.1 mm, FoV in the phase encoding (A >> P) direction 200 mm and matrix size 96 × 96 mm, TR = 2,000 ms and TE = 30 ms. The first 10 s of each run were excluded to allow for steady-state magnetization.
Data preprocessing was performed with SPM12 software (https://www.fil.ion.ucl.ac.uk/spm/; using default parameters, unless specified otherwise) and supporting custom scripts in MATLAB (2020a; https://www.mathworks.com/). Preprocessing of anatomical data included normalization into a common space (Montreal Neurological Institute (MNI) template) and segmentation into probabilistic maps of the gray matter (GM), white matter (WM), and cerebro-spinal fluid (CSF). A GM mask was generated from the GM probability map, and resampled to 2 mm isotropic voxels to mask the functional data. The WM and CSF maps were used as described in temporal preprocessing below. Preprocessing of functional data included motion correction (realignment to the mean image using second-degree b-spline interpolation), normalization (estimated for the mean image using trilinear interpolation), resampling into 2 mm isotropic voxels, smoothing with a 4 mm FWHM (full width at half maximum) Gaussian filter and high-pass filtering at 200 s.
Additional preprocessing of data from the story comprehension runs was performed using the Conn toolbox (Whitfield-Gabrieli & Nieto-Castañón, 2012; https://www.nitrc.org/projects/conn) with default parameters, unless specified otherwise. BOLD signal time courses were extracted from WM and CSF. Five temporal principal components were obtained from each, as well voxel-wise averages. These were regressed out of each voxel’s time course, along with additional noise regressors, specifically, six motion parameters estimated during off-line motion correction (three translations and three rotations) and their first temporal derivatives, and artifact time points (based on global signal outliers and motion). The residual signal was band-pass filtered (0.008–0.09 Hz) to preserve only low-frequency signal fluctuations (Cordes et al., 2001). This filtering did not influence the results reported below.
Participant-Specific Functional Localization of the Language and ToM (and MD, for a Replication Analysis) Networks
Modeling localizer data
For each localizer task, a standard mass univariate analysis was performed in SPM12 whereby a general linear model estimated the effect size of each condition in each experimental run. These effects were each modeled with a boxcar function (representing entire blocks) convolved with the canonical hemodynamic response function. The model also included first-order temporal derivatives of these effects, as well as nuisance regressors representing entire experimental runs, off-line-estimated motion parameters, and time points classified as outliers (i.e., where the scan-to-scan differences in the global BOLD signal are above 5 standard deviations, or where the scan-to-scan motion is above 0.9 mm). The obtained weights were then used to compute the functional contrast of interest: for the language localizer, sentences > nonwords, for the ToM localizer false belief > false photo, and for the MD localizer (replication analysis; see the Stimuli and Procedure section), hard > easy spatial working memory.
Language and ToM (and MD, in the replication analysis) functional regions of interest (fROIs) were defined individually for each participant based on functional contrast maps from the localizer experiments (a toolbox for this procedure is available online; https://evlab.mit.edu/funcloc/). These maps were first restricted to include only GM voxels by excluding voxels that were more likely to belong to either the WM or the CSF based on SPM’s probabilistic segmentation of the participant’s structural data.
Then, fROIs in the language network were defined using group-constrained, participant-specific localization (Fedorenko et al., 2010). For each participant, the map of the sentences > nonwords contrast was intersected with binary masks that constrained the participant-specific language network to fall within areas where activations for this contrast are relatively likely across the population. These masks are based on a group-level representation of the contrast obtained from a previous sample of 220 participants. We used five such masks in the left hemisphere, including regions in the mid-to-posterior and anterior temporal lobe, as well as in the middle frontal gyrus, the inferior frontal gyrus, and its orbital part (Figure 4). A version of these masks is available online (https://evlab.mit.edu/funcloc/). In each of the resulting 5 masks, a participant-specific language fROI was defined as the top 10% of voxels with the highest contrast values. This top n% approach ensures that fROIs can be defined in every participant and that their sizes are the same across participants, allowing for generalizable results (Nieto-Castañón & Fedorenko, 2012).
