Alternative Brain Connectivity Underscores Age-Related Differences in the Processing of Interactive Biological Motion.

Rapidly recognizing and understanding others' social interactions is an important ability that relies on deciphering multiple sources of information, for example, perceiving body information and inferring others' intentions. Despite recent advances in characterizing the brain basis of this ability in adults, its developmental underpinnings are virtually unknown. Here, we used fMRI to investigate which sources of social information support superior temporal sulcus responses to interactive biological motion (i.e., 2 interacting point-light human figures) at different developmental intervals in human participants (of either sex): Children show supportive functional connectivity with key nodes of the mentalizing network, while adults show stronger reliance on regions associated with body- and dynamic social interaction/biological motion processing. We suggest that adults use efficient action-intention understanding via body and biological motion information, while children show a stronger reliance on hidden mental state inferences as a potential means of learning to better understand others' interactive behavior.SIGNIFICANCE STATEMENT Recognizing others' interactive behavior is a critical human skill that depends on different sources of social information (e.g., observable body-action information, inferring others' hidden mental states, etc.). Understanding the brain-basis of this ability and characterizing how it emerges across development are important goals in social neuroscience. Here, we used fMRI to investigate which sources of social information support interactive biological motion processing in children (6-12 years) and adults. These results reveal a striking developmental difference in terms of how wider-brain connectivity shapes functional responses to interactive biological motion that suggests a reliance on distinct neuro-cognitive strategies in service of interaction understanding (i.e., children and adults show a greater reliance on explicit and implicit intentional inference, respectively).

Rational inattention: A new theory of neurodivergent information seeking.

This paper presents rational inattention as a new, transdiagnostic theory of information seeking in neurodevelopmental conditions that have uneven cognitive and socio-emotional profiles, including developmental language disorder (DLD), dyslexia, dyscalculia and autism. Rational inattention holds that the optimal solution to minimizing epistemic uncertainty is to avoid imprecise information sources. The key theoretical contribution of this report is to endogenize imprecision, making it a function of the primary neurocognitive difficulties that have been invoked to explain neurodivergent phenotypes, including deficits in auditory perception, working memory, procedural learning and the social brain network. We argue that disengagement with information sources with low endogenous precision (e.g. speech in DLD, orthography-phonology mappings in dyslexia, numeric stimuli in dyscalculia and social signals in autism) constitutes resource-rational behaviour. We demonstrate the strength of this account in a series of computational simulations. In experiment 1, we simulate information seeking in artificial agents mimicking an array of neurodivergent phenotypes, which optimally explore a complex learning environment containing speech, text, numeric stimuli and social cues. In experiment 2, we simulate optimal information seeking in a cross-modal dual-task paradigm and qualitatively replicate empirical data from children with and without DLD. Across experiments, simulated agents' only aim was to maximally reduce epistemic uncertainty, with no difference in reward across information sources. We show that rational inattention emerges naturally in specific neurodivergent phenotypes as a function of low endogenous precision. For instance, an agent mimicking the DLD phenotype disengages with speech (and preferentially engages with alternative precise information sources) because endogenous imprecision renders speech not conducive to information gain. Because engagement is necessary for learning, simulation demonstrates how optimal information seeking may paradoxically contribute negatively to an already delayed learning trajectory in neurodivergent children. RESEARCH HIGHLIGHTS: We present the first comprehensive theory of information seeking in neurodivergent children to date, centred on the notion of rational inattention. We demonstrate the strength of this account in a series of computational simulations involving artificial agents mimicking specific neurodivergent phenotypes that optimally explore a complex learning environment containing speech, text, numeric stimuli, and social cues. We show how optimal information seeking may, paradoxically, contribute negatively to an already delayed learning trajectory in neurodivergent children. This report advances our understanding of the factors shaping short-term decision making and long-term learning in neurodivergent children.

The role of motion in the neural representation of social interactions in the posterior temporal cortex.

