Author Response
The following is the authors’ response to the original reviews.
eLife assessment
This manuscript represents a cleanly designed experiment for assessing biological motion processing in children (mean age = 9) with and without ADHD. The group differences concerning accuracy in global and local motion processing abilities are solid, but the analyses suggesting dissociable relationships between global and local processing and social skills, age, and IQ need further interrogation. The results are useful in terms of understanding ADHD and the ontogenesis of different components of the processing of biological motion.
We thank the editors for the positive assessment of our manuscript. We have carefully considered the reviewers’ constructive and helpful comments and revised our manuscript accordingly. To address the question about the dissociable relationships between global and local BM processing, we have provided more evidence and additional analyses in this revised version.
Reviewer #1 (Public Review):
Summary:
The paper presents a nice study investigating differences in biological motion perception in participants with ADHD in comparison with controls. Motivated by the idea that there is a relationship between biological motion perception and social capabilities, the authors investigated local and global (holistic) biological motion perception, the group, and several additional behavioral variables that are affected in ADHS (IQ, social responsiveness, and attention/impulsivity). As well as local global biological motion perception is reduced in ADHD participants. In addition, the study demonstrates a significant correlation between local biological motion perception skills and the social responsiveness score in the ADHD group, but not the controls. A path analysis in the ADHD data suggests that general performance in biological motion perception is influenced mainly by global biological motion perception performance and attentional and perceptual reasoning skills.
Strengths:
It is true that there exists not much work on biological motion perception and ADHD. Therefore, the presented study contributes an interesting new result to the biological motion literature and adds potentially also new behavioral markers for this clinical condition. The design of the study is straightforward and technically sound, and the drawn conclusions are supported by the presented results.
Thank you for your positive assessment of our work.
Weaknesses:
Some of the claims about the relationship between genetic factors and ADHD and the components of biological motion processing have to remain speculative at this point because genetic influences were not explicitly tested in this paper.
We agree that the relationship between genetic factors and BM processing in ADHD needs more investigation, We have modified our statement in Discussion section as following:
“Using the classical twin method, Wang et al. found that the distinction between local and global BM processing may stem from the dissociated genetic bases. The former, to a great degree, seems to be acquired phylogenetically20,21,59,60, while the latter is primarily obtained through individual development19.” (lines 421 - 425),
Reviewer #2 (Public Review):
Summary:
Tian et al. aimed to assess differences in biological motion (BM) perception between children with and without ADHD, as well as relationships to indices of social functioning and possible predictors of BM perception (including demographics, reasoning ability and inattention). In their study, children with ADHD showed poorer performance relative to typically developing children in three tasks measuring local, global, and general BM perception. The authors further observed that across the whole sample, performance in all three BM tasks was negatively correlated with scores on the social responsiveness scale (SRS), whereas within groups a significant relationship to SRS scores was only observed in the ADHD group and for the local BM task. Local and global BM perception showed a dissociation in that global BM processing was predicted by age, while local BM perception was not. Finally, general (local & global combined) BM processing was predicted by age and global BM processing, while reasoning ability mediated the effect of inattention on BM processing.
Strengths:
Overall, the manuscript is presented in a relatively clear fashion and methods and materials are presented with sufficient detail so the study could be reproduced by independent researchers. The study uses an innovative, albeit not novel, paradigm to investigate two independent processes underlying BM perception. The results are novel and have the potential to have wide-reaching impact on multiple fields.
We appreciate your positive assessment of our work.
Weaknesses:
Except for the main analysis, it is unclear what the authors' specific predictions are regarding the three different tasks they employ. The three BM tasks are used to probe different processes underlying BM perception, but it is difficult to gather from the introduction why these three specific tasks were chosen and what predictions the authors have about the performance of the ADHD group in these tasks. Relatedly, the authors do not report whether (and if so, how) they corrected for multiple comparisons in their analyses. As the number of tests one should control for depends on the theoretical predictions (http://daniellakens.blogspot.com/2016/02/why-you-dont-need-to-adjust-you-alpha.html), both are necessary for the reader to assess the statistical validity of the results and any inferences drawn from them. The same is the case for the secondary analyses exploring relationships between the 3 individual BM tasks and social function measured by the social responsivity scale (SRS).
