No evidence of theory of mind reasoning in the human language network.

Language comprehension and the ability to infer others' thoughts (theory of mind [ToM]) are interrelated during development and language use. However, neural evidence that bears on the relationship between language and ToM mechanisms is mixed. Although robust dissociations have been reported in brain disorders, brain activations for contrasts that target language and ToM bear similarities, and some have reported overlap. We take another look at the language-ToM relationship by evaluating the response of the language network, as measured with fMRI, to verbal and nonverbal ToM across 151 participants. Individual-participant analyses reveal that all core language regions respond more strongly when participants read vignettes about false beliefs compared to the control vignettes. However, we show that these differences are largely due to linguistic confounds, and no such effects appear in a nonverbal ToM task. These results argue against cognitive and neural overlap between language processing and ToM. In exploratory analyses, we find responses to social processing in the "periphery" of the language network-right-hemisphere homotopes of core language areas and areas in bilateral angular gyri-but these responses are not selectively ToM-related and may reflect general visual semantic processing.

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

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.

The occipital place area is causally and selectively involved in scene perception.

Functional magnetic resonance imaging has revealed a set of regions selectively engaged in visual scene processing: the parahippocampal place area (PPA), the retrosplenial complex (RSC), and a region around the transverse occipital sulcus (previously known as "TOS"), here renamed the "occipital place area" (OPA). Are these regions not only preferentially activated by, but also causally involved in scene perception? Although past neuropsychological data imply a causal role in scene processing for PPA and RSC, no such evidence exists for OPA. Thus, to test the causal role of OPA in human adults, we delivered transcranial magnetic stimulation (TMS) to the right OPA (rOPA) or the nearby face-selective right occipital face area (rOFA) while participants performed fine-grained perceptual discrimination tasks on scenes or faces. TMS over rOPA impaired discrimination of scenes but not faces, while TMS over rOFA impaired discrimination of faces but not scenes. In a second experiment, we delivered TMS to rOPA, or the object-selective right lateral occipital complex (rLOC), while participants performed categorization tasks involving scenes and objects. TMS over rOPA impaired categorization accuracy of scenes but not objects, while TMS over rLOC impaired categorization accuracy of objects but not scenes. These findings provide the first evidence that OPA is causally involved in scene processing, and further show that this causal role is selective for scene perception. Our findings illuminate the functional architecture of the scene perception system, and also argue against the "distributed coding" view in which each category-selective region participates in the representation of all objects.

Multiple and subject-specific roles of uncertainty in reward-guided decision-making.

Decision-making in noisy, changing, and partially observable environments entails a basic tradeoff between immediate reward and longer-term information gain, known as the exploration-exploitation dilemma. Computationally, an effective way to balance this tradeoff is by leveraging uncertainty to guide exploration. Yet, in humans, empirical findings are mixed, from suggesting uncertainty-seeking to indifference and avoidance. In a novel bandit task that better captures uncertainty-driven behavior, we find multiple roles for uncertainty in human choices. First, stable and psychologically meaningful individual differences in uncertainty preferences actually range from seeking to avoidance, which can manifest as null group-level effects. Second, uncertainty modulates the use of basic decision heuristics that imperfectly exploit immediate rewards: a repetition bias and win-stay-lose-shift heuristic. These heuristics interact with uncertainty, favoring heuristic choices under higher uncertainty. These results, highlighting the rich and varied structure of reward-based choice, are a step to understanding its functional basis and dysfunction in psychopathology.

The Language Network Reliably "Tracks" Naturalistic Meaningful Nonverbal Stimuli.

The language network, comprised of brain regions in the left frontal and temporal cortex, responds robustly and reliably during language comprehension but shows little or no response during many nonlinguistic cognitive tasks (e.g., Fedorenko & Blank, 2020). However, one domain whose relationship with language remains debated is semantics-our conceptual knowledge of the world. Given that the language network responds strongly to meaningful linguistic stimuli, could some of this response be driven by the presence of rich conceptual representations encoded in linguistic inputs? In this study, we used a naturalistic cognition paradigm to test whether the cognitive and neural resources that are responsible for language processing are also recruited for processing semantically rich nonverbal stimuli. To do so, we measured BOLD responses to a set of ∼5-minute-long video and audio clips that consisted of meaningful event sequences but did not contain any linguistic content. We then used the intersubject correlation (ISC) approach (Hasson et al., 2004) to examine the extent to which the language network "tracks" these stimuli, that is, exhibits stimulus-related variation. Across all the regions of the language network, meaningful nonverbal stimuli elicited reliable ISCs. These ISCs were higher than the ISCs elicited by semantically impoverished nonverbal stimuli (e.g., a music clip), but substantially lower than the ISCs elicited by linguistic stimuli. Our results complement earlier findings from controlled experiments (e.g., Ivanova et al., 2021) in providing further evidence that the language network shows some sensitivity to semantic content in nonverbal stimuli.