Humans are an inherently social species, with multiple focal brain regions sensitive to various visual social cues such as faces, bodies, and biological motion. More recently, research has begun to investigate how the brain responds to more complex, naturalistic social scenes, identifying a region in the posterior superior temporal sulcus (SI-pSTS; i.e., social interaction pSTS), amongst others, as an important region for processing social interaction. This research, however, has presented images or videos, and thus the contribution of motion to social interaction perception in these brain regions is not yet understood. In the current study, 22 participants viewed videos, image sequences, scrambled image sequences and static images of either social interactions or non-social independent actions. Combining univariate and multivariate analyses, we confirm that bilateral SI-pSTS plays a central role in dynamic social interaction perception but is much less involved when 'interactiveness' is conveyed solely with static cues. Regions in the social brain, including SI-pSTS and extrastriate body area (EBA), showed sensitivity to both motion and interactive content. While SI-pSTS is somewhat more tuned to video interactions than is EBA, both bilateral SI-pSTS and EBA showed a greater response to social interactions compared to non-interactions and both regions responded more strongly to videos than static images. Indeed, both regions showed higher responses to interactions than independent actions in videos and intact sequences, but not in other conditions. Exploratory multivariate regression analyses suggest that selectivity for simple visual motion does not in itself drive interactive sensitivity in either SI-pSTS or EBA. Rather, selectivity for interactions expressed in point-light animations, and selectivity for static images of bodies, make positive and independent contributions to this effect across the LOTC region. Our results strongly suggest that EBA and SI-pSTS work together during dynamic interaction perception, at least when interactive information is conveyed primarily via body information. As such, our results are also in line with proposals of a third visual stream supporting dynamic social scene perception.

Establishing a role of the semantic control network in social cognitive processing: A meta-analysis of functional neuroimaging studies.

The contribution and neural basis of cognitive control is under-specified in many prominent models of socio-cognitive processing. Important outstanding questions include whether there are multiple, distinguishable systems underpinning control and whether control is ubiquitously or selectively engaged across different social behaviours and task demands. Recently, it has been proposed that the regulation of social behaviours could rely on brain regions specialised in the controlled retrieval of semantic information, namely the anterior inferior frontal gyrus (IFG) and posterior middle temporal gyrus. Accordingly, we investigated for the first time whether the neural activation commonly found in social functional neuroimaging studies extends to these 'semantic control' regions. We conducted five coordinate-based meta-analyses to combine results of 499 fMRI/PET experiments and identified the brain regions consistently involved in semantic control, as well as four social abilities: theory of mind, trait inference, empathy and moral reasoning. This allowed an unprecedented parallel review of the neural networks associated with each of these cognitive domains. The results confirmed that the anterior left IFG region involved in semantic control is reliably engaged in all four social domains. This supports the hypothesis that social cognition is partly regulated by the neurocognitive system underpinning semantic control.

Exploring the relationship between anthropomorphism and theory-of-mind in brain and behaviour.

The process of understanding the minds of other people, such as their emotions and intentions, is mimicked when individuals try to understand an artificial mind. The assumption is that anthropomorphism, attributing human-like characteristics to non-human agents and objects, is an analogue to theory-of-mind, the ability to infer mental states of other people. Here, we test to what extent these two constructs formally overlap. Specifically, using a multi-method approach, we test if and how anthropomorphism is related to theory-of-mind using brain (Experiment 1) and behavioural (Experiment 2) measures. In a first exploratory experiment, we examine the relationship between dispositional anthropomorphism and activity within the theory-of-mind brain network (n = 108). Results from a Bayesian regression analysis showed no consistent relationship between dispositional anthropomorphism and activity in regions of the theory-of-mind network. In a follow-up, pre-registered experiment, we explored the relationship between theory-of-mind and situational and dispositional anthropomorphism in more depth. Participants (n = 311) watched a short movie while simultaneously completing situational anthropomorphism and theory-of-mind ratings, as well as measures of dispositional anthropomorphism and general theory-of-mind. Only situational anthropomorphism predicted the ability to understand and predict the behaviour of the film's characters. No relationship between situational or dispositional anthropomorphism and general theory-of-mind was observed. Together, these results suggest that while the constructs of anthropomorphism and theory-of-mind might overlap in certain situations, they remain separate and possibly unrelated at the personality level. These findings point to a possible dissociation between brain and behavioural measures when considering the relationship between theory-of-mind and anthropomorphism.

Perceiving social interactions in the posterior superior temporal sulcus.

Primates are highly attuned not just to social characteristics of individual agents, but also to social interactions between multiple agents. Here we report a neural correlate of the representation of social interactions in the human brain. Specifically, we observe a strong univariate response in the posterior superior temporal sulcus (pSTS) to stimuli depicting social interactions between two agents, compared with (i) pairs of agents not interacting with each other, (ii) physical interactions between inanimate objects, and (iii) individual animate agents pursuing goals and interacting with inanimate objects. We further show that this region contains information about the nature of the social interaction-specifically, whether one agent is helping or hindering the other. This sensitivity to social interactions is strongest in a specific subregion of the pSTS but extends to a lesser extent into nearby regions previously implicated in theory of mind and dynamic face perception. This sensitivity to the presence and nature of social interactions is not easily explainable in terms of low-level visual features, attention, or the animacy, actions, or goals of individual agents. This region may underlie our ability to understand the structure of our social world and navigate within it.

