Single-neuronal predictions of others' beliefs in humans.

Human social behaviour crucially depends on our ability to reason about others. This capacity for theory of mind has a vital role in social cognition because it enables us not only to form a detailed understanding of the hidden thoughts and beliefs of other individuals but also to understand that they may differ from our own1-3. Although a number of areas in the human brain have been linked to social reasoning4,5 and its disruption across a variety of psychosocial disorders6-8, the basic cellular mechanisms that underlie human theory of mind remain undefined. Here, using recordings from single cells in the human dorsomedial prefrontal cortex, we identify neurons that reliably encode information about others' beliefs across richly varying scenarios and that distinguish self- from other-belief-related representations. By further following their encoding dynamics, we show how these cells represent the contents of the others' beliefs and accurately predict whether they are true or false. We also show how they track inferred beliefs from another's specific perspective and how their activities relate to behavioural performance. Together, these findings reveal a detailed cellular process in the human dorsomedial prefrontal cortex for representing another's beliefs and identify candidate neurons that could support theory of mind.

Infants infer potential social partners by observing the interactions of their parent with unknown others.

Infants are born into networks of individuals who are socially connected. How do infants begin learning which individuals are their own potential social partners? Using digitally edited videos, we showed 12-mo-old infants' social interactions between unknown individuals and their own parents. In studies 1 to 4, after their parent showed affiliation toward one puppet, infants expected that puppet to engage with them. In study 5, infants made the reverse inference; after a puppet engaged with them, the infants expected that puppet to respond to their parent. In each study, infants' inferences were specific to social interactions that involved their own parent as opposed to another infant's parent. Thus, infants combine observation of social interactions with knowledge of their preexisting relationship with their parent to discover which newly encountered individuals are potential social partners for themselves and their families.

Preliminary evidence for selective cortical responses to music in one-month-old infants.

Prior studies have observed selective neural responses in the adult human auditory cortex to music and speech that cannot be explained by the differing lower-level acoustic properties of these stimuli. Does infant cortex exhibit similarly selective responses to music and speech shortly after birth? To answer this question, we attempted to collect functional magnetic resonance imaging (fMRI) data from 45 sleeping infants (2.0- to 11.9-weeks-old) while they listened to monophonic instrumental lullabies and infant-directed speech produced by a mother. To match acoustic variation between music and speech sounds we (1) recorded music from instruments that had a similar spectral range as female infant-directed speech, (2) used a novel excitation-matching algorithm to match the cochleagrams of music and speech stimuli, and (3) synthesized "model-matched" stimuli that were matched in spectrotemporal modulation statistics to (yet perceptually distinct from) music or speech. Of the 36 infants we collected usable data from, 19 had significant activations to sounds overall compared to scanner noise. From these infants, we observed a set of voxels in non-primary auditory cortex (NPAC) but not in Heschl's Gyrus that responded significantly more to music than to each of the other three stimulus types (but not significantly more strongly than to the background scanner noise). In contrast, our planned analyses did not reveal voxels in NPAC that responded more to speech than to model-matched speech, although other unplanned analyses did. These preliminary findings suggest that music selectivity arises within the first month of life. A video abstract of this article can be viewed at https://youtu.be/c8IGFvzxudk. RESEARCH HIGHLIGHTS: Responses to music, speech, and control sounds matched for the spectrotemporal modulation-statistics of each sound were measured from 2- to 11-week-old sleeping infants using fMRI. Auditory cortex was significantly activated by these stimuli in 19 out of 36 sleeping infants. Selective responses to music compared to the three other stimulus classes were found in non-primary auditory cortex but not in nearby Heschl's Gyrus. Selective responses to speech were not observed in planned analyses but were observed in unplanned, exploratory analyses.

Emotion prediction as computation over a generative theory of mind.

From sparse descriptions of events, observers can make systematic and nuanced predictions of what emotions the people involved will experience. We propose a formal model of emotion prediction in the context of a public high-stakes social dilemma. This model uses inverse planning to infer a person's beliefs and preferences, including social preferences for equity and for maintaining a good reputation. The model then combines these inferred mental contents with the event to compute 'appraisals': whether the situation conformed to the expectations and fulfilled the preferences. We learn functions mapping computed appraisals to emotion labels, allowing the model to match human observers' quantitative predictions of 20 emotions, including joy, relief, guilt and envy. Model comparison indicates that inferred monetary preferences are not sufficient to explain observers' emotion predictions; inferred social preferences are factored into predictions for nearly every emotion. Human observers and the model both use minimal individualizing information to adjust predictions of how different people will respond to the same event. Thus, our framework integrates inverse planning, event appraisals and emotion concepts in a single computational model to reverse-engineer people's intuitive theory of emotions. This article is part of a discussion meeting issue 'Cognitive artificial intelligence'.

