Parent-mediated intervention in infants with an elevated likelihood for autism reduces dwell time during a gaze-following task.

Cognitive markers may in theory be more sensitive to the effects of intervention than overt behavioral measures. The current study tests the impact of the Intervention with the British Autism Study of Infant Siblings-Video Interaction for Promoting Positive Parenting (iBASIS-VIPP) on an eye-tracking measure of social attention: dwell time to the referred object in a gaze following task. The original two-site, two-arm, assessor-blinded randomized controlled trial (RCT) of this intervention to increase parental awareness, and responsiveness to their infant, was run with infants who have an elevated familial likelihood for autism (EL). Fifty-four EL infants (28 iBASIS-VIPP intervention, 26 no intervention) were enrolled, and the intervention took place between 9 months (baseline) and 15 months (endpoint), with gaze following behavior measured at 15 months. Secondary intention to treat (ITT) analysis showed that the intervention was associated with significantly reduced dwell time to the referent of another person's gaze (ß = -0.32, SE = 0.14, p = 0.03) at 15-month treatment endpoint. Given the established link between gaze following and language, the results are considered in the context of a previously reported, non-significant and transient trend toward lower language scores at the treatment endpoint (Green et al. (2015) The Lancet Psychiatry, 2(2), 133-140). Future intervention trials should aim to include experimental cognitive measures, alongside behavioral measures, to investigate mechanisms associated with intervention effects.

The celebrity effect on gaze following in older and young adults.

BACKGROUND: In daily life, people often follow others' gaze direction to infer their attention and mental state. This phenomenon is known as gaze following. OBJECTIVE: This study aimed to explore whether gaze following in different age groups is influenced by celebrity identity. METHODS: We recruited 70 participants, including 35 older adults and 35 young adults. The experimental materials consisted of three faces with different identity information (a political leader, a movie star, and an ordinary person). Each face had left and right gaze conditions. Targets and cues were presented with both longer and shorter stimulus onset asynchrony (SOA) conditions. RESULTS: Both older adults and young adults exhibited similar gaze following behaviors. Importantly, the celebrity effect on gaze following was observed in both groups, with stronger effects induced by the leader's and star's gazes compared to the ordinary person's gaze. Older adults showed a larger facilitation effect under the longer SOA condition compared to the shorter SOA, while no such SOA-related facilitation effect was found for young adults. CONCLUSION: These findings suggest that older adults can integrate social information from others' faces (celebrity identity) into the process of gaze following as effectively as young adults.

Variation in gaze following across the life span: A process-level perspective.

Following eye gaze is fundamental for many social-cognitive abilities, for example, when judging what another agent can or cannot know. While the emergence of gaze following has been thoroughly studied on a group level, we know little about (a) the developmental trajectory beyond infancy and (b) the sources of individual differences. In Study 1, we examined gaze following across the lifespan (N = 478 3- to 19-year-olds from Leipzig, Germany; and N = 240 20- to 80-year-old international, remotely tested adults). We found a steep performance improvement during preschool years, in which children became more precise in locating the attentional focus of an agent. Precision levels then stayed comparably stable throughout adulthood with a minor decline toward old age. In Study 2, we formalized the process of gaze following in a computational cognitive model that allowed us to conceptualize individual differences in a psychologically meaningful way (N = 60 3- to 5-year-olds, 50 adults). According to our model, participants estimate pupil angles with varying levels of precision based on observing the pupil location within the agent's eyes. In Study 3, we empirically tested how gaze following relates to vector following in non-social settings and perspective-taking abilities (N = 102 4- to 5-year-olds). We found that gaze following is associated with both of these abilities but less so with other Theory of Mind tasks. This work illustrates how the combination of reliable measurement instruments and formal theoretical models allows us to explore the in(ter)dependence of core social-cognitive processes in greater detail. RESEARCH HIGHLIGHTS: Gaze following develops beyond infancy. The highest precision levels in localizing attentional foci are reached in young adulthood with a slight decrease towards old age. We present a computational model that describes gaze following as a process of estimating pupil angles and the corresponding gaze vectors. The model explains individual differences and recovers signature patterns in the data. To estimate the relation between gaze- and vector following, we designed a non-social vector following task. We found substantial correlations between gaze following and vector following, as well as Level 2 perspective-taking. Other Theory of Mind tasks did not correlate.