We appreciate these constructive suggestions. In response, we have included a detailed description in the Introduction section explaining why we employed three different tasks and our predictions about the performance in ADHD:
“Despite initial indications, a comprehensive investigation into BM perception in ADHD is warranted. We proposed that it is essential to deconstruct BM processing into its multiple components and motion features, since treating them as a single entity may lead to misleading or inconsistent findings31. To address this issue, we employed a carefully designed behavioral paradigm used in our previous study19, making slight adjustments to adapt for children. This paradigm comprises three tasks. Task 1 (BM-local) aimed to assess the ability to process local BM cues. Scrambled BM sequences were displayed and participants could use local BM cues to judge the facing direction of the scrambled walker. Task 2 (BM-global) tested the ability to process the global configuration cues of the BM walker. Local cues were uninformative, and participants used global BM cues to determine the presence of an intact walker. Task 3 (BM-general) tested the ability to process general BM cues (local + global cues). The stimulus sequences consisted of an intact walker and a mask containing similar target local cues, so participants could use general BM cues (local + global cues) to judge the facing direction of the walker.” (lines 116 - 130)
“In Experiment 1, we examined three specific BM perception abilities in children with ADHD. As mentioned earlier, children with ADHD also show impaired social interaction, which implies atypical social cognition. Therefore, we speculated that children with ADHD performed worse in the three tasks compared to TD children.” (lines 131 - 134)
Additionally, we have reported the p values corrected for multiple comparisons (false discovery rate, FDR) in the revised manuscript wherever it was necessary to adjust the alpha (lines 310 - 316; Table 2). The pattern of the results remained unchanged.
In relation to my prior point, the authors could provide more clarity on how the conclusions drawn from the results relate to their predictions. For example, it is unclear what specific conclusions the authors draw based on their findings that ADHD show performance differences in all three BM perception tasks, but only local BM is related to social function within this group. Here, the claim is made that their results support a specific hypothesis, but it is unclear to me what hypothesis they are actually referring to (see line 343 & following). This lack of clarity is aggravated by the fact that throughout the rest of the discussion, in particular when discussing other findings to support their own conclusions, the authors often make no distinction between the two processes of interest. Lastly, some of the authors' conclusions related to their findings on local vs global BM processing are not logically following from the evidence: For instance, the authors conclude that their data supports the idea that social atypicalities are likely to reduce with age in ADHD individuals. However, according to their own account, local BM perception - the only measure that was related to social function in their study - is understood to be age invariant (and was indeed not predicted by age in the present study).
Thank you for pointing out this issue. We have carefully revised the Discussion section about our findings to clarify these points:
“Our study contributes several promising findings concerning atypical biological motion perception in ADHD. Specifically, we observe the atypical local and global BM perception in children with ADHD. Notably, a potential dissociation between the processing of local and global BM information is identified. The ability to process local BM cues appears to be linked to the traits of social interaction among children with ADHD. In contrast, global BM processing exhibits an age-related development. Additionally, general BM perception may be affected by factors including attention.” (lines 387 - 393)
We have provided a detailed discussion on the two processes of interest to clarify their potential differences and the possible reasons behind the difference of the divergent developmental trajectories between local and global BM processing:
“BM perception is considered a multi-level phenomenon56-58. At least in part, processing information of local BM and global BM appears to involve different genetic and neural mechanisms16,19. Using the classical twin method, Wang et al. found that the distinction between local and global BM processing may stem from the dissociated genetic bases. The former, to a great degree, seems to be acquired phylogenetically20,21,59,60, while the latter is primarily obtained through individual development19. The sensitivity to local rather than global BM cues seems to emerge early in life. Visually inexperienced chicks exhibit a spontaneous preference for the BM stimuli of hen, even when the configuration was scrambled20. The same finding was reported in newborns. On the contrary, the ability to process global BM cues rather than local BM cues may be influenced by attention28,29 and shaped by experience24,56.” (lines 419 - 430)
“We found that the ability to process global and general BM cues improved significantly with age in both TD and ADHD groups, which imply the processing module for global BM cues tends to be mature with development. In the ADHD group, the improvement in processing general and global BM cues is greater than that in processing local BM cues, while no difference was found in TD group. This may be due to the relatively higher baseline abilities of BM perception in TD children, resulting in a relatively milder improvement. These findings also suggest a dissociation between the development of local and global BM processing. There seems to be an acquisition of ability to process global BM cues, akin to the potential age-related improvements observed in certain aspects of social cognition deficits among individuals with ADHD5, whereas local BM may be considered an intrinsic trait19.” (lines 438 -449)
In addition, we have rephased some inaccurate statements in revised manuscript. Another part of social dysfunction might be stable and due to the atypical local BM perception in ADHD individuals, although some studies found a part of social dysfunction would reduce with age in ADHD individuals. One reason is that some factors related to social dysfunction would improve with age, like the symptom of hyperactivity.
