Perception of biological motion in schizophrenia and healthy individuals: a behavioral and FMRI study

Background

Anomalous visual perception is a common feature of schizophrenia plausibly associated with impaired social cognition that, in turn, could affect social behavior. Past research suggests impairment in biological motion perception in schizophrenia. Behavioral and functional magnetic resonance imaging (fMRI) experiments were conducted to verify the existence of this impairment, to clarify its perceptual basis, and to identify accompanying neural concomitants of those deficits.

Methodology/Findings

In Experiment 1, we measured ability to detect biological motion portrayed by point-light animations embedded within masking noise. Experiment 2 measured discrimination accuracy for pairs of point-light biological motion sequences differing in the degree of perturbation of the kinematics portrayed in those sequences. Experiment 3 measured BOLD signals using event-related fMRI during a biological motion categorization task.Compared to healthy individuals, schizophrenia patients performed significantly worse on both the detection (Experiment 1) and discrimination (Experiment 2) tasks. Consistent with the behavioral results, the fMRI study revealed that healthy individuals exhibited strong activation to biological motion, but not to scrambled motion in the posterior portion of the superior temporal sulcus (STSp). Interestingly, strong STSp activation was also observed for scrambled or partially scrambled motion when the healthy participants perceived it as normal biological motion. On the other hand, STSp activation in schizophrenia patients was not selective to biological or scrambled motion.

Conclusion

Schizophrenia is accompanied by difficulties discriminating biological from non-biological motion, and associated with those difficulties are altered patterns of neural responses within brain area STSp. The perceptual deficits exhibited by schizophrenia patients may be an exaggerated manifestation of neural events within STSp associated with perceptual errors made by healthy observers on these same tasks. The present findings fit within the context of theories of delusion involving perceptual and cognitive processes.     

Speed of Human Biological Form and Motion Processing

Recent work suggests that biological motion processing can begin within ~110 ms of stimulus onset, as indexed by the P1 component of the event-related potential (ERP). Here, we investigated whether modulation of the P1 component reflects configural processing alone, rather than the processing of both configuration and motion cues. A three-stimulus oddball task was employed to evaluate bottom-up processing of biological motion. Intact point-light walkers (PLWs) or scrambled PLWs served as distractor stimuli, whereas point-light displays of tool motion served as standard and target stimuli. In a second experiment, the same design was used, but the dynamic stimuli were replaced with static point-light displays. The first experiment revealed that dynamic PLWs elicited a larger P1 as compared to scrambled PLWs. A similar P1 increase was also observed for static PLWs in the second experiment, indicating that these stimuli were more salient than static, scrambled PLWs. These findings suggest that the visual system can rapidly extract global form information from static PLWs and that the observed P1 effect for dynamic PLWs is not dependent on the presence of motion cues. Finally, we found that the N1 component was sensitive to dynamic, but not static, PLWs, suggesting that this component reflects the processing of both form and motion information. The sensitivity of P1 to static PLWs has implications for dynamic form models of biological motion processing that posit temporal integration of configural cues present in individual frames of PLW animations.     

Investigating the status of biological stimuli as objects of attention in multiple object tracking

Background

Humans are able to track multiple simultaneously moving objects. A number of factors have been identified that can influence the ease with which objects can be attended and tracked. Here, we explored the possibility that object tracking abilities may be specialized for tracking biological targets such as people.

Methodology/Principal Findings

We used the Multiple Object Tracking (MOT) paradigm to explore whether the high-level biological status of the targets affects the efficiency of attentional selection and tracking. In Experiment 1, we assessed the tracking of point-light biological motion figures. As controls, we used either the same stimuli or point-light letters, presented in upright, inverted or scrambled configurations. While scrambling significantly affected performance for both letters and point-light figures, there was an effect of inversion restricted to biological motion, inverted figures being harder to track. In Experiment 2, we found that tracking performance was equivalent for natural point-light walkers and ‘moon-walkers’, whose implied direction was incongruent with their actual direction of motion. In Experiment 3, we found higher tracking accuracy for inverted faces compared with upright faces. Thus, there was a double dissociation between inversion effects for biological motion and faces, with no inversion effect for our non-biological stimuli (letters, houses).

Conclusions/Significance

MOT is sensitive to some, but not all naturalistic aspects of biological stimuli. There does not appear to be a highly specialized role for tracking people. However, MOT appears constrained by principles of object segmentation and grouping, where effectively grouped, coherent objects, but not necessarily biological objects, are tracked most successfully.     

The Inversion Effect in Biological Motion Perception: Evidence for a “Life Detector”?