Individual differences in sociocognitive traits in semi-free-ranging rhesus monkeys (Macaca mulatta).

Characterizing individual differences in cognition is crucial for understanding the evolution of cognition as well as to test the biological consequences of different cognitive traits. Here, we harnessed the strengths of a uniquely large, naturally-living primate population at the Cayo Santiago Biological Field Station to characterized individual differences in rhesus monkey performance across two social cognitive tasks. A total of n = 204 semi-free-ranging adult rhesus monkeys participated in a data collection procedure, where we aimed to test individuals on both tasks at two time-points that were one year apart. In the socioemotional responses task, we assessed monkeys' attention to conspecific photographs with neutral versus negative emotional expressions. We found that monkeys showed overall declines in interest in conspecific photographs with age, but relative increases in attention to threat stimuli specifically, and further that these responses exhibited long-term stability across repeated testing. In the gaze following task we assessed monkeys' propensity to co-orient with an experimenter. Here, we found no evidence for age-related change in responses, and responses showed only limited repeatability over time. Finally, we found some evidence for common individual variation for performance across the tasks: monkeys that showed greater interest in conspecific photographs were more likely to follow a human's gaze. These results show how studies of comparative cognitive development and aging can provide insights into the evolution of cognition, and identify core primate social cognitive traits that may be related across and within individuals.

Visual attention patterns during a gaze following task in neurogenetic syndromes associated with unique profiles of autistic traits: Fragile X and Cornelia de Lange syndromes.

BACKGROUND: Gaze following difficulties are considered an early marker of autism, thought likely to cumulatively impact the development of social cognition, language and social skills. Subtle differences in gaze following abilities may contribute to the diverse range social and communicative autistic characteristics observed across people with genetic syndromes, such as Cornelia de Lange (CdLS) and fragile X (FXS) syndromes. AIMS: To compare profiles of 1) visual attention to the eye region at critical points of the attention direction process, 2) whether children follow the gaze cue to the object, and 3) participant looking time to the target object following the gaze cue between groups and conditions. MATERIALS AND METHODS: Children with CdLS (N = 11) and FXS (N = 8) and autistic (N = 22) and neurotypical (N = 15) children took part in a passive viewing paradigm adapted from Senju and Csibra (2008), in which videos of a central cue (ball/cartoon face/human face) directed attention towards one of two objects. Visual attention patterns were recorded via eye tracking technology. RESULTS: Neurotypical children were used as a reference group against which the autistic, CdLS and FXS groups were compared. Although autistic children looked at the eye region for significantly less time, they looked at the target object as frequently and for a similar duration as neurotypical children. Children with FXS looked at the target as frequently as neurotypical children but looked at it for comparatively less time. Both neurotypical children and children with CdLS frequently looked at the eye region, but children with CdLS were less likely to look at the target than neurotypical children. CONCLUSIONS: Findings provide preliminary evidence of unique patterns of visual attention and gaze following strategies in children with CdLS, children with FXS and autistic children. These unique gaze following patterns may underpin the distinct profiles of social and communication autistic traits observed between these groups.

The slow emergence of gaze- and point-following: A longitudinal study of infants from 4 to 12 months.

