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).

High-Level Representations in Human Occipito-Temporal Cortex Are Indexed by Distal Connectivity.

Human object recognition is dependent on occipito-temporal cortex (OTC), but a complete understanding of the complex functional architecture of this area must account for how it is connected to the wider brain. Converging functional magnetic resonance imaging evidence shows that univariate responses to different categories of information (e.g., faces, bodies, and nonhuman objects) are strongly related to, and potentially shaped by, functional and structural connectivity to the wider brain. However, to date, there have been no systematic attempts to determine how distal connectivity and complex local high-level responses in occipito-temporal cortex (i.e., multivoxel response patterns) are related. Here, we show that distal functional connectivity is related to, and can reliably index, high-level representations for several visual categories (i.e., tools, faces, and places) within occipito-temporal cortex; that is, voxel sets that are strongly connected to distal brain areas show higher pattern discriminability than less well-connected sets do. We further show that in several cases, pattern discriminability is higher in sets of well-connected voxels than sets defined by local activation (e.g., strong amplitude responses to faces in fusiform face area). Together, these findings demonstrate the important relationship between the complex functional organization of occipito-temporal cortex and wider brain connectivity.SIGNIFICANCE STATEMENT Human object recognition relies strongly on OTC, yet responses in this broad area are often considered in relative isolation to the rest of the brain. We employ a novel connectivity-guided voxel selection approach with functional magnetic resonance imaging data to show higher sensitivity to information (i.e., higher multivoxel pattern discriminability) in voxel sets that share strong connectivity to distal brain areas, relative to (1) voxel sets that are less strongly connected, and in several cases, (2) voxel sets that are defined by strong local response amplitude. These findings underscore the importance of distal contributions to local processing in OTC.

The role of the ventrolateral anterior temporal lobes in social cognition.

A key challenge for neurobiological models of social cognition is to elucidate whether brain regions are specialised for that domain. In recent years, discussion surrounding the role of anterior temporal regions epitomises such debates; some argue the anterior temporal lobe (ATL) is part of a domain-specific network for social processing, while others claim it comprises a domain-general hub for semantic representation. In the present study, we used ATL-optimised fMRI to map the contribution of different ATL structures to a variety of paradigms frequently used to probe a crucial social ability, namely 'theory of mind' (ToM). Using multiple tasks enables a clearer attribution of activation to ToM as opposed to idiosyncratic features of stimuli. Further, we directly explored whether these same structures are also activated by a non-social task probing semantic representations. We revealed that common to all of the tasks was activation of a key ventrolateral ATL region that is often invisible to standard fMRI. This constitutes novel evidence in support of the view that the ventrolateral ATL contributes to social cognition via a domain-general role in semantic processing and against claims of a specialised social function.

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.

Characterizing the discriminability of visual categorical information in strongly connected voxels.

Functional brain responses are strongly influenced by connectivity. Recently, we demonstrated a major example of this: category discriminability within occipitotemporal cortex (OTC) is enhanced for voxel sets that share strong functional connectivity to distal brain areas, relative to those that share lesser connectivity. That is, within OTC regions, sets of 'most-connected' voxels show improved multivoxel pattern discriminability for tool-, face-, and place stimuli relative to voxels with weaker connectivity to the wider brain. However, understanding whether these effects generalize to other domains (e.g. body perception network), and across different levels of the visual processing streams (e.g. dorsal as well as ventral stream areas) is an important extension of this work. Here, we show that this so-called connectivity-guided decoding (CGD) effect broadly generalizes across a wide range of categories (tools, faces, bodies, hands, places). This effect is robust across dorsal stream areas, but less consistent in earlier ventral stream areas. In the latter regions, category discriminability is generally very high, suggesting that extraction of category-relevant visual properties is less reliant on connectivity to downstream areas. Further, CGD effects are primarily expressed in a category-specific manner: For example, within the network of tool regions, discriminability of tool information is greater than non-tool information. The connectivity-guided decoding approach shown here provides a novel demonstration of the crucial relationship between wider brain connectivity and complex local-level functional responses at different levels of the visual processing streams. Further, this approach generates testable new hypotheses about the relationships between connectivity and local selectivity.

Fine-grained knowledge about manipulable objects is well-predicted by contrastive language image pre-training.

Object recognition is an important ability that relies on distinguishing between similar objects (e.g., deciding which utensil(s) to use at different stages of meal preparation). Recent work describes the fine-grained organization of knowledge about manipulable objects via the study of the constituent dimensions that are most relevant to human behavior, for example, vision, manipulation, and function-based properties. A logical extension of this work concerns whether or not these dimensions are uniquely human, or can be approximated by deep learning. Here, we show that behavioral dimensions are generally well-predicted by CLIP-ViT - a multimodal network trained on a large and diverse set of image-text pairs. Moreover, this model outperforms comparison networks pre-trained on smaller, image-only datasets. These results demonstrate the impressive capacity of CLIP-ViT to approximate fine-grained object knowledge. We discuss the possible sources of this benefit relative to other models (e.g., multimodal vs. image-only pre-training, dataset size, architecture).

Optimistic Youth: Young Adults Predicted a Faster Decrease in Risk during COVID-19 Emergency State in Portugal.

Perception of risk is known to change throughout the lifespan. Previous studies showed that younger adults are more prone to risk behaviours than older adults. Do these age-related differences influence risk perception during a pandemic crisis? Here, we investigated how age influenced predicted risk during the COVID-19 emergency state in Portugal. We show that time-projected estimations (e.g., appraisals based on 'now' vs. 'in two weeks' time', or 'in four weeks' time') of both risk behaviour and importance of transmission prevention decrease over time. Importantly, projected risk decreased more steeply for younger than older adults. Our findings suggest that younger adults have a different perception of epidemic-related risk than older adults. This seems to support the view that public health policy making during epidemics should differentially target younger adults.