Dyadic interaction processing in the posterior temporal cortex.

Recent behavioural evidence shows that visual displays of two individuals interacting are not simply encoded as separate individuals, but as an interactive unit that is 'more than the sum of its parts'. Recent functional magnetic resonance imaging (fMRI) evidence shows the importance of the posterior superior temporal sulcus (pSTS) in processing human social interactions, and suggests that it may represent human-object interactions as qualitatively 'greater' than the average of their constituent parts. The current study aimed to investigate whether the pSTS or other posterior temporal lobe region(s): 1) Demonstrated evidence of a dyadic information effect - that is, qualitatively different responses to an interacting dyad than to averaged responses of the same two interactors, presented in isolation, and; 2) Significantly differentiated between different types of social interactions. Multivoxel pattern analysis was performed in which a classifier was trained to differentiate between qualitatively different types of dyadic interactions. Above-chance classification of interactions was observed in 'interaction selective' pSTS-I and extrastriate body area (EBA), but not in other regions of interest (i.e. face-selective STS and mentalizing-selective temporo-parietal junction). A dyadic information effect was not observed in the pSTS-I, but instead was shown in the EBA; that is, classification of dyadic interactions did not fully generalise to averaged responses to the isolated interactors, indicating that dyadic representations in the EBA contain unique information that cannot be recovered from the interactors presented in isolation. These findings complement previous observations for congruent grouping of human bodies and objects in the broader lateral occipital temporal cortex area.

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.

High-level language processing regions are not engaged in action observation or imitation.

A set of left frontal, temporal, and parietal brain regions respond robustly during language comprehension and production (e.g., Fedorenko E, Hsieh PJ, Nieto-Castañón A, Whitfield-Gabrieli S, Kanwisher N. J Neurophysiol 104: 1177-1194, 2010; Menenti L, Gierhan SM, Segaert K, Hagoort P. Psychol Sci 22: 1173-1182, 2011). These regions have been further shown to be selective for language relative to other cognitive processes, including arithmetic, aspects of executive function, and music perception (e.g., Fedorenko E, Behr MK, Kanwisher N. Proc Natl Acad Sci USA 108: 16428-16433, 2011; Monti MM, Osherson DN. Brain Res 1428: 33-42, 2012). However, one claim about overlap between language and nonlinguistic cognition remains prominent. In particular, some have argued that language processing shares computational demands with action observation and/or execution (e.g., Rizzolatti G, Arbib MA. Trends Neurosci 21: 188-194, 1998; Koechlin E, Jubault T. Neuron 50: 963-974, 2006; Tettamanti M, Weniger D. Cortex 42: 491-494, 2006). However, the evidence for these claims is indirect, based on observing activation for language and action tasks within the same broad anatomical areas (e.g., on the lateral surface of the left frontal lobe). To test whether language indeed shares machinery with action observation/execution, we examined the responses of language brain regions, defined functionally in each individual participant (Fedorenko E, Hsieh PJ, Nieto-Castañón A, Whitfield-Gabrieli S, Kanwisher N. J Neurophysiol 104: 1177-1194, 2010) to action observation ( experiments 1, 2, and 3a) and action imitation ( experiment 3b). With the exception of the language region in the angular gyrus, all language regions, including those in the inferior frontal gyrus (within "Broca's area"), showed little or no response during action observation/imitation. These results add to the growing body of literature suggesting that high-level language regions are highly selective for language processing (see Fedorenko E, Varley R. Ann NY Acad Sci 1369: 132-153, 2016 for a review). NEW & NOTEWORTHY Many have argued for overlap in the machinery used to interpret language and others' actions, either because action observation was a precursor to linguistic communication or because both require interpreting hierarchically-structured stimuli. However, existing evidence is indirect, relying on group analyses or reverse inference. We examined responses to action observation in language regions defined functionally in individual participants and found no response. Thus language comprehension and action observation recruit distinct circuits in the modern 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.

Functional Organization of Social Perception and Cognition in the Superior Temporal Sulcus.