For the ToM fROIs, we used masks derived from a group-level representation for the false belief > false physical contrast in an independent group of 462 participants (Dufour et al., 2013). These masks included regions in the left and right temporoparietal junction (L/RTPJ), precuneus / posterior cingulate cortex (L/RPC), and dorsal medial prefrontal cortex (MPFC; Figure 4). A version of these masks is available online (https://saxelab.mit.edu/use-our-theory-mind-group-maps), but the masks were edited as follows: The right superior temporal sulcus (RSTS) mask was excluded, as it covers the entire STS, which is known to show complex functional organization, with reduced ToM selectivity (Deen et al., 2015). The middle- and ventral-MPFC masks were also excluded to reduce the number of statistical comparisons in per-fROI analyses, but the dorsal MPFC and PC masks were split into left- and right-hemispheres, for a total of 6 masks.
Additionally, for the replication analysis, fROIs in the MD network were defined based on the hard > easy contrast in the spatial working memory task. Here, instead of using binary masks based on group-level functional data, we used anatomical masks (Blank et al., 2014; Blank & Fedorenko, 2017; Fedorenko et al., 2013; Tzourio-Mazoyer et al., 2002). Nine masks were used in each hemisphere, including regions in the middle frontal gyrus and its orbital part, the opercular part of the inferior frontal gyrus, the precentral gyrus, the superior and inferior parts of the parietal lobe, the insula, the supplementary motor area, and the cingulate cortex (Supplemental Figure A2). (We note that functional masks derived for the MD network based on 197 participants were largely overlapping with the anatomical masks; we chose to use the anatomical masks to maintain comparability between our functional data and data from previous studies that have used these masks.)
In line with prior studies (e.g., Blank & Fedorenko, 2017; Blank et al., 2014; Paunov et al., 2019), the resulting fROIs showed small pairwise overlaps within individuals across networks, and overlapping voxels were excluded in fROI definition. In the current sample, the language-MD and ToM-MD overlaps were negligible, with a median overlap of 0 and average percentage overlap of fewer than 3% of voxels, on average across participants, relative to the total size of all fROIs in either network. Similarly, the language–ToM overlaps were small relative to all fROIs in either network (6.3% of voxels, on average across participants, relative to the total number of voxels in language fROIs and 3.2% relative to all ToM fROIs). This overlap was localized entirely to one pair of fROIs: the left posterior temporal (LPostTemp) language fROI and the left temporoparietal junction (LTPJ) ToM fROI, and was more substantial relative to the total sizes of just these two fROIs: 38.6 voxels, on average across participants, i.e., 13.1% out of 295 total LPostTemp voxels, and 11.6% out of 332 total LTPJ voxels. We therefore repeated all key analyses without excluding these voxels in defining the fROIs. The results of these alternative analyses were qualitatively and statistically similar.
Reality Check and Replication Analyses
Prior to performing our critical analyses, we conducted two reality-check analyses and—in line with increasing emphasis in the field on robust and replicable science (e.g., Poldrack et al., 2017)—an analysis aimed at replicating and extending a previous ISC-based finding from our lab (Blank & Fedorenko, 2017).
ISCs in perceptual cortices
Anatomical ROIs were additionally defined in early visual and auditory cortex in all participants. For visual cortex, regions included inferior, middle, and superior occipital cortex bilaterally (6 ROIs in total; masks available from https://www.nitrc.org/projects/wfu_pickatlas/). For auditory cortex, regions included posteromedial and anterolateral sections of Heschl’s gyrus bilaterally (4 ROIs in total; Morosan et al., 2001; these regions are based on postmortem histology and have been used in a number of previous fMRI papers). All parcels used are available on OSF (https://osf.io/prghx/). Signal extraction, ISC estimation, and inferential statistics were performed identically to the critical analyses (see the Critical Analyses section). ISCs from these regions were used in a reality check (see the Results of Reality Check and Replication Analyses section), to ensure that a double-dissociation obtains between visually and auditorily presented conditions in these perceptual regions.
Resting state ISCs
A subset of 10 participants (who completed 1–7 of the critical conditions) completed a resting state scan, which was included to ensure that data acquisition, preprocessing, and modeling procedures do not induce spurious ISCs. To this end, signal extraction, ISC estimation, and inferential statistics were performed identically to the critical analyses (see the Critical Analyses section).