If biological-motion point-light displays are presented upside down, adequate perception is strongly impaired. Reminiscent of the inversion effect in face recognition, it has been suggested that the inversion effect in biological motion is due to impaired configural processing in a highly trained expert system. Here, we present data that are incompatible with this view. We show that observers can readily retrieve information about direction from scrambled point-light displays of humans and animals. Even though all configural information is entirely disrupted, perception of these displays is still subject to a significant inversion effect. Inverting only parts of the display reveals that the information about direction, as well as the associated inversion effect, is entirely carried by the local motion of the feet. We interpret our findings in terms of a visual filter that is tuned to the characteristic motion of the limbs of an animal in locomotion and hypothesize that this mechanism serves as a general detection system for the presence of articulated terrestrial animals.     

Biological Motion Primes the Animate/Inanimate Distinction in Infancy

Given that biological motion is both detected and preferred early in life, we tested the hypothesis that biological motion might be instrumental to infants’ differentiation of animate and inanimate categories. Infants were primed with either point-light displays of realistic biological motion, random motion, or schematic biological motion of an unfamiliar shape. After being habituated to these displays, 12-month-old infants categorized animals and vehicles as well as furniture and vehicles with the sequential touching task. The findings indicated that infants primed with point-light displays of realistic biological motion showed better categorization of animates than those exposed to random or schematic biological motion. These results suggest that human biological motion might be one of the motion cues that provide the building blocks for infants’ concept of animacy.     

Categorizing sex and identity from the biological motion of faces

Head and facial movements can provide valuable cues to identity in addition to their primary roles in communicating speech and expression [1-8]. Here we report experiments in which we have used recent motion capture and animation techniques to animate an average head [9]. These techniques have allowed the isolation of motion from other cues and have enabled us to separate rigid translations and rotations of the head from nonrigid facial motion. In particular, we tested whether human observers can judge sex and identity on the basis of this information. Results show that people can discriminate both between individuals and between males and females from motion-based information alone. Rigid head movements appear particularly useful for categorization on the basis of identity, while nonrigid motion is more useful for categorization on the basis of sex. Accuracy for both sex and identity judgements is reduced when faces are presented upside down, and this finding shows that performance is not based on low-level motion cues alone and suggests that the information is represented in an object-based motion-encoding system specialized for upright faces. Playing animations backward also reduced performance for sex judgements and emphasized the importance of direction specificity in admitting access to stored representations of characteristic male and female movements.     

Integrating biological motion: the role of grouping in the perception of point-light actions

The human visual system is highly sensitive to biological motion and manages to organize even a highly reduced point-light stimulus into a vivid percept of human action. The current study investigated to what extent the origin of this saliency of point-light displays is related to its intrinsic Gestalt qualities. In particular, we studied whether biological motion perception is facilitated when the elements can be grouped according to good continuation and similarity as Gestalt principles of perceptual organization. We found that both grouping principles enhanced biological motion perception but their effects differed when stimuli were inverted. These results provide evidence that Gestalt principles of good continuity and similarity also apply to more complex and dynamic meaningful stimuli.     

Electrophysiology and brain imaging of biological motion

The movements of the faces and bodies of other conspecifics provide stimuli of considerable interest to the social primate. Studies of single cells, field potential recordings and functional neuroimaging data indicate that specialized visual mechanisms exist in the superior temporal sulcus (STS) of both human and non-human primates that produce selective neural responses to moving natural images of faces and bodies. STS mechanisms also process simplified displays of biological motion involving point lights marking the limb articulations of animate bodies and geometrical shapes whose motion simulates purposeful behaviour. Facial movements such as deviations in eye gaze, important for gauging an individual's social attention, and mouth movements, indicative of potential utterances, generate particularly robust neural responses that differentiate between movement types. Collectively such visual processing can enable the decoding of complex social signals and through its outputs to limbic, frontal and parietal systems the STS may play a part in enabling appropriate affective responses and social behaviour.     

