Mentalizing regions represent distributed, continuous, and abstract dimensions of others' beliefs.

The human capacity to reason about others' minds includes making causal inferences about intentions, beliefs, values, and goals. Previous fMRI research has suggested that a network of brain regions, including bilateral temporo-parietal junction (TPJ), superior temporal sulcus (STS), and medial prefrontal-cortex (MPFC), are reliably recruited for mental state reasoning. Here, in two fMRI experiments, we investigate the representational content of these regions. Building on existing computational and neural evidence, we hypothesized that social brain regions contain at least two functionally and spatially distinct components: one that represents information related to others' motivations and values, and another that represents information about others' beliefs and knowledge. Using multi-voxel pattern analysis, we find evidence that motivational versus epistemic features are independently represented by theory of mind (ToM) regions: RTPJ contains information about the justification of the belief, bilateral TPJ represents the modality of the source of knowledge, and VMPFC represents the valence of the resulting emotion. These representations are found only in regions implicated in social cognition and predict behavioral responses at the level of single items. We argue that cortical regions implicated in mental state inference contain complementary, but distinct, representations of epistemic and motivational features of others' beliefs, and that, mirroring the processes observed in sensory systems, social stimuli are represented in distinct and distributed formats across the human brain.

Localizing Pain Matrix and Theory of Mind networks with both verbal and non-verbal stimuli.

Functional localizer tasks allow researchers to identify brain regions in each individual's brain, using a combination of anatomical and functional constraints. In this study, we compare three social cognitive localizer tasks, designed to efficiently identify regions in the "Pain Matrix," recruited in response to a person's physical pain, and the "Theory of Mind network," recruited in response to a person's mental states (i.e. beliefs and emotions). Participants performed three tasks: first, the verbal false-belief stories task; second, a verbal task including stories describing physical pain versus emotional suffering; and third, passively viewing a non-verbal animated movie, which included segments depicting physical pain and beliefs and emotions. All three localizers were efficient in identifying replicable, stable networks in individual subjects. The consistency across tasks makes all three tasks viable localizers. Nevertheless, there were small reliable differences in the location of the regions and the pattern of activity within regions, hinting at more specific representations. The new localizers go beyond those currently available: first, they simultaneously identify two functional networks with no additional scan time, and second, the non-verbal task extends the populations in whom functional localizers can be applied. These localizers will be made publicly available.

Decoding moral judgments from neural representations of intentions.

Intentional harms are typically judged to be morally worse than accidental harms. Distinguishing between intentional harms and accidents depends on the capacity for mental state reasoning (i.e., reasoning about beliefs and intentions), which is supported by a group of brain regions including the right temporo-parietal junction (RTPJ). Prior research has found that interfering with activity in RTPJ can impair mental state reasoning for moral judgment and that high-functioning individuals with autism spectrum disorders make moral judgments based less on intent information than neurotypical participants. Three experiments, using multivoxel pattern analysis, find that (i) in neurotypical adults, the RTPJ shows reliable and distinct spatial patterns of responses across voxels for intentional vs. accidental harms, and (ii) individual differences in this neural pattern predict differences in participants' moral judgments. These effects are specific to RTPJ. By contrast, (iii) this distinction was absent in adults with autism spectrum disorders. We conclude that multivoxel pattern analysis can detect features of mental state representations (e.g., intent), and that the corresponding neural patterns are behaviorally and clinically relevant.

fMRI item analysis in a theory of mind task.

Conventional analyses of functional magnetic resonance imaging (fMRI) data compare the brain's response to stimulus categories (e.g., pictures of faces, stories about beliefs) across participants. In order to infer that effects observed with the specific items (a particular set of pictures or stories) are generalizable to the entire population (all faces, or all stories about beliefs), it is necessary to perform an "item analysis." Item analyses may also reveal relationships between secondary (non-hypothesized) features of the items and functional activity. Here, we perform an item analysis on a set of stories commonly used for localizing brain regions putatively involved in Theory of Mind (ToM): right and left temporo-parietal junction (RTPJ/LTPJ), precuneus (PC), superior temporal sulcus (STS) and medial prefrontal cortex (MPFC). We address the following questions: Do brain regions that comprise the ToM network respond reliably across items (i.e. different stories about beliefs)? Do these brain regions demonstrate reliable preferences for items within the category? Can we predict any region's response to individual items, by using other features of the stimuli? We find that the ToM network responds reliably to stories about beliefs, generalizing across items as well as subjects. In addition, several regions in the ToM network have reliable preferences for individual items. Linguistic features of the stimuli did not predict these item preferences.

Reduced neural selectivity for mental states in deaf children with delayed exposure to sign language.