Replication analysis: Closer tracking of linguistic input by language regions than by domain-general MD regions
Blank and Fedorenko (2017) reported stronger ISCs during the processing of naturalistic linguistic materials in the language regions, compared to domain-general MD regions. The MD network has been implicated in executive processes and goal-directed behavior (e.g., Duncan, 2010, 2013), including in the domain of language (e.g., see Fedorenko, 2014, for a review; cf. Diachek et al., 2020; Fedorenko & Shain, 2021). We sought to replicate Blank and Fedorenko’s key result in a new set of participants and to extend it to different types of linguistic materials. Specifically, the original study used narratives, including the narrative used in the present study along with three others. We expected the results to generalize to non-narrative linguistic conditions. Ten participants in our data set (n = 6 in the narrative condition) who also participated in the original study were excluded from this analysis. Again, signal extraction, ISC estimation, and inferential statistics were identical to the critical analyses (see the Critical Analyses section).
For each participant and fROI, BOLD signal time courses recorded during each naturalistic condition were extracted from each voxel beginning 6 s following the onset of the stimulus (to exclude an initial rise in the hemodynamic response relative to fixation, which could increase ISCs) and averaged across voxels. For each fROI, participant, and condition we computed an ISC value, namely, Pearson’s product-moment correlation coefficient between the z-scored time course and the corresponding z-scored and averaged time course across the remaining participants (Lerner et al., 2011). ISCs were Fisher-transformed before statistical testing to improve normality (Silver & Dunlap, 1987).
In each fROI, ISCs were then tested for significance against an empirical null distribution based on 1,000 simulated signal time courses that were generated by phase-randomization of the original data (Theiler et al., 1992). Namely, we generated null distributions for individual participants, fit each distribution with a Gaussian, and analytically combined the resulting parameters across participants. The true ISCs, also averaged across participants, were then z-scored relative to these empirical parameters and converted to one-tailed p values.
ISCs were compared across networks and condition types using LME regressions, implemented in MATLAB 2020a. ISCs were modeled with maximal random effects structure appropriate for each analysis (Barr et al., 2013; Baayen et al., 2008), including random intercepts for participants, with random slopes for the effects of interest, and crossed random intercepts for fROI and condition. Hypothesis testing was performed with two-tailed tests over the respective model coefficients, with Satterthwaite approximation for the degrees of freedom.
Further analyses performed within networks across condition types or against the theoretical null distribution (i.e., testing the intercept term), as well as those per fROI within a network or per condition across networks, also always included maximal random effects on the remaining grouping variables. The p values in these analyses are reported following false discovery rate (FDR) correction for multiple comparisons (Benjamini & Yekutieli, 2001).
Lastly, in comparisons against baseline, per-fROI analyses against empirical null distributions are also reported, which aim to ensure that, at the finest grain (each individual fROI and condition, across participants), differences from baseline are independent of assumptions regarding data normality. These tests were also FDR corrected for multiple comparisons for all fROIs within a network, and across all seven conditions of interest.
Results of Reality Check and Replication Analyses
Reality check #1: ISCs in perceptual cortices
We examined ISCs for the conditions of interest in early auditory and visual cortex, grouping the conditions by presentation modality. As expected, we observed stronger ISCs for the auditory conditions in the auditory cortex, and stronger ISCs for the visual conditions in the visual cortex (Figure 3). The LME regression (see the Overall Experimental Design and Statistical Analyses section) revealed a strong crossover interaction (beta = 0.648, SE = 0.046, t(89.79) = 13.970, p = 10−25).
Notably, we also observed that the visual areas weakly but reliably tracked the auditory conditions (beta = 0.066, SE = 0.012, t(38.10) = 5.398, p = 10−7), and the early auditory areas reliably tracked the visual conditions (beta = 0.175, SE = 0.020, t(24.15) = 8.573, p = 10−10). We return to the interpretation of these effects in the Discussion. For the time being, we note that care must be taken in interpreting deviations of the ISCs during “active” (cf. resting state) conditions from baseline.
Reality check #2: Resting state ISCs
To exclude the possibility that the ISCs in the critical analyses are driven by scanner noise or preprocessing/analysis procedures, we measured ISCs across a subset of 10 participants who were scanned in a 5-min resting state condition (Hasson et al., 2004). The ISCs during rest did not significantly differ from baseline in either the language or ToM networks, as assessed with an LME regression, or against the empirical null distribution. This analysis suggests that any above-baseline ISCs for our critical conditions are not an artifact of data acquisition, preprocessing, or analysis procedures.