Results reported are incomplete, making it hard for the reader to comprehensively interpret the findings and assess whether the conclusions drawn are valid. Whenever the authors report negative results (p-values > 0.05), the relevant statistics are not reported, and the data not plotted. In addition, summary statistics (group means) are missing for the main analysis.
Thanks for your comments. We have provided the complete statistical results in the revised manuscript (lines 309 - 316) and supplementary material, which encompass relevant statistics and plots of negative results (Figure 4, Figure S2 and S3), in accordance with our research questions. And we have also included summary statistics in the Results section (lines 287 - 293).
Some of the conclusions/statements in the article are too strong and should be rephrased to indicate hypotheses and speculations rather than facts. For example, in lines 97-99 the authors state that the finding of poor BM performance in TD children in a prior study 'indicated inferior applicability' or 'inapplicable experimental design'. While this is one possibility, a perhaps more plausible interpretation could be that TD children show 'poor' performance due to outstanding maturation of the underlying (global) BM processes (as the authors suggest themselves that BM perception can improve with age). There are several other examples where statements are too strong or misleading, which need attention.
We thank you for pointing out the issue. We have toned down and rephrased the strong statements and made the necessary revisions.
“Another study found that children with ADHD performed worse in BM detection with moderate ratios of noise34. This may be due to the fact that BM stimuli with noise dots will increase the difficulty of identification, which highlights the difference in processing BM between the two groups33,35.” (lines 111 - 115)
Reviewer #3 (Public Review):
Summary:
The authors presented point light displays of human walkers to children (mean = 9 years) with and without ADHD to compare their biological motion perception abilities and relate them to IQ, social responsiveness scale (SRS) scores and age. They report that children with ADHD were worse at all three biological motion tasks, but that those loading more heavily on local processing related to social interaction skills and global processing to age. The important and solid findings are informative for understanding this complex condition, as well as biological motion processing mechanisms in general. However, I am unsure that these differences between local and global skills are truly supported by the data and suggest some further analyses.
Strengths:
The authors present clear differences between the ADHD and TD children in biological motion processing, and this question has not received as much attention as equivalent processing capabilities in autism. They use a task that appears well controlled. They raise some interesting mechanistic possibilities for differences in local and global motion processing, which are distinctions worth exploring. The group differences will therefore be of interest to those studying ADHD, as well as other developmental conditions, and those examining biological motion processing mechanisms in general.
We appreciate your positive feedback. In revised manuscript, we have added more analyses to support the differences between local and global motion processing. Please refer to our response to the point #3 you mentioned below.
Weaknesses:
I am unsure that the data are strong enough to support claims about differences between global and local processing wrt social communication skills and age. The mechanistic possibilities for why these abilities may dissociate in such a way are interesting, but do not seem so plausible to me. I am also concerned about gender, and possible autism, confounds when examining the effect of ADHD. Specifics:
Gender confound. There are proportionally more boys in the ADHD than TD group. The authors appear to attempt to overcome this issue by including gender as a covariate. I am unsure if this addresses the problem. The vast majority of participants in the ADHD group are male, and gender is categorically, not continuously, defined. I'm pretty sure this violates the assumptions of ANCOVA.
We appreciate your comments. We concur with you that although we observed a clear difference between local and global BM processing in ADHD, the evidence is to some extent preliminary. The mechanistic possibilities for why these abilities may dissociate have been discussed in revised manuscript. Please refer to the response to reviewer 2’s point #2. To further examine if gender played a role in the observed results, we used a statistical matching technique to obtain a sub-dataset. The pattern of results remained with the more balanced dataset (see Supplementary Information part 1). According to your suggestion, we have also presented the results without using gender as a covariate in main text and also separated the data of boys and girls on the plots (see Figure 1 and Figure S1). There were indeed no signs of a gender effect.
