Noncortical coding of biological motion in newborn chicks' brain.

Biological motion, the typical movement of vertebrates, is perceptually salient for many animal species. Newly hatched domestic chicks and human newborns show a spontaneous preference for simple biological motion stimuli (point-light displays) at birth prior to any visual learning. Despite evidence of such preference at birth, neural studies performed so far have focused on a specialized neural network involving primarily cortical areas. Here, we presented newly hatched visually naïve domestic chicks to either biological or rigid motion stimuli and measured for the first time their brain activation. Immediate Early Gene (c-Fos) expression revealed selective activation in the preoptic area of the hypothalamus and the nucleus taeniae of the amygdala. These results suggest that subpallial/subcortical regions play a crucial role in biological motion perception at hatching, paving the way for future studies on adult animals, including humans.

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).

Disentangling Object Category Representations Driven by Dynamic and Static Visual Input.

Humans can label and categorize objects in a visual scene with high accuracy and speed, a capacity well characterized with studies using static images. However, motion is another cue that could be used by the visual system to classify objects. To determine how motion-defined object category information is processed by the brain in the absence of luminance-defined form information, we created a novel stimulus set of "object kinematograms" to isolate motion-defined signals from other sources of visual information. Object kinematograms were generated by extracting motion information from videos of 6 object categories and applying the motion to limited-lifetime random dot patterns. Using functional magnetic resonance imaging (fMRI) (n = 15, 40% women), we investigated whether category information from the object kinematograms could be decoded within the occipitotemporal and parietal cortex and evaluated whether the information overlapped with category responses to static images from the original videos. We decoded object category for both stimulus formats in all higher-order regions of interest (ROIs). More posterior occipitotemporal and ventral regions showed higher accuracy in the static condition, while more anterior occipitotemporal and dorsal regions showed higher accuracy in the dynamic condition. Further, decoding across the two stimulus formats was possible in all regions. These results demonstrate that motion cues can elicit widespread and robust category responses on par with those elicited by static luminance cues, even in ventral regions of visual cortex that have traditionally been associated with primarily image-defined form processing.SIGNIFICANCE STATEMENT Much research on visual object recognition has focused on recognizing objects in static images. However, motion is a rich source of information that humans might also use to categorize objects. Here, we present the first study to compare neural representations of several animate and inanimate objects when category information is presented in two formats: static cues or isolated dynamic motion cues. Our study shows that, while higher-order brain regions differentially process object categories depending on format, they also contain robust, abstract category representations that generalize across format. These results expand our previous understanding of motion-derived animate and inanimate object category processing and provide useful tools for future research on object category processing driven by multiple sources of visual information.

Evidence for a role of synchrony but not common fate in the perception of biological group movements.

Extensive research has shown that observers are able to efficiently extract summary information from groups of people. However, little is known about the cues that determine whether multiple people are represented as a social group or as independent individuals. Initial research on this topic has primarily focused on the role of static cues. Here, we instead investigate the role of dynamic cues. In two experiments with male and female human participants, we use EEG frequency tagging to investigate the influence of two fundamental Gestalt principles - synchrony and common fate - on the grouping of biological movements. In Experiment 1, we find that brain responses coupled to four point-light figures walking together are enhanced when they move in sync vs. out of sync, but only when they are presented upright. In contrast, we found no effect of movement direction (i.e., common fate). In Experiment 2, we rule out that synchrony takes precedence over common fate by replicating the null effect of movement direction while keeping synchrony constant. These results suggest that synchrony plays an important role in the processing of biological group movements. In contrast, the role of common fate is less clear and will require further research.

Distributed and hierarchical neural encoding of multidimensional biological motion attributes in the human brain.

The human visual system can efficiently extract distinct physical, biological, and social attributes (e.g. facing direction, gender, and emotional state) from biological motion (BM), but how these attributes are encoded in the brain remains largely unknown. In the current study, we used functional magnetic resonance imaging to investigate this issue when participants viewed multidimensional BM stimuli. Using multiple regression representational similarity analysis, we identified distributed brain areas, respectively, related to the processing of facing direction, gender, and emotional state conveyed by BM. These brain areas are governed by a hierarchical structure in which the respective neural encoding of facing direction, gender, and emotional state is modulated by each other in descending order. We further revealed that a portion of the brain areas identified in representational similarity analysis was specific to the neural encoding of each attribute and correlated with the corresponding behavioral results. These findings unravel the brain networks for encoding BM attributes in consideration of their interactions, and highlight that the processing of multidimensional BM attributes is recurrently interactive.

