Moreover, Gernsbacher et al. Much social synchronization research has been concerned with coding of whether general activity or certain behavioral contents are synchronized i. Condon was one of the early researchers to code for the timing of general activity and he proposed that synchronized bodily coordination was disturbed in social pathologies generally and in particular in children with ASD Condon, Furthermore, Oberman et al.
A breakdown of the temporal synchronization of specific kinds of speech behaviors have also been reported in adolescents with ASD. For example, Feldstein et al. The research reviewed above relies largely on a behavioral coding of specific gestures content to evaluate social synchronization.
Such behavioral coding methods rely on identifying discrete segments of behavior and analyzing the sequencing or timing between them but are time consuming to perform and rely on highly skilled coders. Moreover, such behavioral coding is not particularly well-suited for understanding the full temporal patterning of social synchronization in that it is discrete and not fine-grained enough to capture the complex, time-dependent dynamic organization of interpersonal synchrony.
A coordination dynamics approach to behavior Kelso, provides a framework for the development of such a research methodology. This approach involves recording continuous time-varying process measures of behavior as they unfold and then analyzes the dynamical structure of behavior using time-series analysis techniques. These techniques allow for a more discerning measurement of behavioral coordination by evaluating the synchronization patterning and strength of system components as they change over time Haken et al.
The temporal resolution of this approach allows for the capture of subtle dimensions of coordination that are typically missed by gross outcome measures. The ability to index subtle changes in the patterning and stability of coordination will allow us to determine whether such differences are related to the variations in social competence that are observed in adolescents with ASD.
This coordination dynamics approach has been used to model social coordination Schmidt and Richardson, ; Schmidt et al. For example, both intentional coordination directed by an explicit social goal of the people interacting as well as spontaneous coordination outside of the awareness of the two people interacting of the movements of two people interacting have been modeled using a coupled oscillator dynamic for both simple laboratory tasks Schmidt et al. In the dynamical modeling of this interpersonal synchronization, individual limbs of the two people are treated as embodying oscillators that are linked via perceptual coupling Richardson et al.
A task that has been used to study the both intentional and spontaneous interpersonal coordination is a methodology in which two people coordinate handheld pendulums swung from the wrist joint in the sagittal plane using radial-ulnar abduction—adduction.
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This methodology has demonstrated that the strength of interpersonal synchronization is dependent upon many different physical as well as psychological variables see Schmidt and Richardson, for a review and can be understood in terms of a dynamical model of synchronization. A synchronization dynamic model Varlet et al. This model predicts that even if the two pendulums have different inherent eigenfrequencies which can be induced by manipulating the length or mass of the pendulum and two people are asked to coordinate the movements of two pendulums, they are able to do so and achieve a common tempo.
However, the person swinging the pendulum that prefers to move more slowly e. Using such a dynamical model to understand how synchrony breaks down in social deficits has the distinct advantage of allowing one to infer which dynamical components of the model are underlying the impairment. Varlet et al. However, they did not find any disruptions in spontaneous interpersonal coordination. These findings suggest that individuals with schizophrenia may not be attending to others or may be delayed in their responses during social interactions when they are interacting with them under an explicit social goal to coordinate.
Del-Monte et al. Namely, the first-degree relative pairs also demonstrated larger phase lag and greater variability but only for the intentional rhythmic coordination of pendulums. Relatedly, to demonstrate the feasibility of using dynamical measures of social synchronization to investigate the social deficit in those with ASD, Fitzpatrick et al. They also utilized traditional cognitive measures of social competence joint attention, theory of mind, intentionality, and cooperation and several social motor measures including imitation, synchronization and an interpersonal hand-clapping game.
Findings yielded significant relationships between social cognitive and social synchrony measures and a principal components analysis revealed three different factors social attention, social knowledge, and social action as important for characterizing embodied social competence. These findings suggested that social competence is a complex construct and identified social synchrony as a potentially important pathway for understanding the social problems of children with ASD.
Taken together, the research discussed above suggests that social synchronization is a potentially important pathway for understanding the social problems characteristic of people with social deficits. The current study extends the previous work by employing a pendulum coordination task to examine the content and timing of social motor synchronization of adolescents with ASD.