Perception of ‘Back-Channeling’ Nonverbal Feedback in Musical Duo Improvisation

In witnessing face-to-face conversation, observers perceive authentic communication according to the social contingency of nonverbal feedback cues (‘back-channeling’) by non-speaking interactors. The current study investigated the generality of this function by focusing on nonverbal communication in musical improvisation. A perceptual experiment was conducted to test whether observers can reliably identify genuine versus fake (mismatched) duos from musicians’ nonverbal cues, and how this judgement is affected by observers’ musical background and rhythm perception skill. Twenty-four musicians were recruited to perform duo improvisations, which included solo episodes, in two styles: standard jazz (where rhythm is based on a regular pulse) or free improvisation (where rhythm is non-pulsed). The improvisations were recorded using a motion capture system to generate 16 ten-second point-light displays (with audio) of the soloist and the silent non-soloing musician (‘back-channeler’). Sixteen further displays were created by splicing soloists with back-channelers from different duos. Participants (N = 60) with various musical backgrounds were asked to rate the point-light displays as either real or fake. Results indicated that participants were sensitive to the real/fake distinction in the free improvisation condition independently of musical experience. Individual differences in rhythm perception skill did not account for performance in the free condition, but were positively correlated with accuracy in the standard jazz condition. These findings suggest that the perception of back-channeling in free improvisation is not dependent on music-specific skills but is a general ability. The findings invite further study of the links between interpersonal dynamics in conversation and musical interaction.     

Are you approaching me? Motor execution influences perceived action orientation

Human observers are especially sensitive to the actions of conspecifics that match their own actions. This has been proposed to be critical for social interaction, providing the basis for empathy and joint action. However, the precise relation between observed and executed actions is still poorly understood. Do ongoing actions change the way observers perceive others' actions? To pursue this question, we exploited the bistability of depth-ambiguous point-light walkers, which can be perceived as facing towards the viewer or as facing away from the viewer. We demonstrate that point-light walkers are perceived more often as facing the viewer when the observer is walking on a treadmill compared to when the observer is performing an action that does not match the observed behavior (e.g., cycling). These findings suggest that motor processes influence the perceived orientation of observed actions: Acting observers tend to perceive similar actions by conspecifics as oriented towards themselves. We discuss these results in light of the possible mechanisms subtending action-induced modulation of perception.     

Further Explorations of the Facing Bias in Biological Motion Perception: Perspective Cues,Observer Sex,and Response Times

The human visual system has evolved to be highly sensitive to visual information about other persons and their movements as is illustrated by the effortless perception of point-light figures or ‘biological motion’. When presented orthographically, a point-light walker is interpreted in two anatomically plausible ways: As ‘facing the viewer’ or as ‘facing away’ from the viewer. However, human observers show a ‘facing bias’: They perceive such a point-light walker as facing towards them in about 70-80% of the cases. In studies exploring the role of social and biological relevance as a possible account for the facing bias, we found a ‘figure gender effect’: Male point-light figures elicit a stronger facing bias than female point-light figures. Moreover, we also found an ‘observer gender effect’: The ‘figure gender effect’ was stronger for male than for female observers. In the present study we presented to 11 males and 11 females point-light walkers of which, very subtly, the perspective information was manipulated by modifying the earlier reported ‘perspective technique’. Proportions of ‘facing the viewer’ responses and reaction times were recorded. Results show that human observers, even in the absence of local shape or size cues, easily pick up on perspective cues, confirming recent demonstrations of high visual sensitivity to cues on whether another person is potentially approaching. We also found a consistent difference in how male and female observers respond to stimulus variations (figure gender or perspective cues) that cause variations in the perceived in-depth orientation of a point-light walker. Thus, the ‘figure gender effect’ is possibly caused by changes in the relative locations and motions of the dots that the perceptual system tends to interpret as perspective cues. Third, reaction time measures confirmed the existence of the facing bias and recent research showing faster detection of approaching than receding biological motion.     

Recognizing biological motion and emotions from point-light displays in autism spectrum disorders

One of the main characteristics of Autism Spectrum Disorder (ASD) are problems with social interaction and communication. Here, we explored ASD-related alterations in 'reading' body language of other humans. Accuracy and reaction times were assessed from two observational tasks involving the recognition of 'biological motion' and 'emotions' from point-light displays (PLDs). Eye movements were recorded during the completion of the tests. Results indicated that typically developed-participants were more accurate than ASD-subjects in recognizing biological motion or emotions from PLDs. No accuracy differences were revealed on two control-tasks (involving the indication of color-changes in the moving point-lights). Group differences in reaction times existed on all tasks, but effect sizes were higher for the biological and emotion recognition tasks. Biological motion recognition abilities were related to a person's ability to recognize emotions from PLDs. However, ASD-related atypicalities in emotion recognition could not entirely be attributed to more basic deficits in biological motion recognition, suggesting an additional ASD-specific deficit in recognizing the emotional dimension of the point light displays. Eye movements were assessed during the completion of tasks and results indicated that ASD-participants generally produced more saccades and shorter fixation-durations compared to the control-group. However, especially for emotion recognition, these altered eye movements were associated with reductions in task-performance.     