The superior temporal sulcus (STS) is considered a hub for social perception and cognition, including the perception of faces and human motion, as well as understanding others' actions, mental states, and language. However, the functional organization of the STS remains debated: Is this broad region composed of multiple functionally distinct modules, each specialized for a different process, or are STS subregions multifunctional, contributing to multiple processes? Is the STS spatially organized, and if so, what are the dominant features of this organization? We address these questions by measuring STS responses to a range of social and linguistic stimuli in the same set of human participants, using fMRI. We find a number of STS subregions that respond selectively to certain types of social input, organized along a posterior-to-anterior axis. We also identify regions of overlapping response to multiple contrasts, including regions responsive to both language and theory of mind, faces and voices, and faces and biological motion. Thus, the human STS contains both relatively domain-specific areas, and regions that respond to multiple types of social information.

Fear-specific amygdala function in children and adolescents on the fragile x spectrum: a dosage response of the FMR1 gene.

Mutations of the fragile X mental retardation 1 (FMR1) gene are the genetic cause of fragile X syndrome (FXS). The presence of significant socioemotional problems has been well documented in FXS although the brain basis of those deficits remains unspecified. Here, we investigated amygdala dysfunction and its relation to socioemotional deficits and FMR1 gene expression in children and adolescents on the FX spectrum (i.e., individuals whose trinucleotide CGG repeat expansion from 55 to over 200 places them somewhere within the fragile X diagnostic range from premutation to full mutation). Participants performed an fMRI task in which they viewed fearful, happy, and scrambled faces. Neuroimaging results demonstrated that FX participants revealed significantly attenuated amygdala activation in Fearful > Scrambled and Fearful > Happy contrasts compared with their neurotypical counterparts, while showing no differences in amygdala volume. Furthermore, we found significant relationships between FMR1 gene expression, anxiety/social dysfunction scores, and reduced amygdala activation in the FX group. In conclusion, we report novel evidence regarding a dosage response of the FMR1 gene on fear-specific functions of the amygdala, which is associated with socioemotional deficits in FXS.

Spurious group differences due to head motion in a diffusion MRI study.

Diffusion-weighted MRI (DW-MRI) has become a popular imaging modality for probing the microstructural properties of white matter and comparing them between populations in vivo. However, the contrast in DW-MRI arises from the microscopic random motion of water molecules in brain tissues, which makes it particularly sensitive to macroscopic head motion. Although this has been known since the introduction of DW-MRI, most studies that use this modality for group comparisons do not report measures of head motion for each group and rely on registration-based correction methods that cannot eliminate the full effects of head motion on the DW-MRI contrast. In this work we use data from children with autism and typically developing children to investigate the effects of head motion on differences in anisotropy and diffusivity measures between groups. We show that group differences in head motion can induce group differences in DW-MRI measures, and that this is the case even when comparing groups that include control subjects only, where no anisotropy or diffusivity differences are expected. We also show that such effects can be more prominent in some white-matter pathways than others, and that they can be ameliorated by including motion as a nuisance regressor in the analyses. Our results demonstrate the importance of taking head motion into account in any population study where one group might exhibit more head motion than the other.

Domain-specific development of face memory but not face perception.

How does the remarkable human ability for face recognition arise over development? Competing theories have proposed either late maturity (beyond 10 years) or early maturity (before 5 years), but have not distinguished between perceptual and memory aspects of face recognition. Here, we demonstrate a perception-memory dissociation. We compare rate of development for (adult, human) faces versus other social stimuli (bodies), other discrete objects (cars), and other categories processed in discrete brain regions (scenes, bodies), from 5 years to adulthood. For perceptual discrimination, performance improved with age at the same rate for faces and all other categories, indicating no domain-specific development. In contrast, face memory increased more strongly than non-face memory, indicating domain-specific development. The results imply that each theory is partly true: the late maturity theory holds for face memory, and the early maturity theory for face perception.

Converging evidence that left extrastriate body area supports visual sensitivity to social interactions.

Navigating our complex social world requires processing the interactions we observe. Recent psychophysical and neuroimaging studies provide parallel evidence that the human visual system may be attuned to efficiently perceive dyadic interactions. This work implies, but has not yet demonstrated, that activity in body-selective cortical regions causally supports efficient visual perception of interactions. We adopt a multi-method approach to close this important gap. First, using a large fMRI dataset (n = 92), we found that the left hemisphere extrastriate body area (EBA) responds more to face-to-face than non-facing dyads. Second, we replicated a behavioral marker of visual sensitivity to interactions: categorization of facing dyads is more impaired by inversion than non-facing dyads. Third, in a pre-registered experiment, we used fMRI-guided transcranial magnetic stimulation to show that online stimulation of the left EBA, but not a nearby control region, abolishes this selective inversion effect. Activity in left EBA, thus, causally supports the efficient perception of social interactions.