The dual nature of working memory deficits: methamphetamine abusers have more impaired social working memory capacity than canonical working memory capacity.

Social working memory (WM) temporarily retains and manipulates various aspects of social information. Extensive research has highlighted impaired social cognitive functions in individuals with substance addiction. However, the specific deficit in social WM within this population remains notably understudied. Bridging this gap, we investigated social WM capacity using biological motion (BM) stimuli in methamphetamine (MA) abusers compared to an inmate control group, alongside contrasting these findings with their canonical WM deficits. Across two studies, we recruited female MA abusers (N = 80) undergoing post-isolation rehabilitation within a mandatory confinement circumstance. To ensure a pertinent comparison, we recruited female inmates (N = 80) subjected to comparable confinement. Results show substantial BM WM impairment in MA abusers, yet non-BM WM remains mostly intact. These findings highlight a pronounced social WM deficit in MA abusers, surpassing their canonical WM deficit relative to inmate controls. This suggests a distinct dissociation between social and canonical WM processing.

Cortical encoding of rhythmic kinematic structures in biological motion.

Biological motion (BM) perception is of great survival value to human beings. The critical characteristics of BM information lie in kinematic cues containing rhythmic structures. However, how rhythmic kinematic structures of BM are dynamically represented in the brain and contribute to visual BM processing remains largely unknown. Here, we probed this issue in three experiments using electroencephalogram (EEG). We found that neural oscillations of observers entrained to the hierarchical kinematic structures of the BM sequences (i.e., step-cycle and gait-cycle for point-light walkers). Notably, only the cortical tracking of the higher-level rhythmic structure (i.e., gait-cycle) exhibited a BM processing specificity, manifested by enhanced neural responses to upright over inverted BM stimuli. This effect could be extended to different motion types and tasks, with its strength positively correlated with the perceptual sensitivity to BM stimuli at the right temporal brain region dedicated to visual BM processing. Modeling results further suggest that the neural encoding of spatiotemporally integrative kinematic cues, in particular the opponent motions of bilateral limbs, drives the selective cortical tracking of BM information. These findings underscore the existence of a cortical mechanism that encodes periodic kinematic features of body movements, which underlies the dynamic construction of visual BM perception.

The walking sick: Perception of experimental sickness from biological motion.

Identification of sick conspecifics allows for avoidance of infectious threats, and is therefore an important behavioral defense against diseases. Here, we investigated if humans can identify sick individuals solely from biological motion and posture (using point-light displays). Additionally, we sought to determine which movements and sickness parameters would predict such detection. We collected video clips and derived point-light displays (one stride presented in a loop) of sick walkers (injected with lipopolysaccharide at 2.0 ng/kg body weight) and the same walkers when healthy (injected with saline). We then presented these displays to two groups, one group classified each walker as sick or healthy (study 1, n = 106), and the other group scored the walkers' health on a visual analogue scale (study 2, n = 106). The raters were able to identify sick individuals above chance, and rated sick walkers as having worse health, both from observing video clips and point-light displays. Furthermore, both sickness detection and worse apparent health were predicted by inflammation-induced increase in rigidity and slower walking, but not other cues. Altogether, these findings indicate that biological motion can serve as a sickness cue, possibly allowing humans to identify sick conspecifics from a distance, and thereby allowing for disease avoidance.

EEG Frequency Tagging Reveals the Integration of Form and Motion Cues into the Perception of Group Movement.

The human brain has dedicated mechanisms for processing other people's movements. Previous research has revealed how these mechanisms contribute to perceiving the movements of individuals but has left open how we perceive groups of people moving together. Across three experiments, we test whether movement perception depends on the spatiotemporal relationships among the movements of multiple agents. In Experiment 1, we combine EEG frequency tagging with apparent human motion and show that posture and movement perception can be dissociated at harmonically related frequencies of stimulus presentation. We then show that movement but not posture processing is enhanced when observing multiple agents move in synchrony. Movement processing was strongest for fluently moving synchronous groups (Experiment 2) and was perturbed by inversion (Experiment 3). Our findings suggest that processing group movement relies on binding body postures into movements and individual movements into groups. Enhanced perceptual processing of movement synchrony may form the basis for higher order social phenomena such as group alignment and its social consequences.

Autistic children's visual sensitivity to face movement.