The aim of this study is to determine whether adolescents with ASD exhibit an interpersonal synchrony deficit and whether this can be used to differentiate adolescents with and without ASD. In particular, we are evaluating a whether disruptions are evident in both intentional and spontaneous coordination; and b which components of the coupled oscillator dynamic are impaired e. An impairment in coupling strength would reveal difficulty in attending to social cues, an impairment in information transmission would suggest problems with detecting and processing the information in time for an appropriate response, and disruptions in both would indicate problems with both attending to social cues as well as processing the information.
The use of a social motor synchronization task allows for a precise, objective, and dynamical measure of synchronization and a more nuanced exploration of the temporal nature of synchronization. In addition, the direct dynamical modeling available using the pendulum paradigm will allow us to explore whether a social synchronization deficit is general or specific to a disorder i. A total of 18 adolescents paired with one of their parents participated in this study.
There were nine adolescents with a diagnosis of ASD eight males, one female, average age There was one adolescent with ASD who was left-handed; all other participants in both groups were right-handed. The ADOS-2 is a semi-structured, standardized assessment of communication, social interaction, and play for individuals referred because of a question of a possible diagnosis of autism. Control participants also completed the ADOS Five participants were administered Module 3 whereas 13 were administered Module 4 based on their developmental and language level.
All parents of participants gave informed, written consent for their children to take part in the study, and adolescents also provided assent to participate. Participants were recruited from local communities through print advertising, a recruitment brochure, email, social media, and community events. Recruitment material was posted on various community and University of Massachusetts Medical School websites. Each chair had a forearm support attached to the inside of the chair parallel to the ground. Adolescents swung the pendulums with their dominant hand and parents swung the pendulums with the non-dominant hand.
Experimental set-up for the spontaneous and intentional pendulum task. Participants sat on chairs side-by-side while oscillating pendulums. A sensor was attached to the end of each pendulum to record the angular displacement of the pendulum. The time series of participants were low-pass filtered using a 10 Hz Butterworth filter. Two handheld pendulums, each composed of a wooden dowel that was 54 cm in length and had a g weight attached at either the bottom or the middle of the pendulum, were used.
The placement of the weight manipulated the inertial loading of the pendulum, and hence, the preferred frequency of oscillation. The pairing of the two pendulums resulted in three pendulum combination conditions for participant pairs that reflect differential inertial loadings of the pendulums and differential preferred frequencies of oscillation: 0 no inertial difference between pendulum conditions, both adolescent and parent have pendulum weighted at bottom, no preferred frequency of oscillation difference ; 1 [parent had pendulum with higher inertial loading mass at bottom and adolescent had pendulum with lower inertial loading mass at middle , adolescent had higher preferred frequency of oscillation and should lead the coordination]; and -1 [adolescent had pendulum with higher inertial loading mass at bottom and parent had pendulum with lower inertial loading mass at middle , parent had higher preferred frequency of oscillation and should lead the coordination].
Two different synchronization tasks were performed, spontaneous synchrony and intentional synchrony. Trials, including the not looking control segments and looking spontaneous coordination segments, were completed for each of the three pendulum combination conditions. Two replications per pendulum condition were completed for a total of six spontaneous synchrony trials.
Trials were 60 s, with two replications for each pendulum combination condition, for both in-phase and anti-phase coordination resulting in a total of 12 intentional coordination trials 6 in-phase, 6 anti-phase. Relative phase is an angle that measures where one rhythm is in its cycle i. A continuous relative phase time series was computed from the two angular positions of pendulums using the Hilbert transform Pikovsky et al. The degree of synchronization was evaluated by a measure of relative phase variability. This measure yields an index of synchronization between 0 and 1 with 1 reflecting a perfect synchronization and 0 reflecting an absence of synchronization.
The circular variance represents the proportion of relative phases relationships visited by the two time series. A circular variance of 0 means that the two time series never visited the same relative phase relationship more than once. Higher values of circular variance indicate that the two time series repeatedly visited a set of relative phase relationships throughout the trial. To evaluate the synchronization that occurred in both intentional in-phase and anti-phase synchronization tasks, two dependent measures were calculated from the relative phase time series.