Using child-friendly movie stimuli to study the development of face, place, and object regions from age 3 to 12 years.

Scanning young children while they watch short, engaging, commercially-produced movies has emerged as a promising approach for increasing data retention and quality. Movie stimuli also evoke a richer variety of cognitive processes than traditional experiments, allowing the study of multiple aspects of brain development simultaneously. However, because these stimuli are uncontrolled, it is unclear how effectively distinct profiles of brain activity can be distinguished from the resulting data. Here we develop an approach for identifying multiple distinct subject-specific Regions of Interest (ssROIs) using fMRI data collected during movie-viewing. We focused on the test case of higher-level visual regions selective for faces, scenes, and objects. Adults (N = 13) were scanned while viewing a 5.6-min child-friendly movie, as well as a traditional localizer experiment with blocks of faces, scenes, and objects. We found that just 2.7 min of movie data could identify subject-specific face, scene, and object regions. While successful, movie-defined ssROIS still showed weaker domain selectivity than traditional ssROIs. Having validated our approach in adults, we then used the same methods on movie data collected from 3 to 12-year-old children (N = 122). Movie response timecourses in 3-year-old children's face, scene, and object regions were already significantly and specifically predicted by timecourses from the corresponding regions in adults. We also found evidence of continued developmental change, particularly in the face-selective posterior superior temporal sulcus. Taken together, our results reveal both early maturity and functional change in face, scene, and object regions, and more broadly highlight the promise of short, child-friendly movies for developmental cognitive neuroscience.

Advantages and limitations of representing groups in terms of recursive utilities.

Group representations based on recursive utilities can be used to derive the same predictions as Pietraszewski in conflict situations. Additionally, these representations generalize to non-conflict situations, asymmetric relationships, and represent the stakes in a conflict. However, both proposals fail to represent asymmetries of power and responsibility and to account for generalizations from specific observed individuals to collections of non-observed individuals.

A size-adaptive 32-channel array coil for awake infant neuroimaging at 3 Tesla MRI.

PURPOSE: Functional magnetic resonance imaging (fMRI) during infancy poses challenges due to practical, methodological, and analytical considerations. The aim of this study was to implement a hardware-related approach to increase subject compliance for fMRI involving awake infants. To accomplish this, we designed, constructed, and evaluated an adaptive 32-channel array coil. METHODS: To allow imaging with a close-fitting head array coil for infants aged 1-18 months, an adjustable head coil concept was developed. The coil setup facilitates a half-seated scanning position to improve the infant's overall scan compliance. Earmuff compartments are integrated directly into the coil housing to enable the usage of sound protection without losing a snug fit of the coil around the infant's head. The constructed array coil was evaluated from phantom data using bench-level metrics, signal-to-noise ratio (SNR) performances, and accelerated imaging capabilities for both in-plane and simultaneous multislice (SMS) reconstruction methodologies. Furthermore, preliminary fMRI data were acquired to evaluate the in vivo coil performance. RESULTS: Phantom data showed a 2.7-fold SNR increase on average when compared with a commercially available 32-channel head coil. At the center and periphery regions of the infant head phantom, the SNR gains were measured to be 1.25-fold and 3-fold, respectively. The infant coil further showed favorable encoding capabilities for undersampled k-space reconstruction methods and SMS techniques. CONCLUSIONS: An infant-friendly head coil array was developed to improve sensitivity, spatial resolution, accelerated encoding, motion insensitivity, and subject tolerance in pediatric MRI. The adaptive 32-channel array coil is well-suited for fMRI acquisitions in awake infants.

Processing communicative facial and vocal cues in the superior temporal sulcus.

Facial and vocal cues provide critical social information about other humans, including their emotional and attentional states and the content of their speech. Recent work has shown that the face-responsive region of posterior superior temporal sulcus ("fSTS") also responds strongly to vocal sounds. Here, we investigate the functional role of this region and the broader STS by measuring responses to a range of face movements, vocal sounds, and hand movements using fMRI. We find that the fSTS responds broadly to different types of audio and visual face action, including both richly social communicative actions, as well as minimally social noncommunicative actions, ruling out hypotheses of specialization for processing speech signals, or communicative signals more generally. Strikingly, however, responses to hand movements were very low, whether communicative or not, indicating a specific role in the analysis of face actions (facial and vocal), not a general role in the perception of any human action. Furthermore, spatial patterns of response in this region were able to decode communicative from noncommunicative face actions, both within and across modality (facial/vocal cues), indicating sensitivity to an abstract social dimension. These functional properties of the fSTS contrast with a region of middle STS that has a selective, largely unimodal auditory response to speech sounds over both communicative and noncommunicative vocal nonspeech sounds, and nonvocal sounds. Region of interest analyses were corroborated by a data-driven independent component analysis, identifying face-voice and auditory speech responses as dominant sources of voxelwise variance across the STS. These results suggest that the STS contains separate processing streams for the audiovisual analysis of face actions and auditory speech processing.