There is a pressing need for studies of large sample sizes and variable age ranges to delineate the mechanism underlying reduced visual attention to biological motion in autism. Here we focused on the basic movement of the eyes or mouth in guiding attention. The stimuli face blinked continuously or moved the mouth silently. In a large sample (145 autistic and 132 non-autistic participants) ranging from 3 to 17 years old, we assessed whether autistic participants showed reduced visual attention to basic movement of the eyes or mouth using a free-viewing eye-tracking task. We found that, like non-autistic participants, autistic participants increased their eye-looking time when viewing the blinking face and increased mouth-looking time when viewing the mouth-moving face. Furthermore, these effects were stable across ages, suggesting the presence of a developmentally stable attentional capture by basic face movements in both groups. We also found that autistic participants looked less at basic face movement than non-autistic participants. Our results suggest that autistic children and adolescents could modulate their visual attention to the basic face movements, but their modulation effect is weaker than non-autistic participants. These results further our understanding of the mechanism underlying visual attention-to-face movement in autistic people.

The gender-based facing bias in 3-D biological motion perception.

In biological motion perception, movements of several point lights can evoke a vivid impression of living animals, including humans. Recent studies have reported that male point-light walkers tend to be perceived as facing toward the viewer more than female walkers, and have hypothesized that the gender-based facing bias arises from motion signals. The purpose of this study was to test this hypothesis under experimental conditions where binocular disparity was added to biological motion stimuli. In the two experiments reported here, participants were presented with disparity-defined female and male point-light figures facing toward or away from the viewer. In Experiment 1, we measured "facing-the-viewer" responses in upright and inverted walker configurations. It was found that the facing bias was greater for the male walker than for the female walker in most disparity magnitudes, regardless of walker inversion. In Experiment 2, the walker stimuli were replaced by static snapshots of the walkers. The results showed that the facing bias did not differ between the female and male static figures. These results suggest that motion signals play an important role in producing the gender-based facing bias, even when binocular disparity is added to biological motion stimuli.

Different aspects of visual perception are important for 12-year social functioning depending on gestational age.

AIM: Perceptual mechanisms in social functioning might promote interventions. We investigated relations between visual perception and social functioning, in preterm children. METHODS: A prospective preterm cohort born in Uppsala County, Sweden, in 2004-2007 and 49 full-term controls were examined at 12 years. Aspects of visual perception, including static shapes, emotions and time to detect biological motion, were related to social functioning and visual acuity. RESULTS: The preterm group comprised 25 extremely preterm children, EPT, born below 28 gestational weeks and 53 children born between 28 and 31 weeks. Preterm children had difficulties in perception of static shapes (p = 0.004) and biological motion (p < 0.001), but not in emotion perception, compared to controls. In the EPT children, poorer shape perception and lower scores on emotion perception were associated with more social problems (p = 0.008) and lower visual acuity (p = 0.004). Shape perception explained more variance in social functioning than emotion perception. In controls, fewer social problems were linked to faster biological motion perception (p = 0.04). CONCLUSION: Static shape and biological motion perception was affected in the preterm groups. Biological motion perception was relevant for social functioning in full-term children. In EPT children, only shape perception was linked to social functioning, suggesting differential visual perception mechanisms for social deficits.

Construction and validation of the Dalian emotional movement open-source set (DEMOS).

Human body movements are important for emotion recognition and social communication and have received extensive attention from researchers. In this field, emotional biological motion stimuli, as depicted by point-light displays, are widely used. However, the number of stimuli in the existing material library is small, and there is a lack of standardized indicators, which subsequently limits experimental design and conduction. Therefore, based on our prior kinematic dataset, we constructed the Dalian Emotional Movement Open-source Set (DEMOS) using computational modeling. The DEMOS has three views (i.e., frontal 0°, left 45°, and left 90°) and in total comprises 2664 high-quality videos of emotional biological motion, each displaying happiness, sadness, anger, fear, disgust, and neutral. All stimuli were validated in terms of recognition accuracy, emotional intensity, and subjective movement. The objective movement for each expression was also calculated. The DEMOS can be downloaded for free from https://osf.io/83fst/ . To our knowledge, this is the largest multi-view emotional biological motion set based on the whole body. The DEMOS can be applied in many fields, including affective computing, social cognition, and psychiatry.

A two-stage framework for neural processing of biological motion.