Preserved functional organization of auditory cortex in two individuals missing one temporal lobe from infancy.

Human cortical responses to natural sounds, measured with fMRI, can be approximated as the weighted sum of a small number of canonical response patterns (components), each having interpretable functional and anatomical properties. Here, we asked whether this organization is preserved in cases where only one temporal lobe is available due to early brain damage by investigating a unique family: one sibling missing their left temporal lobe from infancy, another missing the right temporal lobe from infancy, and a third anatomically neurotypical. None of the siblings manifested behavioral deficits. We analyzed fMRI responses to diverse natural sounds within the intact hemispheres of these individuals and compared them to 12 neurotypical participants. All siblings manifested typical-like auditory responses in their intact hemispheres. These results suggest that the development of the auditory cortex in each hemisphere does not depend on the existence of the other hemisphere, highlighting the redundancy and equipotentiality of the bilateral auditory system.

Scalar Implicature is Sensitive to Contextual Alternatives.

The quantifier "some" often elicits a scalar implicature during comprehension: "Some of today's letters have checks inside" is often interpreted to mean that not all of today's letters have checks inside. In previous work, Goodman and Stuhlmüller (G&S) proposed a model that predicts that this implicature should depend on the speaker's knowledgeability: If the speaker has only examined some of the available letters (e.g., two of three letters), people are less likely to infer that "some" implies "not all" than if the speaker has examined all of the available letters. G&S also provided behavioral evidence in support of their model. In this paper, we first show that a simple extension of G&S's model (1) predicts G&S's knowledgeability effects, and in addition, (2) predicts that the knowledgeability effect will be reduced when the speaker's usage indicates numeral alternatives are available. We tested the new model's predictions in four preregistered experiments. All experiments supported the first model prediction, replicating G&S's finding of a main effect of the speaker's knowledge. Further, Experiments 2 and 4 supported the second model prediction showing that the words that a speaker tends to use affect the strength of scalar implicature that comprehenders make. In particular, when the speaker has partial knowledge (e.g., has only examined two of three letters), comprehenders think that "some" is more likely to mean "not all" when the speaker also tends to produce number words in similar sentences (e.g., "2 of today's rooms have working smoke detectors."). These results have important ramifications for theories of meaning: the context beyond the sentence (e.g., the speaker's tendency to use particular words) affects the set of alternatives that comprehenders consider when inferring meaning.

Preserved functional organization of human auditory cortex in individuals missing one temporal lobe from infancy.

Human cortical responses to natural sounds, measured with fMRI, can be approximated as the weighted sum of a small number of canonical response patterns (components), each having interpretable functional and anatomical properties. Here, we asked whether this organization is preserved in cases where only one temporal lobe is available due to early brain damage by investigating a unique family: one sibling born without a left temporal lobe, another without a right temporal lobe, and a third anatomically neurotypical. We analyzed fMRI responses to diverse natural sounds within the intact hemispheres of these individuals and compared them to 12 neurotypical participants. All siblings manifested the neurotypical auditory responses in their intact hemispheres. These results suggest that the development of the auditory cortex in each hemisphere does not depend on the existence of the other hemisphere, highlighting the redundancy and equipotentiality of the bilateral auditory system.

Frontal language areas do not emerge in the absence of temporal language areas: A case study of an individual born without a left temporal lobe.

Language processing relies on a left-lateralized fronto-temporal brain network. How this network emerges ontogenetically remains debated. We asked whether frontal language areas emerge in the absence of temporal language areas through a 'deep-data' investigation of an individual (EG) born without her left temporal lobe. Using fMRI methods that have been validated to elicit reliable individual-level responses, we find that-as expected for early left-hemisphere damage-EG has a fully functional language network in her right hemisphere (comparable to the LH network in n = 145 controls) and intact linguistic abilities. However, we detect no response to language in EG's left frontal lobe (replicated across two sessions, 3 years apart). Another network-the multiple demand network-is robustly present in frontal lobes bilaterally, suggesting that EG's left frontal cortex can support non-linguistic cognition. The existence of temporal language areas therefore appears to be a prerequisite for the emergence of the frontal language areas.

Differential Tracking of Linguistic vs. Mental State Content in Naturalistic Stimuli by Language and Theory of Mind (ToM) Brain Networks.

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.