Replication analysis: Closer tracking of linguistic input by language regions than by domain-general MD regions
We successfully replicated the key finding for the narrative condition (beta = 0.181, SE = 0.039, t(34.89) = 4.664, p = 10−5; p values are FDR-corrected for the four linguistic conditions) and extended it to the audio play (beta = 0.307, SE = 0.052, t(34.23) = 5.944, p = 10−7), the dialogue (beta = 0.157, SE = 0.039, t(33.05) = 4.014, p = 10−5), and the expository text (beta = 0.129, SE = 0.036, t(36.75) = 3.543, p = 10−4) conditions (Supplemental Figure A3). These results suggest that across diverse kinds of linguistic stimuli, the language network’s activity is more tightly coupled with the inputs, compared to the domain-general MD regions’ activity.
Results of Critical Analyses
Evidence for dissociation between the language and ToM networks in direct network comparisons
We tested three key predictions, which, if supported, provide evidence in favor of language–ToM dissociability in naturalistic settings. First, the ToM network should track conditions rich in ToM content irrespective of whether these conditions are linguistic or non-linguistic, whereas the language network should track linguistic conditions more strongly than non-linguistic ones. Indeed, we found a network (language, ToM) × condition type (linguistic: narrative, audio play, dialogue, expository text; non-linguistic: animated film, live action film clip, Heider & Simmel-style animation) interaction (beta = 0.191, SE = 0.059, t(84.06) = 3.270, p = 0.002). We also found main effects of condition type and network: The linguistic conditions were—on average across networks—tracked more strongly than the non-linguistic conditions (beta = 0.124, SE = 0.0459, t(96.47) = 2.700, p = 0.008), and the language network tracked the conditions more strongly, on average, than the ToM network (beta = 0.096, SE = 0.039, t(86.87) = 2.487, p = 0.015).
Second, for non-linguistic conditions, the ToM network should exhibit stronger tracking of conditions with mental state content than the language network. Indeed, the ToM network showed higher ISCs than the language network (beta = 0.095, SE = 0.043, t(35.59) = 2.197, p = 0.035).
And third, for the linguistic condition without mental state content (the expository text), the language network should exhibit stronger tracking than the ToM network. Indeed, the language network showed higher ISCs than the ToM network (beta = 0.111, SE = 0.044, t(19.10) = 2.507, p = 0.021).
The same qualitative pattern obtains when the nonverbal ToM localizer is used to define the ToM fROIs (Supplemental Figure C1).
A more detailed characterization of the two networks’ ISC profiles
In this section, we examine more closely the detailed pattern of ISCs in the two networks of interest. The first aim of these analyses is to establish that the observed dissociation is not driven by particular conditions or regions within the networks, but rather that different aspects of the data provide convergent support for the dissociation. The second aim is to highlight aspects of the ISC pattern that are not consistent with a complete language–ToM dissociation, and thus to evaluate the strength of counterevidence in favor of the null hypothesis, that language and ToM are not dissociable in naturalistic cognition (see Supplemental Figure B1 for ISCs per fROI for each network and condition).
First, the ToM network reliably tracked each of the six conditions with mental state content: story (beta = 0.363, SE = 0.037, t(26.55) = 9.693, p = 10−10; p values are FDR-corrected for seven conditions—we are including all conditions in the correction, not only the +ToM conditions), audio play (beta = 0.295, SE = 0.028, t(10.54) = 10.716, p = 10−7), dialogue (beta = 0.203, SE = 0.026, t(16.40) = 7.797, p = 10−7), animated short (beta = 0.472, SE = 0.053, t(9.35) = 8.830, p = 10−6), live action film (beta = 0.241, SE = 0.035, t(11.18) = 6.869, p = 10−6), and Heider & Simmel style animation (beta = 0.205, SE = 0.026, t(15.72) = 7.838, p = 10−7). Moreover, in tests against the empirical null distributions these effects were significant in every ToM fROI with the exception of the dialogue condition in the RPC, (all other ps < 0.04, FDR-corrected for the six fROIs and seven conditions).
Second, the ToM network showed no preference for linguistic vs. non-linguistic conditions with mental state content (beta = 0.018, SE = 0.043, t(49.74) = 0.675, ns), consistent with these regions’ role in representing mental states irrespective of how this information is conveyed (e.g., Jacoby et al., 2016).