It remains to be understood how biological motion is hierarchically computed, from discrimination of local biological motion animacy to global dynamic body perception. Here, we addressed this functional separation of the correlates of the perception of local biological motion from perception of global motion of a body. We hypothesized that local biological motion processing can be isolated, by using a single dot motion perceptual decision paradigm featuring the biomechanical details of local realistic motion of a single joint. To ensure that we were indeed tackling processing of biological motion properties we used discrimination instead of detection task. We discovered using representational similarity analysis that two key early dorsal and two ventral stream regions (visual motion selective hMT+ and V3A, extrastriate body area EBA and a region within fusiform gyrus FFG) showed robust and separable signals related to encoding of local biological motion and global motion-mediated shape. These signals reflected two independent processing stages, as revealed by representational similarity analysis and deconvolution of fMRI responses to each motion pattern. This study showed that higher level pSTS encodes both classes of biological motion in a similar way, revealing a higher-level integrative stage, reflecting scale independent biological motion perception. Our results reveal a two-stage framework for neural computation of biological motion, with an independent contribution of dorsal and ventral regions for the initial stage.

Human movements do not look the same in a tilted world: Gravitational constraints influence the perception of biological motion.

We investigated whether gravitational constraints influence the interaction of visual, proprioceptive and vestibular cues for Biological Motion Perception (BMP). Participants were asked to distinguish between plausible and random point-light movements, while passively placed in either an upright or a tilted body orientation. Manipulating the body orientation with respect to gravity leads to different gravitational signals transmitted by the visual, proprioceptive, and vestibular systems. Participants were overall faster in distinguishing plausible point-light movements than random movements. Critically, response times for biologically plausible point-light movements - but not for random movements - were significantly prolonged in the tilted body orientation. Our results suggest that BMP depends not only on the spatial-temporal cues embedded in point-light movements but also rely on the congruency between current gravitational signals detected by the sensory systems and our previous knowledge of terrestrial gravity. STATEMENT OF RELEVANCE: As humankind is preparing for a new space age, understanding how gravity influences behaviour and cognition has never been more pressing. All living organisms have evolved to survive in a terrestrial gravitational field. Although we cannot consciously feel gravity, it has an impact in our life: it affects how we move and interact with the external environment. The sensory signals from the vestibular system are continuously combined with visual and proprioceptive cues to help us in maintaining a stable representation of the world. Here we placed participants in a tilted body orientation and were able to determine that a conflict between prior gravitational knowledge and what was actively sensed about gravity affected human Biological Movement Perception. Humans suffer changes in perception under non-terrestrial gravity conditions that may potentially compromise performance during space exploration.

Differences in working memory coding of biological motion attributed to oneself and others.

The question how the brain distinguishes between information about self and others is of fundamental interest to both philosophy and neuroscience. In this functional magnetic resonance imaging (fMRI) study, we sought to distinguish the neural substrates of representing a full-body movement as one's movement and as someone else's movement. Participants performed a delayed match-to-sample working memory task where a retained full-body movement (displayed using point-light walkers) was arbitrarily labeled as one's own movement or as performed by someone else. By using arbitrary associations we aimed to address a limitation of previous studies, namely that our own movements are more familiar to us than movements of other people. A searchlight multivariate decoding analysis was used to test where information about types of movement and about self-association was coded. Movement specific activation patterns were found in a network of regions also involved in perceptual processing of movement stimuli, however not in early sensory regions. Information about whether a memorized movement was associated with the self or with another person was found to be coded by activity in the left middle frontal gyrus (MFG), left inferior frontal gyrus (IFG), bilateral supplementary motor area, and (at reduced threshold) in the left temporoparietal junction (TPJ). These areas are frequently reported as involved in action understanding (IFG, MFG) and domain-general self/other distinction (TPJ). Finally, in univariate analysis we found that selecting a self-associated movement for retention was related to increased activity in the ventral medial prefrontal cortex.

Decoding point-light displays and fully visible hand grasping actions within the action observation network.

Action observation typically recruits visual areas and dorsal and ventral sectors of the parietal and premotor cortex. This network has been collectively termed as extended action observation network (eAON). Within this network, the elaboration of kinematic aspects of biological motion is crucial. Previous studies investigated these aspects by presenting subjects with point-light displays (PLDs) videos of whole-body movements, showing the recruitment of some of the eAON areas. However, studies focused on cortical activation during observation of PLDs grasping actions are lacking. In the present functional magnetic resonance imaging (fMRI) study, we assessed the activation of eAON in healthy participants during the observation of both PLDs and fully visible hand grasping actions, excluding confounding effects due to low-level visual features, motion, and context. Results showed that the observation of PLDs grasping stimuli elicited a bilateral activation of the eAON. Region of interest analyses performed on visual and sensorimotor areas showed no significant differences in signal intensity between PLDs and fully visible experimental conditions, indicating that both conditions evoked a similar motor resonance mechanism. Multivoxel pattern analysis (MVPA) revealed significant decoding of PLDs and fully visible grasping observation conditions in occipital, parietal, and premotor areas belonging to eAON. Data show that kinematic features conveyed by PLDs stimuli are sufficient to elicit a complete action representation, suggesting that these features can be disentangled within the eAON from the features usually characterizing fully visible actions. PLDs stimuli could be useful in assessing which areas are recruited, when only kinematic cues are available, for action recognition, imitation, and motor learning.