Acquisition of visual attention-following skills, notably gaze- and point-following, contributes to infants' ability to share attention with caregivers, which in turn contributes to social learning and communication. However, the development of gaze- and point-following in the first 18 months remains controversial, in part because of different testing protocols and standards. To address this, we longitudinally tested N = 43 low-risk, North American middle-class infants' tendency to follow gaze direction, pointing gestures, and gaze-and-point combinations. Infants were tested monthly from 4 to 12 months of age. To control motivational differences, infants were taught to expect contingent reward videos in the target locations. No-cue trials were included to estimate spontaneous target fixation rates. A comparison sample (N = 23) was tested at 9 and 12 months to estimate practice effects. Results showed gradual increases in both gaze- and point-following starting around 7 months, and modest month-to-month individual stability from 8 to 12 months. However, attention-following did not exceed chance levels until after 6 months. Infants rarely followed cues to locations behind them, even at 12 months. Infants followed combined gaze-and-point cues more than gaze alone, and followed points at intermediate levels (not reliably different from the other cues). The comparison group's results showed that practice effects did not explain the age-related increase in attention-following. The results corroborate and extend previous findings that North American middle-class infants' attention-following in controlled laboratory settings increases slowly and incrementally between 6 and 12 months of age. RESEARCH HIGHLIGHTS: A longitudinal experimental study documented the emergence and developmental trajectories of North American middle-class infants' visual attention-following skills, including gaze-following, point-following, and gaze-and-point-following. A new paradigm controlled for factors including motivation, attentiveness, and visual-search baserates. Motor development was ruled out as a predictor or limiter of the emergence of attention-following. Infants did not follow attention reliably until after 6 months, and following increased slowly from 7 to 12 months. Infants' individual trajectories showed modest month-to-month stability from 8 to 12 months of age.

The impact of maternal gaze responsiveness on infants' gaze following and later vocabulary development.

Research has shown that infants' language development is influenced by their gaze following-an ability linked to their cognitive and social development. Following social learning approaches, this pilot study explored whether variations in gaze following and later vocabulary scores relate to early mother-infant interactions by focusing on the role of mothers' gaze responsiveness in infants' attentional and language development. We recruited 15 mother-child pairs in Poland and assessed their engagement in joint attention episodes. Results indicate that mothers foster their infants' gaze-following ability by providing them with numerous opportunities to participate in the task. We also confirmed a correlation between infants' gaze-following ability at 6 months and their vocabulary scores at 24 months. However, combining both infants' gaze following and mothers' gaze monitoring as predictors in one model revealed that maternal gaze monitoring was a stronger predictor of infants' later vocabulary growth. Overall, this study emphasizes that mothers' gaze responsiveness is a crucial feature of scaffolding that impacts on infants' gaze following and language development.

Covert and overt automatic imitation are correlated.

Most theoretical accounts of imitation assume that covert and overt measures of automatic imitation tap into the same underlying construct. Despite this widespread assumption, it is not well supported by empirical evidence. In fact, the only study investigating the relation between covert and overt automatic imitation failed to find a correlation between them (Genschow et al., 2017, PLOS ONE, 12[9], Article e0183784). However, because overt and covert imitation were measured using two very different tasks, and because the measure of overt imitation was found to be unreliable, it is still not clear whether a correlation between both measures exists. Here, we address this question by reanalyzing the results of a previous virtual reality study in which automatic imitation was indexed with an overt and covert measure of gaze following, both obtained within one and the same task (Cracco et al., 2022, IScience, Article 104891). The results show that, in this situation, both types of imitation do correlate. As such, our results provide support for the idea that overt and covert measures of automatic imitation measure the same underlying construct.

Remote, tablet-based assessment of gaze following: a nationwide infant twin study.

Introduction: Much of our understanding of infant psychological development relies on an in-person, laboratory-based assessment. This limits research generalizability, scalability, and equity in access. One solution is the development of new, remotely deployed assessment tools that do not require real-time experimenter supervision. Methods: The current nationwide (Sweden) infant twin study assessed participants remotely via their caregiver's tablets (N = 104, ages 3 to 17 months). To anchor our findings in previous research, we used a gaze-following task where experimental and age effects are well established. Results: Closely mimicking results from conventional eye tracking, we found that a full head movement elicited more gaze following than isolated eye movements. Furthermore, predictably, we found that older infants followed gaze more frequently than younger infants. Finally, while we found no indication of genetic contributions to gaze-following accuracy, the latency to disengage from the gaze cue and orient toward a target was significantly more similar in monozygotic twins than in dizygotic twins, an indicative of heritability. Discussion: Together, these results highlight the potential of remote assessment of infants' psychological development, which can improve generalizability, inclusion, and scalability in developmental research.