Autism. Autism and ADHD are highly comorbid. The authors state that the TD children did not have an autism or ADHD diagnosis, but they do not state that the ADHD children did not have an autism diagnosis. Given the nature of the claims, this seems crucial information for the reader.
Thanks for your suggestion. We have confirmed that all children with ADHD in our study were not diagnosed with autism. We used a semi-structured interview instrument (K-SADSPL-C) to confirm every recruited child with ADHD but not with ASD. The exclusion criteria for both groups were mentioned in the Materials and methods section:
“Exclusion criteria for both groups were: (a) neurological diseases; (b) other neurodevelopmental disorders (e.g., ASD, Mental retardation, and tic disorders), affective disorders and schizophrenia…” (lines 158 - 162)
Conclusions. The authors state frequently that it was the local BM task that related to social communication skills (SRS) and not the global tasks. However, the results section shows a correlation between SRS and all three tasks. The only difference is that when looking specifically within the ADHD group, the correlation is only significant for the local task. I think that if the authors wish to make strong claims here they must show inferential stats supporting (1) a difference between ADHD and TD SRS-Task 1 correlations, and (2) a difference in those differences for Task 2 and 3 relative to Task 1. I think they should also show a scatterplot of this correlation, with separate lines of best fit for the two groups, for Tasks 2 and 3 as well. I.e. Figure 4 should have 3 panels. I would recommend the same type of approach for age. Currently, they have small samples for correlations, and are reading much of theoretical significance between some correlations passing significance threshold and others not. It would be incredibly interesting if the social skills (as measured by SRS) only relate to local BM abilities, and age only to global, but I think the data are not so clear with the current information. I would be surprised if all BM abilities did not improve with age. Even if there is some genetic starter kit (and that this differs according to particular BM component), most abilities improve with learning/experience/age.
Thank you for this recommendation. We have added more statistics to test differences between the correlations (a difference between ADHD and TD in SRS-Task 1 correlations (see the first paragraph of Supplementary Information part 2), a difference in SRS-response accuracy correlations for Task 2 and 3 relative to Task 1(see the second paragraph of Supplementary Information part 2), and a difference in age-response accuracy correlations for Task 2 and 3 relative to Task 1 in ADHD group (see Supplementary Information part 3)). Additionally, we have included scatterplots for SRS-Task1, SRS-Task2, SRS-Task3 (with separate lines of best fit for the two groups in each, see Figure 4), SRS-ADHD, SRS-TD, age-ADHD and age-TD (with separate lines of best fit for the three tasks in each, see Figure S2 and S3) to make a clear demonstration. Detailed results have been presented in the revised manuscript and Supplementary Information. We expect these further analyses would strengthen our conclusions.
Theoretical assumptions. The authors make some sweeping statements about local vs global biological motion processing that need to be toned down. They assume that local processing is specifically genetically whereas global processing is a product of experience. The fact their global, but not local, task performance improves with age would tend to suggest there could be some difference here, but the existing literature does not allow for this certainty. The chick studies showing a neonatal preference are controversial and confounded - I cannot remember the specifics but I think there an upper vs lower visual field complexity difference here.
Thank you for pointing out this issue. We have toned down rephrased our claims that the difference between local and global BM processing according to your suggestion:
“These findings suggest that local and global mechanisms might play different roles in BM perception, though the exact mechanisms underlying the distinction remain unclear. Exploring the two components of BM perception will enhance our understanding of the difference between local and global BM processing, shedding light on the psychological processes involved in atypical BM perception.” (lines 87 - 92)
Reviewer #1 (Recommendations For The Authors):
I have only a number of minor points that should be addressed prior to publication:
L. 95ff: What is meant by 'inapplicability of experimental designs' ? This paragraph is somewhat unclear.
In revised manuscript, we have clarified this point (lines 111 - 115).