Following Other People's Footsteps: A Contextual-Attraction Effect Induced by Biological Motion.

Our visual system is bombarded with numerous social interactions that form intangible social bonds among people, as exemplified by synchronized walking in crowds. Here, we investigated whether these perceived social bonds implicitly intrude on visual perception and induce a contextual effect. Using multiple point-light walkers and a classical contextual paradigm, we tested 72 college-age adults across six experiments and found that the perceived direction of the central walker was attracted toward the direction of the surrounding walkers. The observed contextual-attraction effect occurred even when the surrounding walkers differed from the central walker in gender and walking speed but disappeared when they were asynchronously presented or replaced by inanimate motion. Strikingly, this contextual-attraction effect partially persisted in the context of local motion rather than static figures. These findings, in contrast to the typical contextual-repulsion effect, lend support for the distinctiveness of perceived social bonds on contextual modulation and suggest a specialized contextual mechanism tuned to social factors.

Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia.

Schizophrenia is associated with marked impairments in social cognition. However, the neural correlates of these deficits remain unclear. Here we use naturalistic stimuli to examine the role of the right temporoparietal junction/posterior superior temporal sulcus (TPJ-pSTS)-an integrative hub for the cortical networks pertinent to the understanding complex social situations-in social inference, a key component of social cognition, in schizophrenia. Twenty-seven schizophrenia participants and 21 healthy control subjects watched a clip of the film The Good, the Bad and the Ugly while high resolution multiband functional MRI images were collected. We used inter-subject correlation to measure the evoked activity, which we then compared to social cognition as measured by The Awareness of Social Inference Test (TASIT). We also compared between groups the TPJ-pSTS blood oxygen level-dependent activity (i) relationship with the motion content in the film; (ii) synchronization with other cortical areas involved in the viewing of the movie; and (iii) relationship with the frequency of saccades made during the movie. Activation deficits were greatest in middle TPJ (TPJm) and correlated significantly with impaired TASIT performance across groups. Follow-up analyses of the TPJ-pSTS revealed decreased synchronization with other cortical areas, decreased correlation with the motion content of the movie, and decreased correlation with the saccades made during the movie. The functional impairment of the TPJm, a hub area in the middle of the TPJ-pSTS, predicts deficits in social inference in schizophrenia participants by disrupting the integration of visual motion processing into the TPJ. This disrupted integration then affects the use of the TPJ to guide saccades during the visual scanning of the movie clip. These findings suggest that the TPJ may be a treatment target for improving deficits in a key component of social cognition in schizophrenia participants.

Visual Sensory Cortices Causally Contribute to Auditory Word Recognition Following Sensorimotor-Enriched Vocabulary Training.

Despite a rise in the use of "learning by doing" pedagogical methods in praxis, little is known as to how the brain benefits from these methods. Learning by doing strategies that utilize complementary information ("enrichment") such as gestures have been shown to optimize learning outcomes in several domains including foreign language (L2) training. Here we tested the hypothesis that behavioral benefits of gesture-based enrichment are critically supported by integrity of the biological motion visual cortices (bmSTS). Prior functional neuroimaging work has implicated the visual motion cortices in L2 translation following sensorimotor-enriched training; the current study is the first to investigate the causal relevance of these structures in learning by doing contexts. Using neuronavigated transcranial magnetic stimulation and a gesture-enriched L2 vocabulary learning paradigm, we found that the bmSTS causally contributed to behavioral benefits of gesture-enriched learning. Visual motion cortex integrity benefitted both short- and long-term learning outcomes, as well as the learning of concrete and abstract words. These results adjudicate between opposing predictions of two neuroscientific learning theories: While reactivation-based theories predict no functional role of specialized sensory cortices in vocabulary learning outcomes, the current study supports the predictive coding theory view that these cortices precipitate sensorimotor-based learning benefits.