Development of predictive responses in theory of mind brain regions.

When we watch movies, we consider the characters' mental states in order to understand and predict the narrative. Recent work in functional magnetic resonance imaging (fMRI) uses movie-viewing paradigms to measure functional responses in brain regions recruited for such mental state reasoning (the theory of mind ["ToM"] network). Here, two groups of young children (n = 30 3-4 years old, n = 26 6-7 years old) viewed a short animated movie twice while undergoing fMRI. As children get older, ToM brain regions were recruited earlier in time during the second presentation of the movie. This "narrative anticipation" effect is specific: there was no such effect in a control network of brain regions that responds just as robustly to the movie (the "Pain Matrix"). These results complement prior studies in adults that suggest that ToM brain regions play a role not just in inferring, but in actively predicting, other people's thoughts and feelings, and provide novel evidence that as children get older, their ToM brain regions increasingly make such predictions.

Rationalization: Why, when, and what for?

In this commentary, we ask when rationalization is most likely to occur and to not occur, and about where to expect, and how to measure, its benefits.

Representational similarity precedes category selectivity in the developing ventral visual pathway.

Many studies have investigated the development of face-, scene-, and body-selective regions in the ventral visual pathway. This work has primarily focused on comparing the size and univariate selectivity of these neural regions in children versus adults. In contrast, very few studies have investigated the developmental trajectory of more distributed activation patterns within and across neural regions. Here, we scanned both children (ages 5-7) and adults to test the hypothesis that distributed representational patterns arise before category selectivity (for faces, bodies, or scenes) in the ventral pathway. Consistent with this hypothesis, we found mature representational patterns in several ventral pathway regions (e.g., FFA, PPA, etc.), even in children who showed no hint of univariate selectivity. These results suggest that representational patterns emerge first in each region, perhaps forming a scaffold upon which univariate category selectivity can subsequently develop. More generally, our findings demonstrate an important dissociation between category selectivity and distributed response patterns, and raise questions about the relative roles of each in development and adult cognition.

Parts-based representations of perceived face movements in the superior temporal sulcus.

Facial motion is a primary source of social information about other humans. Prior fMRI studies have identified regions of the superior temporal sulcus (STS) that respond specifically to perceived face movements (termed fSTS), but little is known about the nature of motion representations in these regions. Here we use fMRI and multivoxel pattern analysis to characterize the representational content of the fSTS. Participants viewed a set of specific eye and mouth movements, as well as combined eye and mouth movements. Our results demonstrate that fSTS response patterns contain information about face movements, including subtle distinctions between types of eye and mouth movements. These representations generalize across the actor performing the movement, and across small differences in visual position. Critically, patterns of response to combined movements could be well predicted by linear combinations of responses to individual eye and mouth movements, pointing to a parts-based representation of complex face movements. These results indicate that the fSTS plays an intermediate role in the process of inferring social content from visually perceived face movements, containing a representation that is sufficiently abstract to generalize across low-level visual details, but still tied to the kinematics of face part movements.

Multivariate pattern dependence.

When we perform a cognitive task, multiple brain regions are engaged. Understanding how these regions interact is a fundamental step to uncover the neural bases of behavior. Most research on the interactions between brain regions has focused on the univariate responses in the regions. However, fine grained patterns of response encode important information, as shown by multivariate pattern analysis. In the present article, we introduce and apply multivariate pattern dependence (MVPD): a technique to study the statistical dependence between brain regions in humans in terms of the multivariate relations between their patterns of responses. MVPD characterizes the responses in each brain region as trajectories in region-specific multidimensional spaces, and models the multivariate relationship between these trajectories. We applied MVPD to the posterior superior temporal sulcus (pSTS) and to the fusiform face area (FFA), using a searchlight approach to reveal interactions between these seed regions and the rest of the brain. Across two different experiments, MVPD identified significant statistical dependence not detected by standard functional connectivity. Additionally, MVPD outperformed univariate connectivity in its ability to explain independent variance in the responses of individual voxels. In the end, MVPD uncovered different connectivity profiles associated with different representational subspaces of FFA: the first principal component of FFA shows differential connectivity with occipital and parietal regions implicated in the processing of low-level properties of faces, while the second and third components show differential connectivity with anterior temporal regions implicated in the processing of invariant representations of face identity.

Using individual functional channels of interest to study cortical development with fNIRS.