L. 146: The groups were not perfectly balanced for sex. Would results change fundamentally in a more balanced design, or can arguments be given that gender does not play a role, like it seems to be the case for some functions in biological motion perception (e.g. Pavlova et al. 2015; Tsang et al 2018). One could provide a justification that this disbalance does not matter or test for subsampled balanced data sets maybe.
This point is similar to the point #1 from reviewer 3, and we have addressed this issue in our response above.
L. 216 f.: In this paragraph it does not become very clear that the mask for the global task consisted of scrambles generated from walkers walking in the same direction. The mask for the local task then should consist of a balanced mask that contains the same amount of local motion cues indicating right and leftwards motion. Was this the case? (Not so clear from this paragraph.)
Regarding the local task, the introduction of mask would make the task too difficult for children. Therefore, in the local task, we only displayed a scrambled walker without a mask, which was more suitable for children to complete the task. We have made clear this point in the corresponding paragraph (lines 232 - 241).
L. 224 ff.: Here it would be helpful to see the 5 different 'facing' directions of the walkers. What does this exactly mean? Do they move on oblique paths that are not exactly orthogonal to the viewing directions, and how much did these facing directions differ?
Out of the five walkers we used, two faced straight left or right, orthogonal to the viewing directions. Two walked with their bodies oriented 45 degrees from the observer, to the left or right. The last one walked towards the observer. We have included a video (Video 4) to demonstrate the 5 facing directions.
L. 232: How was the number of 5 practicing trials determined/justified?
As mentioned in main text, global BM processing is susceptible to learning. Therefore, too many practicing trials would increase BM visual experience and influence the results. We determined the number of training trials to be 5 based on the results of the pilot experiment. During this phase, we observed that nearly all children were able to understand the task requirements well after completing 5 practicing trials.
L 239: Apparently no non-parametric statistics was applied. Maybe it would be good to mention in the Statistics section briefly why this was justified.
We appreciate your suggestion and have cited two references in the Statistics section (Fagerland et al. 2012, Rochon et al. 2012). Fagerland et al., mentioned that when the sample size increases, the t-test is more robust. According to the central limit theorem, when the sample size is greater than 30, the sampling distribution of the mean can be safely assumed to be normal.
(http://www2.psychology.uiowa.edu/faculty/mordkoff/GradStats/part%201/I.07%20normal.p df). In fact, we also ran non-parametric statistics for our data and found the results to be robust.
L 290: 'FIQ' this abbreviation should be defined.
Regarding the abbreviation ’FIQ’, it stands for the abbreviation of the full-scale intellectual quotient, which was mentioned in Materials and methods section:
“Scores of the four broad areas constitute the full-scale intellectual quotient (FIQ).”
L. 290 ff.: These model 'BM-local = age + gender etc ' is a pretty sloppy notation. I think what is meant that a GLM was used that uses the predictors gender etc. time appropriate beta_i values. This formula should be corrected or one just says that a GLM was run with the predictors gender ....
The same criticism applies to these other models that follow.
We thank you for pointing this out. We have modified all formulas accordingly in the revised manuscript (see part3 of the Results section).
All these models assume linearity of the combination of the predictors.was this assumption verified?
We referred to the previous study of BM perception in children. They found main predictor variables, including IQ (Rutherford et al., 2012; Jones et al., 2011) and age (Annaz et al., 2010; van et al., 2016), have a linear relation with the ability of BM processing.
L. 296ff.: For model (b) it looks like general BM performance is strongly driven by the predictor global BM performance in the group of patients. Does the same observation also apply to the normals?
The same phenomenon was not observed in TD children. We have briefly discussed this point in the Discussion section of the revised manuscript (lines 449 - 459).
Reviewer #2 (Recommendations For The Authors):
(1) Please add public access to the data repository so data availability can be assessed.
The data of the study will be available at https://osf.io/37p5s/.
(2) Although overall, the language was clear and understandable, there are a few parts where language might confuse a reader and lead to misconceptions. For instance, line 52: Did the authors mean to refer to 'emotions and intentions' instead of 'emotions and purposes'? See also examples where rephrasing may help to reflect a statement is speculation rather than fact.
Thanks for the comments. We have carefully checked the full text and rephrased the confused statements.