And third, the ToM network tracked the linguistic conditions with mental state content (story, audio play, dialogue) more strongly than the one without mental state content (expository text) (beta = 0.199, SE = 0.037, t(30.69) = 5.344, p = 10−7), suggesting that the network represents mental state information in linguistic signals, rather than the linguistic signal itself. However, the ToM network did exhibit weaker but significantly above-baseline tracking of the expository text (beta = 0.093, SE = 0.022, t(22.22) = 4.165, p = 0.001). In per-fROI tests against the empirical null distributions, this effect was only reliable in the LTPJ (p = 0.015; all other ps > 0.05; FDR-corrected for the six fROIs). We consider possible explanations in the Discussion.
First, the language network reliably tracked each of the three linguistic conditions with mental state content: story (beta = 0.374, SE = 0.041, t(13.27) = 9.171, p = 10−7; p values are FDR-corrected for seven conditions), audio play (beta = 0.479, SE = 0.046, t(8.75) = 10.370, p = 10−6), and dialogue (beta = 0.294, SE = 0.045, t(9.72) = 6.491, p = 10−4). Moreover, these effects were significant in every language fROI, in tests against the empirical null distributions (ps < 0.01, FDR-corrected for the five fROIs and seven conditions).
Second, importantly, the language network also reliably tracked the linguistic condition with no mental state content (beta = 0.204, SE = 0.044, t(8.72) = 4.668, p = 10−4), and this effect, too, was significant in every language fROI (ps < 0.03, FDR-corrected for the five fROIs). This result suggests that mental state content is not necessary to elicit reliable ISCs in the language network.
And third, the language network showed stronger tracking of linguistic relative to non-linguistic conditions with mental state content (beta = 0.177, SE = 0.043, t(43.54) = 4.155, p = 10−5). This result suggests a special role for linguistic input in driving the network’s responses.
However, the language network exhibited some patterns that might be taken to suggest that mental state content—or social information more generally—is, to some extent, important for linguistic processing. First, the language network tracked the linguistic conditions with mental state content more strongly than the linguistic condition with no mental state content, i.e., the expository text (beta = 0.188, SE = 0.061, t(25.67) = 3.050, p = 0.005). This result may be taken to suggest that mental state content contributes to the language network’s input tracking over and above the linguistic content alone. This interpretation warrants caution, however. In particular, reflecting the general challenges of naturalistic stimuli (see Discussion), the linguistic condition with no mental state content is not matched to the linguistic conditions with mental state content on various potentially relevant features, from how engaging they are, which could influence the depth of linguistic encoding, to specifically linguistic properties (e.g., lexical and syntactic complexity), which could also affect the strength of ISCs (e.g., Shain et al., 2020; Wehbe et al., 2021). Furthermore, only a single linguistic condition with no mental state content was included in the current study, making it difficult to rule out idiosyncratic features driving the difference.
And second, the above-baseline ISCs in the language network for the non-linguistic conditions—although weaker than those for the linguistic conditions—are also notable, suggesting some degree of reliable tracking in the language network for non-linguistic meaningful information (see also Ivanova et al., 2021, for evidence of reliable responses in the language network to visual events).
Much prior work in cognitive neuroscience has suggested—based on traditional controlled experimental paradigms—that the network of brain regions that support linguistic interpretation and the brain regions that support mental state reasoning are distinct (e.g., Deen et al., 2015; Fedorenko et al., 2011; Mar, 2011; Mason & Just, 2009; Paunov, 2019; Saxe & Kanwisher, 2003). However, such paradigms differ drastically from real-world cognition, where we process rich and complex information. And linguistic and social cognition seem to be strongly intertwined in everyday life. Here, we tested whether the language and ToM networks are dissociated in their functional profiles as assessed using the ISC approach, where neural activity patterns are correlated across individuals during the processing of naturalistic materials (e.g., Hasson et al., 2004, 2008). Following Blank and Fedorenko (2017), we combined the ISC approach with the power of individual-participant functional localization (e.g., Brett et al., 2002; Fedorenko et al., 2010; Nieto-Castañón & Fedorenko, 2012; Saxe, Brett, & Kanwisher, 2006). This synergistic combination has two key advantages over the whole-brain voxel-wise ISC approach, where individual brains are first anatomically aligned and, then, each stereotaxic location serves as a basis for comparing signal time courses across participants. First, relating the resulting cortical topography of ISCs to the topography of known functional brain networks can only proceed through “reverse inference” based on anatomy (Fedorenko, 2021; Poldrack, 2006). Instead, evaluating signal time courses from functionally defined regions ensures interpretability and allows us to straightforwardly link our findings to the wealth of prior studies characterizing the response profiles of our two networks of interest. And second, this approach allows us to directly test the correlations in the language network against those in the ToM network. Such an explicit comparison between networks allows for stronger inferences compared with those licensed when each network is separately tested against a null baseline and differences across networks are indirectly inferred (e.g., see Nieuwenhuis et al., 2011, for discussion).