Language provides a rich source of information about other people's thoughts and feelings. Consequently, delayed access to language may influence conceptual development in Theory of Mind (ToM). We use functional magnetic resonance imaging and behavioral tasks to study ToM development in child (n = 33, 4-12 years old) and adult (n = 36) fluent signers of American Sign Language (ASL), and characterize neural ToM responses during ASL and movie-viewing tasks. Participants include deaf children whose first exposure to ASL was delayed up to 7 years (n = 12). Neural responses to ToM stories (specifically, selectivity of the right temporo-parietal junction) in these children resembles responses previously observed in young children, who have similar linguistic experience, rather than those in age-matched native-signing children, who have similar biological maturation. Early linguistic experience may facilitate ToM development, via the development of a selective brain region for ToM.

There's more to "sparkle" than meets the eye: Knowledge of vision and light verbs among congenitally blind and sighted individuals.

We examined the contribution of first-person sensory experience to concepts by comparing the meanings of perception (visual/tactile) and emission (light/sound) verbs among congenitally blind (N = 25) and sighted speakers (N = 22). Participants judged semantic similarity for pairs of verbs referring to events of visual (e.g. to peek), tactile (e.g. to feel) and amodal perception (e.g. to perceive) as well as light (e.g. to shimmer) and sound (e.g. to boom) emission and manner of motion (to roll) (total word pairs, N = 2041). Relative to the sighted, blind speakers had higher agreement among themselves on touch perception and sound emission verbs. However, for visual verbs, the judgments of blind and sighted participants were indistinguishable, both in the semantic criteria used and subject-wise variability. Blind and sighted individuals alike differentiate visual perception verbs from verbs of touch and amodal perception and differentiate among acts of visual perception e.g. intense/continuous from brief acts of looking (e.g. peek vs. stare). Light emission verbs are differentiated according to intensity (blaze vs. glow) and stability (blaze vs. flash). Thus detailed knowledge of visual word meanings is acquired without first-person sensory access.

When minds matter for moral judgment: intent information is neurally encoded for harmful but not impure acts.

Recent behavioral evidence indicates a key role for intent in moral judgments of harmful acts (e.g. assault) but not impure acts (e.g. incest). We tested whether the neural responses in regions for mental state reasoning, including the right temporoparietal junction (RTPJ), are greater when people evaluate harmful vs impure violations. In addition, using multivoxel pattern analysis, we investigated whether the voxel-wise pattern in these regions distinguishes intentional from accidental actions, for either kind of violation. The RTPJ was preferentially recruited in response to harmful vs impure acts. Moreover, although its response was equally high for intentional and accidental acts, the voxel-wise pattern in the RTPJ distinguished intentional from accidental acts in the harm domain but not the purity domain. Finally, we found that the degree to which the RTPJ discriminated between intentional and accidental acts predicted the impact of intent information on moral judgments but again only in the harm domain. These findings reveal intent to be a uniquely critical factor for moral evaluations of harmful vs impure acts and shed light on the neural computations for mental state reasoning.

Thinking about seeing: perceptual sources of knowledge are encoded in the theory of mind brain regions of sighted and blind adults.

Blind people's inferences about how other people see provide a window into fundamental questions about the human capacity to think about one another's thoughts. By working with blind individuals, we can ask both what kinds of representations people form about others' minds, and how much these representations depend on the observer having had similar mental states themselves. Thinking about others' mental states depends on a specific group of brain regions, including the right temporo-parietal junction (RTPJ). We investigated the representations of others' mental states in these brain regions, using multivoxel pattern analyses (MVPA). We found that, first, in the RTPJ of sighted adults, the pattern of neural response distinguished the source of the mental state (did the protagonist see or hear something?) but not the valence (did the protagonist feel good or bad?). Second, these neural representations were preserved in congenitally blind adults. These results suggest that the temporo-parietal junction contains explicit, abstract representations of features of others' mental states, including the perceptual source. The persistence of these representations in congenitally blind adults, who have no first-person experience with sight, provides evidence that these representations emerge even in the absence of relevant first-person perceptual experiences.

Theory of mind: a neural prediction problem.

Predictive coding posits that neural systems make forward-looking predictions about incoming information. Neural signals contain information not about the currently perceived stimulus, but about the difference between the observed and the predicted stimulus. We propose to extend the predictive coding framework from high-level sensory processing to the more abstract domain of theory of mind; that is, to inferences about others' goals, thoughts, and personalities. We review evidence that, across brain regions, neural responses to depictions of human behavior, from biological motion to trait descriptions, exhibit a key signature of predictive coding: reduced activity to predictable stimuli. We discuss how future experiments could distinguish predictive coding from alternative explanations of this response profile. This framework may provide an important new window on the neural computations underlying theory of mind.