A perceção do risco muda ao longo da vida. Estudos anteriores mostraram que os jovens adultos são mais propensos a comportamentos de risco do que os adultos mais velhos. Será que estas diferenças relacionadas com a idade influenciam a perceção de risco durante uma crise pandémica? Aqui, investigámos como a idade influenciou o risco previsto durante o estado de emergência da COVID-19 em Portugal. Demonstramos que as estimativas de tempo projetadas (e.g., avaliações baseadas em agora vs. "daqui a duas semanas", ou "daqui a quatro semanas") tanto do comportamento de risco como da importância da prevenção da transmissão diminuem ao longo do tempo. É importante notar que o risco projetado diminuiu mais acentuadamente para os jovens adultos do que para os adultos mais velhos. Os nossos resultados sugerem que os jovens adultos têm uma perceção do risco relacionado com epidemias diferente do que os adultos mais velhos e parecem corroborar a perspetiva de que a elaboração de políticas de saúde pública durante epidemias deve visar de forma diferente os jovens adultos.

Developmental changes in visual responses to social interactions.

Recent evidence demonstrates that a region of the posterior superior temporal sulcus (pSTS) is selective to visually observed social interactions in adults. In contrast, little is known about neural responses to social interactions in children. Here, we used fMRI to ask whether the pSTS is 'tuned' to social interactions in children at all, and if so, how selectivity might differ from adults. This was investigated in the pSTS, along with several other socially-tuned regions in neighbouring temporal cortex: extrastriate body area, face selective STS, fusiform face area, and mentalizing selective temporo-parietal junction. Both children and adults showed selectivity to social interaction within right pSTS, while only adults showed selectivity on the left. Adults also showed both more focal and greater selectivity than children (6-12 years) bilaterally. Exploratory sub-group analyses showed that younger children (6-8), but not older children (9-12), are less selective than adults on the right, while there was a continuous developmental trend (adults > older > younger) in left pSTS. These results suggest that, over development, the neural response to social interactions is characterized by increasingly more selective, focal, and bilateral pSTS responses, a process that likely continues into adolescence.

Head motion during fMRI tasks is reduced in children and adults if participants take breaks.

Head motion remains a challenging confound in functional magnetic resonance imaging (fMRI) studies of both children and adults. Most pediatric neuroimaging labs have developed experience-based, child-friendly standards concerning e.g. the maximum length of a session or the time between mock scanner training and actual scanning. However, it is unclear which factors of child-friendly neuroimaging approaches are effective in reducing head motion. Here, we investigate three main factors including (i) time lag of mock scanner training to the actual scan, (ii) prior scan time, and (iii) task engagement in a dataset of 77 children (aged 6-13) and 64 adults (aged 18-35) using a multilevel modeling approach. In children, distributing fMRI data acquisition across multiple same-day sessions reduces head motion. In adults, motion is reduced after inside-scanner breaks. Despite these positive effects of splitting up data acquisition, motion increases over the course of a study as well as over the course of a run in both children and adults. Our results suggest that splitting up fMRI data acquisition is an effective tool to reduce head motion in general. At the same time, different ways of splitting up data acquisition benefit children and adults.

Neural responses to visually observed social interactions.

Success in the social world requires the ability to perceive not just individuals and their actions, but pairs of people and the interactions between them. Despite the complexity of social interactions, humans are adept at interpreting those interactions they observe. Although the brain basis of this remarkable ability has remained relatively unexplored, converging functional MRI evidence suggests the posterior superior temporal sulcus (pSTS) is centrally involved. Here, we sought to determine whether this region is sensitive to both the presence of interactive information, as well as to the content of qualitatively different interactions (i.e. competition vs. cooperation). Using point-light human figure stimuli, we demonstrate that the right pSTS is maximally activated when contrasting dyadic interactions vs. dyads performing independent, non-interactive actions. We then used this task to localize the same pSTS region in an independent participant group, and tested responses to non-human moving shape stimuli (i.e. two circles' movements conveying either interactive or non-interactive behaviour). We observed significant support vector machine classification for both the presence and type of interaction (i.e. interaction vs. non-interaction, and competition vs. cooperation, respectively) in the pSTS, as well as neighbouring temporo-parietal junction (TPJ). These findings demonstrate the important role that these regions play in perceiving and understanding social interactions, and lay the foundations for further research to fully characterize interaction responses in these areas.

Neurodevelopmental perspectives on dance learning: Insights from early adolescence and young adulthood.

Studies investigating human motor learning and movement perception have shown that similar sensorimotor brain regions are engaged when we observe or perform action sequences. However, the way these networks enable translation of complex observed actions into motor commands-such as in the context of dance-remains poorly understood. Emerging evidence suggests that the ability to encode specific visuospatial and kinematic movement properties encountered via different routes of sensorimotor experience may be an integral component of action learning throughout development. Using a video game-based dance training paradigm, we demonstrate that patterns of voxel activity in visual and sensorimotor brain regions when perceiving movements following training are related to the sensory modalities through which these movements were encountered during whole-body dance training. Compared to adolescents, young adults in this study demonstrated more distinctive patterns of voxel activity in visual cortices in relation to different types of sensorimotor experience. This finding suggests that cortical maturity might influence the extent to which prior sensorimotor experiences shape brain activity when watching others in action, and potentially impact how we acquire new motor skills.