Beyond human-likeness: Socialness is more influential when attributing mental states to robots.

We sought to replicate and expand previous work showing that the more human-like a robot appears, the more willing people are to attribute mind-like capabilities and socially engage with it. Forty-two participants played games against a human, a humanoid robot, a mechanoid robot, and a computer algorithm while undergoing functional neuroimaging. We confirmed that the more human-like the agent, the more participants attributed a mind to them. However, exploratory analyses revealed that the perceived socialness of an agent appeared to be as, if not more, important for mind attribution. Our findings suggest top-down knowledge cues may be equally or possibly more influential than bottom-up stimulus cues when exploring mind attribution in non-human agents. While further work is now required to test this hypothesis directly, these preliminary findings hold important implications for robotic design and to understand and test the flexibility of human social cognition when people engage with artificial agents.

Auditory dyadic interactions through the "eye" of the social brain: How visual is the posterior STS interaction region?

Human interactions contain potent social cues that meet not only the eye but also the ear. Although research has identified a region in the posterior superior temporal sulcus as being particularly sensitive to visually presented social interactions (SI-pSTS), its response to auditory interactions has not been tested. Here, we used fMRI to explore brain response to auditory interactions, with a focus on temporal regions known to be important in auditory processing and social interaction perception. In Experiment 1, monolingual participants listened to two-speaker conversations (intact or sentence-scrambled) and one-speaker narrations in both a known and an unknown language. Speaker number and conversational coherence were explored in separately localised regions-of-interest (ROI). In Experiment 2, bilingual participants were scanned to explore the role of language comprehension. Combining univariate and multivariate analyses, we found initial evidence for a heteromodal response to social interactions in SI-pSTS. Specifically, right SI-pSTS preferred auditory interactions over control stimuli and represented information about both speaker number and interactive coherence. Bilateral temporal voice areas (TVA) showed a similar, but less specific, profile. Exploratory analyses identified another auditory-interaction sensitive area in anterior STS. Indeed, direct comparison suggests modality specific tuning, with SI-pSTS preferring visual information while aSTS prefers auditory information. Altogether, these results suggest that right SI-pSTS is a heteromodal region that represents information about social interactions in both visual and auditory domains. Future work is needed to clarify the roles of TVA and aSTS in auditory interaction perception and further probe right SI-pSTS interaction-selectivity using non-semantic prosodic cues.

Attentional bias towards social interactions during viewing of naturalistic scenes.

Human visual attention is readily captured by the social information in scenes. Multiple studies have shown that social areas of interest (AOIs) such as faces and bodies attract more attention than non-social AOIs (e.g., objects or background). However, whether this attentional bias is moderated by the presence (or absence) of a social interaction remains unclear. Here, the gaze of 70 young adults was tracked during the free viewing of 60 naturalistic scenes. All photographs depicted two people, who were either interacting or not. Analyses of dwell time revealed that more attention was spent on human than background AOIs in the interactive pictures. In non-interactive pictures, however, dwell time did not differ between AOI type. In the time-to-first-fixation analysis, humans always captured attention before other elements of the scene, although this difference was slightly larger in interactive than non-interactive scenes. These findings confirm the existence of a bias towards social information in attentional capture and suggest our attention values social interactions beyond the presence of two people.

Neural correlates of coherent and biological motion perception in autism.

Recent evidence suggests those with autism may be generally impaired in visual motion perception. To examine this, we investigated both coherent and biological motion processing in adolescents with autism employing both psychophysical and fMRI methods. Those with autism performed as well as matched controls during coherent motion perception but had significantly higher thresholds for biological motion perception. The autism group showed reduced posterior Superior Temporal Sulcus (pSTS), parietal and frontal activity during a biological motion task while showing similar levels of activity in MT+/V5 during both coherent and biological motion trials. Activity in MT+/V5 was predictive of individual coherent motion thresholds in both groups. Activity in dorsolateral prefrontal cortex (DLPFC) and pSTS was predictive of biological motion thresholds in control participants but not in those with autism. Notably, however, activity in DLPFC was negatively related to autism symptom severity. These results suggest that impairments in higher-order social or attentional networks may underlie visual motion deficits observed in autism.