We examined the ISCs in the language and ToM networks during the processing of seven naturalistic conditions: three linguistic conditions with mental state content (+linguistic, +ToM), three non-linguistic conditions (silent animations and live action films) with social content but no language (–linguistic, +ToM), and a linguistic condition with no social content (+linguistic, −ToM). We found reliable differences in the ISC patterns between the language and ToM networks, in support of the hypothesis that language and ToM are dissociable even during the processing of rich and complex naturalistic materials. In particular, the ToM network tracked materials rich in mental state content irrespective of whether this content was presented linguistically or non-linguistically (see also Jacoby et al., 2016), but it showed only weak tracking of the stimulus with no mental state content. In contrast, the language network preferentially tracked linguistic materials over non-linguistic ones, and it did so regardless of whether these materials contained information about mental states.
These results expand on the existing body of knowledge about language and social cognition, with both theoretical and methodological implications. Critically, the observed dissociation extends prior findings of dissociable functional profiles between the language and the ToM networks during task-based paradigms to rich naturalistic conditions. This result suggests that the two networks represent different kinds of information. (They may also perform distinct computations on the perceptual inputs, though the idea of a canonical computation carried out across the cortex is gaining ground (e.g., Fedorenko & Shain, 2021; Keller & Mrsic-Flogel, 2018), and predictive processing seems like one likely candidate (e.g., Koster-Hale & Saxe, 2013; Shain et al., 2020). In particular, the language regions appear to track linguistic features of the input (see also Shain et al., 2020, 2021; Wehbe et al., 2021). Our results extend prior findings from ISC paradigms (Blank & Fedorenko, 2017; Honey et al., 2012; Lerner et al., 2011; Regev et al., 2013; Schmälzle et al., 2015; Silbert et al., 2014; Wilson et al., 2007), which all used materials rich in mental state content, as is typical of linguistic information, to a stimulus that is largely devoid of information about mental states—an expository text. Strong tracking of the latter stimulus aligns with prior findings from task-based paradigms of robust responses to linguistic materials with little or no mental state content (e.g., Deen et al., 2015; Jacoby & Fedorenko, 2020).
The ToM regions, in contrast, appear to track some features related to representing mental states across diverse kinds of representations (linguistic materials, animations, including highly abstract and minimalistic ones, and live action movies), again aligning with prior findings from task-based paradigms (e.g., Castelli et al., 2000; Fletcher et al., 1995; Gallagher et al., 2000; Jacoby et al., 2016; Ruby & Decety, 2003; Saxe & Kanwisher, 2003; Saxe, Schulz, & Jiang, 2006; Vogeley et al., 2001). It is important to keep in mind that the fact that the two networks are dissociable does not imply that they do not interact. Indeed, Paunov et al. (2019) reported reliably above-chance correlations in the patterns of inter-regional synchronization between the language and ToM networks, suggesting some degree of functional integration.
On the methodological level, these results vindicate the divide-and-conquer strategy in general, where cognitive domains are treated as components of a “nearly decomposable system” (Simon, 1962)—and the functional localization approach (e.g., Brett et al., 2002; Fedorenko et al., 2010; Saxe, Brett, & Kanwisher, 2006) in particular. Language and ToM appear to be distinct, supported by dissociable cortical networks for the processing of linguistic vs. mental state information, at least in adulthood (see also Braga et al., 2020). It is therefore justifiable to study each cognitive faculty and each network separately, although further probing the mechanisms of their potential interactions is equally important.