Individual differences in gaze-cuing effect are associated with facial emotion recognition and social conformity.

Spontaneous gaze following and the concomitant joint attention enable us to share representations of the world with others, which forms a foundation of a broad range of social cognitive processes. Although this form of social orienting has long been suggested as a critical starting point for the development of social and communicative behavior, there is limited evidence directly linking it to higher-level social cognitive processes among healthy adults. Here, using a gaze-cuing paradigm, we examined whether individual differences in gaze following tendency predict higher-order social cognition and behavior among healthy adults. We found that individuals who showed greater gaze-cuing effect performed better in recognizing others' emotion and had greater tendency to conform with group opinion. These findings provide empirical evidence supporting the fundamental role of low-level socio-attentional processes in human sociality.

Variability in infant social responsiveness: Age and situational differences in attention-following.

Attention following (AF) is a cornerstone of social cognitive development and a longstanding topic of infancy research. However, there is conflicting evidence regarding the development of AF. One reason for discrepant findings could be that infants' AF responses do not generalize across settings, and are influenced by situational factors. Theories of AF development based on data collected in laboratory paradigms might skew our understanding of infants' everyday AF. To reveal more generalizable patterns of infant AF development, we compared healthy, North American infants' (N = 48) AF developmental trajectories between a controlled laboratory paradigm and a naturalistic, home-based, parent-directed paradigm. Longitudinal micro-behavioral coding was analyzed to compare individual infants' AF between the two settings every month from 6 to 9 months of age. We aimed to (1) examine longitudinal development of infant AF in two settings; (2) compare AF development between settings, and (3) explore differences in adult cueing behaviors that influence AF. We found that longitudinal trajectories of AF differed between home and lab, with more AF at home in earlier months. Additionally, AF at home was related to maternal cueing variables including bid duration and frequency. These results have implications for the assessment of infants' developing social attention behaviors.

Inferential eye movement control while following dynamic gaze.

Attending to other people's gaze is evolutionary important to make inferences about intentions and actions. Gaze influences covert attention and triggers eye movements. However, we know little about how the brain controls the fine-grain dynamics of eye movements during gaze following. Observers followed people's gaze shifts in videos during search and we related the observer eye movement dynamics to the time course of gazer head movements extracted by a deep neural network. We show that the observers' brains use information in the visual periphery to execute predictive saccades that anticipate the information in the gazer's head direction by 190-350ms. The brain simultaneously monitors moment-to-moment changes in the gazer's head velocity to dynamically alter eye movements and re-fixate the gazer (reverse saccades) when the head accelerates before the initiation of the first forward gaze-following saccade. Using saccade-contingent manipulations of the videos, we experimentally show that the reverse saccades are planned concurrently with the first forward gaze-following saccade and have a functional role in reducing subsequent errors fixating on the gaze goal. Together, our findings characterize the inferential and functional nature of social attention's fine-grain eye movement dynamics.

Can the robot "see" what I see? Robot gaze drives attention depending on mental state attribution.