Activation in posterior superior temporal sulcus parallels parameter inducing the percept of animacy

An essential, evolutionarily stable feature of brain function is the detection of animate entities, and one of the main cues to identify them is their movement. We developed a model of a simple interaction between two objects, in which an increase of the correlation between their movements varied the amount of interactivity and animacy observers attributed to them. Functional magnetic resonance imaging revealed that activation in the posterior superior temporal sulcus and gyrus (pSTS/pSTG) increased in relation to the degree of correlated motion between the two objects. This activation increase was not different when subjects performed an explicit or implicit task while observing these interacting objects. These data suggest that the pSTS and pSTG play a role in the automatic identification of animate entities, by responding directly to an objective movement characteristic inducing the percept of animacy, such as the amount of interactivity between two moving objects.     

Effect of Intentional Bias on Agency Attribution of Animated Motion: An Event-Related fMRI Study

Animated movements of simple geometric shapes can readily be interpreted as depicting social events in which animate agents are engaged in intentional activity. However, the brain regions associated with such intention have not been clearly elucidated. In this study, intentional bias was manipulated using shape and pattern animations while measuring associated brain activity using event-related functional magnetic resonance imaging (fMRI). Twenty-five higher-intention involved and twenty-five lower-intention involved animations were presented to participants. Behavioral results showed that the degree of agency attribution of the mental state increased as intentional involvement increased. fMRI results revealed that the posterior superior temporal sulcus (STS), inferior temporal gyrus (ITG), inferior frontal gyrus (IFG), premotor, temporal pole, supramarginal gyrus, and superior parietal lobule (SPL) were activated while participants viewed the high-intention animations. In contrast, occipital, lingual, and middle frontal gyri were activated while the participants viewed the low-intention animations. These findings suggest that as agent attribution increases, the visual brain changes its functional role to the intentional brain and becomes a flexible network for processing information about social interaction.     

Comparing biological motion perception in two distinct human societies

Cross cultural studies have played a pivotal role in elucidating the extent to which behavioral and mental characteristics depend on specific environmental influences. Surprisingly, little field research has been carried out on a fundamentally important perceptual ability, namely the perception of biological motion. In this report, we present details of studies carried out with the help of volunteers from the Mundurucu indigene, a group of people native to Amazonian territories in Brazil. We employed standard biological motion perception tasks inspired by over 30 years of laboratory research, in which observers attempt to decipher the walking direction of point-light (PL) humans and animals. Do our effortless skills at perceiving biological activity from PL animations, as revealed in laboratory settings, generalize to people who have never before seen representational depictions of human and animal activity? The results of our studies provide a clear answer to this important, previously unanswered question. Mundurucu observers readily perceived the coherent, global shape depicted in PL walkers, and experienced the classic inversion effects that are typically found when such stimuli are turned upside down. In addition, their performance was in accord with important recent findings in the literature, in the abundant ease with which they extracted direction information from local motion invariants alone. We conclude that the effortless, veridical perception of PL biological motion is a spontaneous and universal perceptual ability, occurring both inside and outside traditional laboratory environments.     

Perceiving the Direction of Articulatory Motion in Point-Light Actions

Human observers are able to perceive the motion direction of actions (either forward or backward) on the basis of the articulatory, relative motion of the limbs, even when the actions are shown under point-light conditions. However, most studies have focused on the action of walking. The primary purpose of the present study is to further investigate the perception of articulatory motion in different point-light actions (walking, crawling, hand walking, and rowing). On each trial, participants were presented with a forward or backward moving person and they had to decide on the direction of articulatory motion of the person. We analyzed sensitivity (d'') as well as response bias (c). In addition to the type of action, the diagnosticity of the available information was manipulated by varying the visibility of the body parts (full body, only upper limbs, or only lower limbs) and the viewpoint from which the action was seen (from frontal view to sagittal view). We observe that, depending on the specific action, perception of direction of motion is driven by different body parts. Implications for the possible existence of a life detector, i.e., an evolutionarily old and innate visual filter that is tuned to quickly and automatically detect the presence of a moving living organism and direct attention to it, are discussed.     