First, circular variance was calculated to measure the overall degree of synchronization. As mentioned above, a circular variance of 0 indicates no synchronization and a circular variance of 1 indicates perfect synchronization. Participants completed two separate experimental sessions, approximately 1 week apart. Additional clinical phenotyping measures were administered as part of a larger study during this session but are not reported here.
In the second visit, the social synchronization tasks were completed. All participant pairs completed the spontaneous synchrony trials at the start of the experimental session to prevent experimental task demands from influencing performance. The order of presentation of the in-phase and anti-phase intentional synchrony trials was counterbalanced across participants—half of the participant pairs completed in-phase trials followed by anti-phase trials and half completed anti-phase trials followed by in-phase trials. Two additional experimental tasks were also completed as part of a larger study but they are not being reported here.
To summarize the design of the experiment, diagnosis group ASD, neurotypical control was a between-subject variable. Group differences in clinical phenotyping were evaluated with independent samples t -tests. In the spontaneous social synchrony task, diagnosis group was a between-subject variable, and pendulum combination condition [-1 adolescent with higher loading, parent should lead , 0 no differential loading , 1 parent with higher loading, child should lead ], and looking condition 1st 30 s, not looking; 2nd 30 s looking; 3rd 30 s not looking were within-subject variables.
Bonferroni post hoc tests were used as necessary to determine the nature of the effects. IQ was not a significant factor in any of the analyses, nor did IQ occur as a variable in any significant interactions. Therefore, results are reported below without IQ as a covariate. These results indicate that both groups had higher spontaneous entrainment when the pendulums were the same rather than different, that both the groups demonstrated spontaneous entrainment during the looking condition as evidenced by higher circular variance and that ASD pairs had less spontaneous entrainment than the control pairs across all trial segments.
Neither the interaction between pendulum combination and diagnosis nor the three-way interaction were significant. Circular variance for spontaneous coordination conditions. For the intentional synchrony trials, an ANOVA on circular variance of relative phase verified several dynamical model predictions that have been observed before in a number of studies see Schmidt and Richardson, for a review. Importantly, across all conditions, a main effect of diagnosis group revealed that ASD pairs had less stable entrainment than control pairs [0.
Intentional coordination phase entrainment as indexed by circular variance of relative phase supports the dynamical model predictions. Namely, entrainment is lower for anti-phase B than in-phase A and entrainment is higher for similar pendulum combinations than different combinations. Importantly, the ASD pairs had lower overall entrainment than the control pairs in all conditions. Note: Convention comparable with Varlet et al. The positive sign of the phase shift values indicate that across both groups the adolescent always led the parent and, there was a trend toward the adolescent with ASD to lead by more [ Phase shift supports the dynamical model predictions for intentional coordination.
The adolescent led less when the parent had the larger pendulum and led the most when they had the larger pendulum. This was true for both groups and was evident for both in-phase A and anti-phase B coordination. The phase shift was greater overall for the group with ASD than the controls and the difference between groups was more pronounced for anti-phase than in-phase.
To verify this conclusion, a regression analysis was conducted with subject pair mean phase shift values as the dependent variable and actual eigenfrequency differences frequency detuning value as determined from the unintentional non-looking segments as the independent variable. The significant slopes in these analyses indicate the model predicted change in phase shift with the eigenfrequency differences of the pendulum pairs whereas the significant intercepts indicate that for both groups the child led the parent in the coordination.
This slope difference verifies a steeper linear increase in the phase shift with pendulum combination for the ASD group, indicative of weaker coupling. The lack of difference between the intercepts indicates that overall the ASD group did not lead the parent more: there was not an overall phase advance by the ASD group, which would translate into an overall tendency to anticipate.
Phase shift regressions indicate weaker coupling for autism pairs. A regression with relative phase angle phase shit as the dependent variable and calculated delta omega as the independent variable revealed that for both the pairs with autism A and controls B with autism and controls the slope and intercept were significantly different from 0. The intercepts were not significantly different between groups but the slopes were. The pairs with autism have a steeper slope, indicative of weaker interpersonal coupling.