Mentalizing, where humans infer the mental states of others, facilitates understanding and interaction in social situations. Humans also tend to adopt mentalizing strategies when interacting with robotic agents. There is an ongoing debate about how inferred mental states affect gaze following, a key component of joint attention. Although the gaze from a robot induces gaze following, the impact of mental state attribution on robotic gaze following remains unclear. To address this question, we asked forty-nine young adults to perform a gaze cueing task during which mental state attribution was manipulated as follows. Participants sat facing a robot that turned its head to the screen at its left or right. Their task was to respond to targets that appeared either at the screen the robot gazed at or at the other screen. At the baseline, the robot was positioned so that participants would perceive it as being able to see the screens. We expected faster response times to targets at the screen the robot gazed at than targets at the non-gazed screen (i.e., gaze cueing effect). In the experimental condition, the robot's line of sight was occluded by a physical barrier such that participants would perceive it as unable to see the screens. Our results revealed gaze cueing effects in both conditions although the effect was reduced in the occluded condition compared to the baseline. These results add to the expanding fields of social cognition and human-robot interaction by suggesting that mentalizing has an impact on robotic gaze following.

Gaze Following as an Early Diagnostic Marker of Autism in a New Word Learning Task in Toddlers.

The aim was to test the use of eye-tracking methodology for the early detection of ASD in a task of association between unfamiliar objects and pseudowords. Significant differences were found between ASD (n = 57) and TD (n = 57) Spanish speaking toddlers in the number and time of fixation. The TD children showed more and longer fixations on eyes and mouth while the ASD children attended almost exclusively to objects, making it difficult to integrate lexical and phonological information. Moreover, the TD toddlers looked at the mouth when the pseudoword was produced while the ASD toddlers did not. Gaze fixation on eyes and mouth during word learning recorded by eye-tracking may be used as a biomarker for the early diagnosis of ASD.

Interpersonal matching of autistic trait levels in typically developed individuals is associated with spontaneous gaze following and initiation during face-to-face social interaction.

OBJECTIVES: People with autism spectrum disorders (ASD) usually exhibit typical behaviours and thoughts that are called autistic traits. Autistic traits are widely and continuously distributed among typically developed (TD) and ASD populations. Previous studies have found that people with ASD have difficulty in following the eye gaze of social peers. However, it remains unknown whether TD adults with high or low autistic traits also differ in spontaneous gaze following and initiation in face-to-face social interactions. To fill this gap, this study used a novel and naturalistic gaze-cueing paradigm to examine this research question. DESIGN: A 4 (group: high-high, high-low, low-high or low-low autistic traits) × 3 (congruency: congruent, neutral, or incongruent) mixed-measures design was used. METHODS: Typically developed adults who were high or low in autistic traits completed a visual search task while a confederate who was high or low in autistic traits sat facing them. Critically, the match of autistic traits within a participant-confederate pair was manipulated. The confederate gazed at (congruent) or away from (incongruent) the location of the target prior to the appearance of the target. Participants were not explicitly instructed to follow the confederate's gaze. RESULTS: Autistic traits were associated with spontaneous gaze following and initiation in face-to-face social interactions. Specifically, only when both the participant and confederate were low in autistic traits did the incongruent gaze cues of confederates interfere with the participants' responses. CONCLUSIONS: Autistic traits impeded gaze following and initiation by TD adults. This study has theoretical and practical implications regarding autistic trait-induced social deficits and indicates a new approach for social skill interventions.

Causal manipulation of gaze-following in the macaque temporal cortex.

Gaze-following, the ability to shift one's own attention to places or objects others are looking at, is essential for social interactions. Single unit recordings from the monkey cortex and neuroimaging work on the human and monkey brain suggest that a distinct region in the temporal cortex, the gaze-following patch (GFP), underpins this ability. Since previous studies of the GFP have relied on correlational techniques, it remains unclear whether gaze-following related activity in the GFP indicates a causal role rather than being just a reverberation of behaviorally relevant information produced elsewhere. To answer this question, we applied focal electrical and pharmacological perturbation to the GFP. Both approaches, when applied to the GFP, disrupted gaze-following if the monkeys had been instructed to follow gaze, along with the ability to suppress it if vetoed by the context. Hence the GFP is necessary for gaze-following as well as its cognitive control.

Atypical gaze-following behaviour in infants with congenital heart disease.