(3) Line 83/84: Autism is not a 'mental disorder' - please change to something like 'developmental disability'. Authors are encouraged to adapt their language according to terms preferred by the community (e.g., see Fig. 5 in this article:
https://onlinelibrary.wiley.com/doi/10.1002/aur.2864)
Suggestion well taken. We have changed the wording accordingly:
“In recent years, BM perception has received significant attention in studies of mental disorders (e.g., schizophrenia30) and developmental disabilities, particularly in ASD, characterized by deficits in social communication and social interaction31,32.” (lines 93 - 95)
(4) Please report how the sample size for the study was determined.
In the Materials and methods section (lines 168 - 173), we explained how the sample size was determined.
Line 94: It would be helpful to have a brief description of what neurophysiological differences have been observed upon BM perception in children with ADHD.
Thanks for the comment. We have added a brief description of neurophysiological findings in children with ADHD (lines 108 - 111).
(6) Line 106/107 and 108/109: please add references.
We have revised this part, and the relevant findings and references are in line with the revised manuscript (lines 77, 132 - 133).
(7) Line 292: Please add what order the factors were entered into each regression model.
Regarding this issue, we used SPSS 26 for the main analysis. SPSS utilizes the Type III sum of squares (default) to evaluate models. Regardless of the order in the GLM, we will obtain the same result. For more information, please refer to the documentation of SPSS 26 (https://www.ibm.com/docs/en/spss-statistics/26.0.0?topic=features-glm-univariate-analysis).
Reviewer #3 (Recommendations For The Authors)
(1) Task specifics. It is key to understanding the findings, as well as the dissociation between tasks, that the precise nature of the stimuli is clear. I think there is room for improvement in description here. Task 1 is described as involving relocating dots within the range of the intact walker. Of course, PLWs are created by presenting dots at the joints, so relocation can involve either moving to another place on the body, or random movement within the 2D spatial array (which likely involves moving it off the body). Which was done? It is said that Ps must indicate the motion direction, but what was the display of the walker? Sagittal? Task 2 requires detecting whether there is an intact walker amongst scrambled walkers. Were all walkers completely overlaid? Task 3 requires detecting the left v right facing of an intact walker at different orientations, presented amongst noise. So Task 3 requires determining facing direction and Task 1 walking direction. Are these tasks the same but described differently? Or can walkers ever walk backwards? Wrt this point, I also think it would help the reader if example videos were uploaded.
We appreciate you for bringing this to our attention. With regards to Task 1, it appears that your second speculation is correct. We scrambled the original dots and randomly presented them within the 2D spatial array (which likely involved moving them off the body). As a result, the global configuration of the 13 dots was completed disrupted while preserving the motion trajectory of each individual dot. This led to the display of scrambled dots on the monitor (which does not resemble a human). In practice, these local BM cues contain information about motion direction. In Task 2, the target walkers completely overlaid by a mask that is approximately 1.44 times the size of the intact walker. The task requirements of Task 1 and Task3 are same, which is judging the motion (walking) direction. The difference is that Task 1 displayed a scrambled walker while Task 3 displayed an intact walker within a mask. We have clarified these points and improved our descriptions in Procedure section and created example videos for each task, which we believe will be helpful for the readers to understand each task.
(2) Gender confound (see above). I think that the authors should present the results without gender as a covariate. Can they separate boys and girls on the plots with different coloured individual datapoints, such that readers can see whether it's actually a gender effect driving the supposed ADHD effect? And show that there are no signs of a gender effect in their TD group?
This point is similar to the point #1 you mentioned. Please refer to our response to that point above.
(3) Autism possible confound (see above). I think the authors must report whether any of the ADHD group had an autism diagnosis.
Please refer to the response for the point #2 your mentioned.
(4) Conclusions concerning differences between the local and global tasks wrt SRS and age (see above). I believe the authors should add stats demonstrating differences between the correlations to support such claims, as well as demonstrating appropriate scatterplots for SRS-Task 1, SRS-Task 2, SRS-Task 3 and age-Task 1, age-Task2 and age-Task 3 (with separate lines of best fit for the two groups in each).
Please refer to the response for the point #3 your mentioned.
(5) Theoretical assumptions (see above). I would suggest rephrasing all claims here to outline that these discussed mechanistic differences between local and global BM processing are only possibilities and not known on the basis of existing data.
Please refer to the response for the point #4 your mentioned.