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The findings reported here indicate that adolescents with ASD demonstrated a disruption of both spontaneous synchronization and intentional synchronization. Analysis of circular variance of relative phase confirmed spontaneous social entrainment occurred in both groups, corroborating past research on the ubiquity of spontaneous entrainment.
For intentional social coordination, the circular variance of relative phase confirmed a number of dynamical model predictions. Namely, for both groups, anti-phase synchronization was weaker than in-phase synchronization and coordinating different pendulums was less stable than coordinating similar pendulums. Importantly though, these analyses also indicate that intentional social synchronization was weaker for the ASD pairs.
Thus, our findings on the degree of synchronization using circular variance indicate that ASD participants synchronized less well under conditions in which synchronization occurs spontaneously in the presence of perceptual information of the social partner and in situations when there is an explicit social goal to coordinate with another person e. Evaluation of the pattern of synchronization using the phase shift for the intentional task replicated past findings of frequency detuning in which there was greater lagging for the person with the larger pendulum.
In terms of the dynamical model in Eq. Such a weakness in dynamical entrainment corresponds to a lower sensitivity and attention to the movements of the other person. Kinsbourne and Helt have suggested that interpersonal synchrony problems in ASD may be due to a lack of social attention and these findings are consistent with such a claim. Similarly, Bebko et al. This interpretation is reinforced by Koehne et al. Those participants were told that the movements of the dot were either controlled by a human or a computer, but no social information was present during the task.
Participants were not required to use social attention or perception and their synchronization ability was not impaired. Additional research is needed to carefully evaluate the role of animacy on synchronization ability by systematically varying the level of task sociality. These findings would indicate that the synchronization problems of adolescents with ASD was due to problems with attention or perception but not with the timing of information transmission. One could also argue that the synchronization difficulties evident in ASD may be the result of motor control problems, which are also common in ASD Ghaziuddin and Butler, ; Pan et al.
A number of researchers suggest that motor problems may contribute to the social difficulties of those with ASD Gernsbacher et al. Disentangling the roles that motor control and social attention and perception play in synchronization is needed in future research. The finding that the majority of children led the parent in synchronization, in both groups, is somewhat surprising.
One might have expected adolescents with ASD to be less likely to lead in the coordination. In fact, Warlaumont et al. Similarly, Varlet et al. This specific pattern of disruptions in synchronization ability may be unique to ASD. Whereas participants with schizophrenia have been found to have a social synchrony deficit during intentional synchronization but not spontaneous synchronization Varlet et al. It appears that in individuals with schizophrenia synchronization is disrupted only when there is an explicit social goal, while in ASD the reduction in coupling strength is evident both when there is an explicit social goal to coordinate and when there is no explicit social goal to coordinate.
Furthermore, during intentional coordination participants with schizophrenia not only had a weaker coupling strength but also demonstrated a delay in information transmission Varlet et al. In contrast, the participants with ASD did not have a deficit in the rate of information transfer. These findings suggest that social synchronization deficit evident in ASD is different from schizophrenia and may be different from other disorders characterized by problems with social interactions.
Consequently, social synchronization may prove to be a bio-behavioral marker of the social deficits in ASD. In addition, the dissociation of deficits in intentional and spontaneous social synchronization suggests that these kinds of entrainment may function independently and have distinct underlying mechanisms. One might argue that these differences could be due to the fact that the participants with schizophrenia were adults and the participants with ASD were adolescents.
This seems unlikely, however, because the data from the adolescent controls replicated the dynamical model predictions that have been extensively demonstrated with adult participants.
Another important difference between schizophrenia and ASD is that schizophrenia typically has an onset in early adulthood while the onset of ASD is much earlier and could account for the disruptions in spontaneous synchronization evident in ASD but not schizophrenia. Caution, therefore, is warranted in drawing firm conclusions until future research has explored these differences with larger sample sizes, conducted studies to directly compare diagnostic groups, and compared adult and adolescent populations to isolate any developmental differences.