BACKGROUND: Neurodevelopmental impairments are the most prevalent non-cardiac long-term sequelae in children with complex congenital heart disease (CHD). Deficits include the social-emotional and social-cognitive domains. Little is known about the predecessors of social-cognitive development in infants with CHD during the first year of life. Gaze-following behaviour can be used to measure early social-cognitive abilities. AIMS: To assess gaze-following development in infants with CHD compared to healthy controls. STUDY DESIGN: Prospective cohort study. PARTICIPANTS: Twenty-three infants who underwent neonatal correction for CHD and 84 healthy controls. OUTCOME MEASURES: Gaze-following behaviour was assessed by eye tracking at 6 and 12 months. Difference scores for first fixation, fixation frequency and fixation duration towards the gaze-cued object were calculated across 6 trials and compared between groups at both testing time points while adjusting for known confounders. Linear mixed models were calculated to assess the longitudinal trajectory of gaze-following development while accounting for the nested and dependent data structure. RESULTS: At 6 months, no difference in gaze-following behaviour between CHD and healthy controls was found. At 12 months, fixation frequency towards the gaze-cued was lower and looking duration was shorter in CHD compared to controls (p = 0.0077; p = 0.0068). Infants with CHD showed less increase with age in the fixation frequency towards the congruent object (p = 0.041) compared to controls. CONCLUSION: During the first year of life, gaze-following development diverges in infants with CHD compared to healthy controls. Further research is needed to investigate the clinical relevance of these findings and the association with later social-cognitive development.

A frontoparietal network for volitional control of gaze following.

Gaze following is a major element of non-verbal communication and important for successful social interactions. Human gaze following is a fast and almost reflex-like behaviour, yet it can be volitionally controlled and suppressed to some extent if inappropriate or unnecessary, given the social context. In order to identify the neural basis of the cognitive control of gaze following, we carried out an event-related fMRI experiment, in which human subjects' eye movements were tracked while they were exposed to gaze cues in two distinct contexts: A baseline gaze following condition in which subjects were instructed to use gaze cues to shift their attention to a gazed-at spatial target and a control condition in which the subjects were required to ignore the gaze cue and instead to shift their attention to a distinct spatial target to be selected based on a colour mapping rule, requiring the suppression of gaze following. We could identify a suppression-related blood-oxygen-level-dependent (BOLD) response in a frontoparietal network comprising dorsolateral prefrontal cortex (dlPFC), orbitofrontal cortex (OFC), the anterior insula, precuneus, and posterior parietal cortex (PPC). These findings suggest that overexcitation of frontoparietal circuits in turn suppressing the gaze following patch might be a potential cause of gaze following deficits in clinical populations.

Social Isolation Affects the Mimicry Response in the Use of Smartphones : An Ethological Experiment during the COVID-19 Pandemic.

Humans are social animals that rely on different ways to interact with each other. The COVID-19 pandemic strongly changed our communication strategies. Because of the importance of direct contact for our species, we predict that immediately after the forced social isolation, people were more prone to engage in direct rather than in virtual interactions, thus showing a lower mimicry response in the use of smartphones. In a non-longitudinal study, we collected behavioral data under naturalistic contexts and directly compared the data of the mimicry response gathered immediately following the Italian lockdown (May-September 2020) with those gathered one year later (May-October 2021). Contrary to our expectations, the mimicry response in the use of smartphones was higher immediately after the lockdown than a year later. Probably the large use of these devices during the lockdown translated into a greater sensitivity to be affected by others' smartphone manipulation. Indeed, social isolation modified, at least in the short term, the ways we interact with others by making us more prone to engage in "virtual" social interactions. The bright side of the coin unveiled by our findings is that the effect seems to diminish over time. The large behavioral dataset analyzed here (1,608 events; 248 people) also revealed that the mimicry response in the use of smartphones was higher between familiar subjects than between strangers. In this view, mimicry in manipulating smartphones can be considered an example of joint action that fosters behavioral synchrony between individuals that, in the long-term, can translate into the formation of social bonding.