Rapid Perceptual Switching of a Reversible Biological Figure

Certain visual stimuli can give rise to contradictory perceptions. In this paper we examine the temporal dynamics of perceptual reversals experienced with biological motion, comparing these dynamics to those observed with other ambiguous structure from motion (SFM) stimuli. In our first experiment, naïve observers monitored perceptual alternations with an ambiguous rotating walker, a figure that randomly alternates between walking in clockwise (CW) and counter-clockwise (CCW) directions. While the number of reported reversals varied between observers, the observed dynamics (distribution of dominance durations, CW/CCW proportions) were comparable to those experienced with an ambiguous kinetic depth cylinder. In a second experiment, we compared reversal profiles with rotating and standard point-light walkers (i.e. non-rotating). Over multiple test repetitions, three out of four observers experienced consistently shorter mean percept durations with the rotating walker, suggesting that the added rotational component may speed up reversal rates with biomotion. For both stimuli, the drift in alternation rate across trial and across repetition was minimal. In our final experiment, we investigated whether reversals with the rotating walker and a non-biological object with similar global dimensions (rotating cuboid) occur at random phases of the rotation cycle. We found evidence that some observers experience peaks in the distribution of response locations that are relatively stable across sessions. Using control data, we discuss the role of eye movements in the development of these reversal patterns, and the related role of exogenous stimulus characteristics. In summary, we have demonstrated that the temporal dynamics of reversal with biological motion are similar to other forms of ambiguous SFM. We conclude that perceptual switching with biological motion is a robust bistable phenomenon.     

Lack of Visual Orienting to Biological Motion and Audiovisual Synchrony in 3-Year-Olds with Autism

It has been suggested that children with autism orient towards audiovisual synchrony (AVS) rather than biological motion and that the opposite pattern is to be expected in typical development. Here, we challenge this notion by showing that 3-year-old neurotypical children orient to AVS and to biological motion in point-light displays but that 3-year-old children with autism orient to neither of these types of information. Thus, our data suggest that two fundamental mechanisms are disrupted in young children with autism: one that supports orienting towards others’ movements and one that supports orienting towards multimodally specified events. These impairments may have consequences for socio-cognitive development and brain organization.     

Do dogs mind the dots? Investigating domestic dogs' (Canis familiaris) preferential looking at human-shaped point-light figures

It is generally assumed that dogs show increased attention towards humans. A major part of this includes attention towards visual cues such as bodily gestures. We tested empirically whether dogs are visually attentive towards human body movement. Based on methods from visual perception research in humans, we used point-light figures (PLFs) to investigate whether dogs attend to human body movement compared to other forms of motion. We investigated dogs' attentiveness towards vocalisation-paired PLFs by adopting a preferential looking paradigm. Results indicate that dogs show increased attention towards vocalisation-paired human-shaped PLFs in comparison with inverted and non-inverted scrambled configurations of the same PLFs. This increased attention, however, was only present in the case of PLFs that simulated a human in frontal orientation but not for PLFs in lateral orientation. We conclude that dogs prefer to look at PLFs of socially relevant (i.e. frontally facing) human body (i.e. natural) movement rather than scrambled (i.e. unnatural) displays. Our results indicate that PLFs may function as a promising tool to investigate dogs' visual perceptual preferences and mechanisms.     

¿I like the way you move¿: how hormonal changes across the menstrual cycle affect female perceptions of gait

ABSTRACT: BACKGROUND: Variations in hormone concentrations across the menstrual cycle affect human female mate preferences. It has been shown that around the time of ovulation human females prefer more masculine male voices, faces, and bodies while simultaneously preferring less faces that are more feminine. They prefer also displays of male dominance, males with more symmetrical faces, and the scent of males with high levels of body symmetry. The aim of the experiments reported here was to investigate whether there are changes in female preferences for walking gaits across the menstrual cycle. RESULTS: Experiment 1 showed female observers could discriminate between point-light walkers with low and high levels of fluctuating asymmetries in their gaits. Female observers were more sensitive to asymmetries in female gaits than they were for asymmetries in male gaits. Experiment 2 showed that level of gait asymmetry did not affect the abilities of observers to discriminate female from male walkers. Experiment 3 showed that female observers did not change their preference for low and high asymmetry walkers across their menstrual cycles. However, females showed a decreased preference for all female walkers at the time during which it was estimated observers were at peak fertility. That same change in preference was not observed for male walkers. CONCLUSIONS: These data suggest female observers may not value gait asymmetry, as a mate selection cue, in the same way that they value asymmetries in faces and bodies. While only "average" gaits were used in these experiments, rather than the gaits of individual walkers, the types of asymmetries in gait tested here were not used in the same way as static cues for judging the apparent healthiness of individuals. Females do discriminate well average female gait asymmetries and do change their preferences for those gaits across their menstrual cycle. Doing so may reflect the operation of processes that equip females with an advantage when competing for mates at times of peak fertility.