Our results demonstrating that social synchronization successfully differentiates adolescents with and without ASD is consistent with other work using dynamical measures of synchronization that has found similar differences in social synchronization abilities in children with ASD ages 6—10 years old; Fitzpatrick et al. These findings are also consistent with behavioral-coding work indicating disruptions in synchronization of parent—child interactions Condon, ; Trevarthen and Daniel, ; Feldman, , timing of facial mimicry Oberman et al. The confirmation of social synchronization differences in an older population using a task that allowed direct dynamical modeling, combined with the finding that the synchronization deficit in ASD is different from the deficit seen in schizophrenia, raises the important possibility that social synchronization could be a bio-behavioral marker for ASD.
This research also points to the importance of using objective, dynamical, process-oriented measures of social synchronization to be able to fully evaluate the temporal nature of social synchronization. Our research focused on synchronization in the context of a social motor task. Future research is planned to use this dynamical methodology to explore social synchronization in more naturalistic tasks such as the coordination of whole body movements and speech during conversation tasks.
Cross recurrence analysis provides another potentially fruitful dynamical methodology for analyzing the temporal and directional characteristics of interpersonal exchanges e. Cross recurrence analysis has demonstrated, for example, that mother—infant gaze patterns become more tightly coupled developmentally Nomikou et al. Questions remain, however, about whether synchronization differences are due to underlying mechanisms that are social, motor, or due to attention or perceptual processing disruptions.
One potential limitation of this research is that the participants were performing the task with their parent. While this was chosen to reduce the anxiety that would be inherent in doing the task with a stranger, it may have contributed to the finding that, in both groups the adolescents always led the parent in the coordination. It is possible that there could be something distinct about the interactions between parent and adolescent that would not generalize to interactions of other social pairs.
In addition, due to the heritability of ASD e. Alternatively, it is possible that parents of children with ASD over-compensate and adjust their behavior more to match their child. If that were the case, it would suggest the synchronization ability of the adolescents might be overestimated here. Green et al. This means that factors of the interaction are by its very nature uncontrolled. This could be circumvented in future research by using video-based presentation of the partner as this would not only allow for the standardization of the movements of the partner used to elicit social behavior, but also for the manipulation of the reciprocity of coupling between the partner and adolescent and the simultaneous recording of the movements of both.
This sort of precision in presentation and manipulation of social movements and simultaneous measurement of the user interaction as it unfolds will help clarify the unique contribution of each partner to initiating and maintaining the social synchronization. Furthermore, the relatively small number of participant pairs used suggests that replication would be prudent before large-scale conclusions can be drawn about the specific pattern of results being a bio-behavioral marker unique to ASD.
Nonetheless, studies including large samples of both ASD and schizophrenia dyads should be performed to definitely conclude that the social synchronization deficits are different for these two groups. An inherent challenge in delineating the precise nature of ASD-specific social deficits lies in the fact that the population of individuals with ASD is phenotypically and behaviorally heterogeneous. The participants in our sample were relatively high-functioning. In future work we plan to investigate the heterogeneity in adolescents with ASD by recruiting a more diverse participant population and measuring behavior across multiple domains motor, social, cognitive, emotional, neural and conducting a discriminant analysis to estimate the contribution each of these components makes to the synchronization difficulties both on the group and individual level.
This will allow us to better understand the heterogeneity in ASD and how it relates to synchronization ability.
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To help identify the mechanisms underlying intentional and spontaneous synchronization, additional research is planned using electroencephalogram EEG and functional magnetic resonance imaging fMRI to map brain activity during social synchronization to determine how neurophysiological activity in individuals with ASD is different from that of controls. Researchers are beginning to investigate the underlying neural activity involved in social synchronization Kelso et al.
It means that older RS patients looked shorter time at social stimuli human faces and longer time at non-social stimuli clock. Even when the oldest RS patient 30 years old, who in fact looked at target areas much shorter than the others RS participants , was not considered in this analysis, correlations continued strongly negative. On the other hand, such correlations in ASD group were not significant at all, even considering a moderate positive correlation regarding picture 2, which would mean that older ASD patients looked longer at a happy woman face but not at children faces.