Although the overall pattern clearly supports a language–ToM dissociation between the two networks, some aspects of the results are not in line with a complete dissociation. In particular, (1) the language regions show reliable tracking of non-linguistic conditions with mental state content; (2) the language regions show stronger tracking of linguistic conditions with than without mental state content; and (3) the ToM regions show weak but reliable tracking of the linguistic condition with no mental state content. These findings may be due to methodological limitations: The above-baseline ISCs (especially the relatively weak ones) may not reflect stimulus tracking. Although we have ruled out the possibility that the above-baseline ISCs are driven by acquisition, preprocessing, or analysis artifacts in our reality-check analysis of resting state data, they could be driven by other, non-mutually-exclusive, factors. One possibility is that inter-network interactions could induce ISCs. In particular, given that the language and the ToM network show some degree of synchronization in activity during naturalistic cognition (Paunov et al., 2019), the ToM network’s tracking of a linguistic stimulus with no mental state content, for example, may be due to the fact that the language system is tracking this stimulus, and there is some “leakage” of this tracking to the ToM network through inter-network synchronization. Similarly, the language network’s preference of linguistic stimuli with mental state content over those without mental state content may be due to the leakage from the ToM network.
Another possibility is that the incomplete dissociation between language and ToM (at least with respect to (1) and (3) above) may be at least partly attributable to pragmatic processing, arguably present across all conditions: The non-linguistic ToM conditions are still story-like and hence communicative, and the linguistic non-ToM stimulus arguably still requires attribution of communicative intentions, as discussed in the introduction. The division of labor between the language and ToM networks in pragmatic inference is an exciting future direction. Demonstrating that these two networks are, in the first place, dissociable, even during rich naturalistic cognition––the goal of the present study––is an important step to pursuing this line of research. With this groundwork in place, neuroimaging evidence can be increasingly brought to bear on the question of which aspects of pragmatics require mental state reasoning, as evidenced by the engagement of the ToM network. Given the broad scope of pragmatics, encompassing diverse heterogeneous phenomena, an empirically motivated pragmatic taxonomy may be developed by investigating whether some classes of pragmatic inference are resolved within the language network proper (e.g., “lower-level” inferences about lexical or syntactic ambiguity) whereas others (e.g., establishing discourse coherence or understanding irony) require the ToM network (e.g., Bosco et al., 2018; Hagoort & Levinson, 2014; Sperber & Wilson, 2002).
Finally, the stimuli themselves may be too confounded to fully dissociate the respective contributions of language- and ToM-related components. For example, in linguistic stimuli, mental state attribution often requires particular syntactic structures—sentential complements.
More generally, the use of naturalistic materials, despite their advantages (e.g., Hasson et al., 2018; Nastase et al., 2020; Sonkusare et al., 2019), is associated with a host of challenges. The key one, mentioned above, is that certain features are necessarily confounded in naturalistic settings and can only be dissociated through careful experimentation and altering the natural statistics of the input. Relying on naturalistic materials alone can lead to wrong conclusions about the cognitive and neural architecture. This problem is especially pronounced in studying the relationship between language and social cognition given that language is primarily used in social settings and to share socially relevant information. The use of linguistic materials with no social information and of non-linguistic mental-state-rich materials has been critical, here and in earlier studies, to uncover the dissociation that holds between the language and ToM systems.
Another challenge associated with the use of naturalistic materials is that they are difficult, or altogether impossible, to match for diverse properties bound to affect neural responses. Again, this problem presents a particular challenge in comparing responses to materials rich in social information vs. materials devoid of such information given that the former are, almost by definition, going to be more engaging and exciting given the social nature of primates, including humans (e.g., Aronson, 1980; Cheney & Seyfarth, 1990; Tomasello, 2014). Possible ways to address these concerns could involve (a) characterizing the natural statistics of co-occurrences between linguistic and social processing in order to better understand how well the naturalistic stimuli reflect those statistics and perhaps altering naturalistic conditions to allow dissociating features that commonly co-occur in life; (b) developing novel neural analysis methods to isolate the components of neural signals attributable to a particular cognitive process / brain network (e.g., using analytic methods well suited to high-dimensional data such as independent components analysis (ICA) across both cortical space and large feature spaces representative of naturalistic environments (e.g., Norman-Haignere et al., 2015), or across both cortical space and time (e.g., probabilistic ICA; see Beckmann et al., 2005, for an overview); and (c) carefully annotating naturalistic materials and performing reverse correlation analyses (e.g., Hasson et al., 2004; Richardson et al., 2018) in an effort to understand the precise features that elicit increases in neural responses in different brain regions. The latter approach may be particularly informative with respect to the question of possible gradation of demands on language and ToM processing both within naturalistic stimuli and across conditions that we here grouped in the same type or general categories of +/−ToM and +/−Lang. Our results seem to suggest that considerable within-category heterogeneity exists in the degree of stimulus tracking (e.g., in the language network, the dialogue is tracked less strongly than the narrative, and in the ToM network, the Heider & Simmel-style animation is tracked less strongly than the animated film). Our data set is not ideally suited for such investigation because it includes only a single instance of each condition, and no attempt was made to match the conditions on at least some dimensions that may improve homogeneity, but this is a promising direction for future work.