Functional near-infrared spectroscopy (fNIRS) is a noninvasive neuroimaging technique that could be uniquely effective for investigating cortical function in human infants. However, prior efforts have been hampered by the difficulty of aligning arrays of fNIRS optodes placed on the scalp to anatomical or functional regions of underlying cortex. This challenge can be addressed by identifying channels of interest in individual participants, and then testing the reliability of those channels' response profiles in independent data. Using this approach, cortical regions with preferential responses to faces versus scenes, and to scenes versus faces, were observed reliably in both adults and infants. By contrast, standard analysis techniques did not reliably identify significant responses to both categories in either age group. These results reveal scene-responsive regions, and confirm face-responsive regions, in preverbal infants. More generally, the analysis approach will be a robust and sensitive tool for future characterization of the early functional development of the human brain.

Amygdala lesions do not compromise the cortical network for false-belief reasoning.

The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM--false-belief reasoning--suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition.

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.

Structural Connectivity Fingerprints Predict Cortical Selectivity for Multiple Visual Categories across Cortex.

A fundamental and largely unanswered question in neuroscience is whether extrinsic connectivity and function are closely related at a fine spatial grain across the human brain. Using a novel approach, we found that the anatomical connectivity of individual gray-matter voxels (determined via diffusion-weighted imaging) alone can predict functional magnetic resonance imaging (fMRI) responses to 4 visual categories (faces, objects, scenes, and bodies) in individual subjects, thus accounting for both functional differentiation across the cortex and individual variation therein. Furthermore, this approach identified the particular anatomical links between voxels that most strongly predict, and therefore plausibly define, the neural networks underlying specific functions. These results provide the strongest evidence to date for a precise and fine-grained relationship between connectivity and function in the human brain, raise the possibility that early-developing connectivity patterns may determine later functional organization, and offer a method for predicting fine-grained functional organization in populations who cannot be functionally scanned.

Differences in the right inferior longitudinal fasciculus but no general disruption of white matter tracts in children with autism spectrum disorder.

One of the most widely cited features of the neural phenotype of autism is reduced "integrity" of long-range white matter tracts, a claim based primarily on diffusion imaging studies. However, many prior studies have small sample sizes and/or fail to address differences in data quality between those with autism spectrum disorder (ASD) and typical participants, and there is little consensus on which tracts are affected. To overcome these problems, we scanned a large sample of children with autism (n = 52) and typically developing children (n = 73). Data quality was variable, and worse in the ASD group, with some scans unusable because of head motion artifacts. When we follow standard data analysis practices (i.e., without matching head motion between groups), we replicate the finding of lower fractional anisotropy (FA) in multiple white matter tracts. However, when we carefully match data quality between groups, all these effects disappear except in one tract, the right inferior longitudinal fasciculus (ILF). Additional analyses showed the expected developmental increases in the FA of fiber tracts within ASD and typical groups individually, demonstrating that we had sufficient statistical power to detect known group differences. Our data challenge the widely claimed general disruption of white matter tracts in autism, instead implicating only one tract, the right ILF, in the ASD phenotype.

"Visual" Cortex Responds to Spoken Language in Blind Children.

Plasticity in the visual cortex of blind individuals provides a rare window into the mechanisms of cortical specialization. In the absence of visual input, occipital ("visual") brain regions respond to sound and spoken language. Here, we examined the time course and developmental mechanism of this plasticity in blind children. Nineteen blind and 40 sighted children and adolescents (4-17 years old) listened to stories and two auditory control conditions (unfamiliar foreign speech, and music). We find that "visual" cortices of young blind (but not sighted) children respond to sound. Responses to nonlanguage sounds increased between the ages of 4 and 17. By contrast, occipital responses to spoken language were maximal by age 4 and were not related to Braille learning. These findings suggest that occipital plasticity for spoken language is independent of plasticity for Braille and for sound. We conclude that in the absence of visual input, spoken language colonizes the visual system during brain development. Our findings suggest that early in life, human cortex has a remarkably broad computational capacity. The same cortical tissue can take on visual perception and language functions. SIGNIFICANCE STATEMENT: Studies of plasticity provide key insights into how experience shapes the human brain. The "visual" cortex of adults who are blind from birth responds to touch, sound, and spoken language. To date, all existing studies have been conducted with adults, so little is known about the developmental trajectory of plasticity. We used fMRI to study the emergence of "visual" cortex responses to sound and spoken language in blind children and adolescents. We find that "visual" cortex responses to sound increase between 4 and 17 years of age. By contrast, responses to spoken language are present by 4 years of age and are not related to Braille-learning. These findings suggest that, early in development, human cortex can take on a strikingly wide range of functions.