Finally, positive correlations were significant in TD group regarding all three social stimuli, without any correlation regarding non-social stimuli clock ; that is, older typically developing children looked at target areas longer than younger ones. This is the first study to compare eye tracking of social human faces and non-social clock stimuli in RS and ASD patients, and differences in the pattern of visual fixation at such stimuli were significantly evidenced. Eye tracking technologies allowing the quantification of eye gaze have been used more and more since the beginning of this century.
The first publication on their use aimed to determine visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism Since then some aspects of eye tracking have been used as outcome measures in studies on ASD 15 , 16 , 17 , and many centers have been using them clinically for diagnostic assessment or even therapeutic interventions in individuals with ASD. Few years later, Baptista et al.
In , Velloso et al. These authors discussed some limitations of that pilot study, such as the short time of exposure to the stimuli 4 seconds and the way the concepts was teach to those children. Recently, the study was replied with longer exposure time 8 seconds and with a more systematic but not yet adequate way to teach these basic concepts to RS girls, and the results were the very same A little later, Vignoli et al.
Their preliminary findings indicated that epilepsy characteristics and EEG patterns suggestive of epileptic encephalopathy should be considered prognostic factors in neuropsychological outcome of RS patients, especially concerning the input phase attention of information processing. On the other hand, they did not find a close relationship between cognitive impairment and the use of a specific antiepileptic drug. Recently, researchers of the Montefiori Medical Center 21 , 22 , 23 used eye tracking technology in RS patients to assess their social preferences, to determine their basic features of nonverbal cognitive processes, such as characteristics of their visual fixation pattern meaningful x random and visual attention in response to novelty , and to examine attention and recognition memory for faces and patterns.
In the first study, RS girls demonstrated a tendency towards socially weighted stimuli social preferences , and looked longer at eyes compared to mouth and nose. The following study reported that RETT girls demonstrated a preference for novel and salient stimuli in a way that normally developing children do. In the last study, the authors combined eye tracking technology with a visual paired-comparison VPC paradigm and found out that patients with RS could recognize faces and patterns, although their recognition was poorer than that of age-matched participants.
Now we can add to such objective and systematic findings that patients with RS are undoubtedly more socially engaged than those with ASD and even than younger TD children, although such social engagement tends to decrease with age in RS and, as expected, to increase in young TD children.
This negative correlation between age and social engagement in patients with RS is not difficult to understand when we consider all the physiological suffering affecting them along the life since the first manifestations of the disease, especially the breathing irregularities, low O 2 saturation, seizures, very frequent gastrointestinal and orthopedic problems.
Other point is that their neuromotor condition apraxia, inability to use hands, manual stereotypies etc. At last, a number of families tend to reduce more consistent interactions with and for their daughters when they get the adulthood, since parents get older, sometimes sick, and sometimes even die. So the maintenance of their social engagement depends on a lot of conditions, differently from patients with ASD who show no social interests independently of their ages.
It was already observed that epileptic characteristics can be associated with poorer attention in patients with RS New studies are needed now to understand the physiological and environmental conditions which can interfere both in the social engagement and the cognitive abilities of such population, so that better and more realistic interventional strategies can be developed.
The differences observed in visual fixation at social stimuli of patients with RS and TD children are perhaps super-estimated, since they were not age-matched in our study. We sure understand that TD young children are not the more adequate control to understand social preferences in RS; on the other hand, comparisons between RS and TD children are not an easy or even feasible task, since age-matched groups, especially considering older patients, would probably result in huge developmental differences, and to match them by intellectual tests is still impossible.
Our clinical experience along 50 years show us that is very difficult to follow rigorous scientific criteria when studying RS, especially regarding the composition of a realistic control group. It is a fact that RS and ASD are significantly more frequent in females and males, respectively, what has reflected in our samples very strongly.
In our next steps in this research line we will compare visual fixation in social stimuli of only aged-matched girls with RS and ASD, so that such variables can be controlled. In spite of these evident fragilities, our results show that RS patients present social domain more preserved than other cognitive aspects, at least regarding what we know up to now, indicating probably more functional areas which may be focused on in the development of new therapeutic and leisure strategies.
It is a fact that eye tracking technologies have made possible to understand ever better not only the cognitive pathways of patients without verbal communication and, in the case of RS, without motor possibilities, but also the different outcomes involving RS and ASD.
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