A few other exciting future directions are worth highlighting, some of which may build directly on the approaches introduced and the findings reported in the current study. First, the language and ToM networks appear to be dissociable in the adult mind and brain. However, it is possible—perhaps even plausible—that this dissociation emerges over the course of development. Prior neuroimaging work has shown that the ToM network becomes gradually more specialized for mental state attribution (e.g., Gweon et al., 2012; Richardson et al., 2018; Saxe et al., 2009); and this specialization appears to be protracted with delayed language acquisition (Richardson et al., 2020). Very little is known about how specialization for linguistic processing (e.g., Fedorenko et al., 2011; Monti et al., 2012) emerges. Perhaps early on in development, a set of lateral frontal, lateral temporal, and midline cortical areas are tuned to any socially relevant information, and these areas later fractionate into those specialized for processing linguistic signals vs. those for mental state attribution vs. those that support many other kinds of social signals, both visual (e.g., eye gaze, facial expressions, gestures) and auditory (e.g., nonverbal vocalizations, prosodic information, speech acoustics). This fractionation is likely driven by computational and metabolic advantages of localized processing (e.g., Barlow, 1995; Chklovskii & Koulakov, 2004; Foldiak & Young, 1995; Olshausen & Field, 2004; see Kanwisher, 2010, for discussion). Probing linguistic and social cognition across the lifespan will be critical to understand how the two networks form and develop, leading to the segregation we observe in the adult brain.
Second, as noted above, given the likely frequent interactions between the language and ToM networks (including their most strongly dissociated components), searching for possible mechanisms of those interactions (e.g., Paunov et al., 2019) seems critical. This would require a combination of studies characterizing the patterns of anatomical connections for the language and ToM regions (e.g., Saur et al., 2010; Wiesmann et al., 2017) and studies probing online interactions using methods with high temporal resolution, like magnetoencephalography or intracranial recordings.
Third, we are still a long way away from a mechanistic-level understanding of what the language or the ToM regions do. The use of naturalistic stimuli, including in the context of the ISC approach, is promising. In particular, by examining the points in the stimulus where most participants show increases in neural activity can help generate (and subsequently test) specific hypotheses about the necessary and sufficient features of the input that are required to elicit neural responses in the relevant brain regions.
To conclude, we have demonstrated that the dissociation between the language and ToM networks that has been previously reported based on traditional task paradigms robustly generalizes to rich naturalistic conditions. However, the precise nature of each network’s representations and computations, the emergence of these networks in development, and the mechanisms for information sharing between them remain to be discovered.
Evelina Fedorenko, National Institute on Deafness and Other Communication Disorders (https://dx.doi.org/10.13039/100000055), Award ID: DC016607. Evelina Fedorenko, National Institute on Deafness and Other Communication Disorders (https://dx.doi.org/10.13039/100000055), Award ID: DC016950. Evelina Fedorenko, Simons Foundation (https://dx.doi.org/10.13039/100000893).
Alexander M. Paunov: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Software; Validation; Visualization; Writing – original draft. Idan A. Blank: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Software; Validation; Visualization. Olessia Jouravlev: Data curation; Investigation. Zachary Mineroff: Data curation; Formal analysis; Investigation; Software. Jeanne Gallée: Data curation; Resources. Evelina Fedorenko: Conceptualization; Funding acquisition; Methodology; Project administration; Resources; Supervision; Writing – review & editing.
- Theory of mind (ToM):
The social cognitive ability to reason about others’ minds in terms of unobservable mental states like belief, desire, and intention.
The context-based inference of intended (nonliteral) meaning.
- Inter-subject correlation:
A model-free method for estimating the degree of “tracking” of a (usually complex, naturalistic) stimulus across individuals.
- Functional localizer:
A task used to identify specialized regions of interest (fROIs) within individuals to establish functional correspondence of regions and networks across individuals.
Competing Interests: The authors have declared that no competing interests exist.
Handling Editor: Roel Willems