Motor differences in autism during a human-robot imitative gesturing task
DOI:
https://doi.org/10.51224/SRXIV.21Keywords:
autism, imitation, motion capture, robotics, dynamic time warping, motor skills, gestureAbstract
Difficulty with imitative gesturing is frequently observed as a clinical feature of autism. Current practices for assessment of imitative gesturing ability–behavioral observation and parent report–do not allow precise measurement of specific components of imitative gesturing performance, instead relying on subjective judgments. Advances in technology allow researchers to objectively quantify the nature of these movement differences, and to use less socially stressful interaction partners (e.g., robots). In this study, we aimed to quantify differences in imitative gesturing between autism and neurotypical development during human-robot interaction. Thirty-five autistic (n = 19) and neurotypical (n = 16) participants imitated social gestures of an interactive robot (e.g., wave). The movements of the participants and the robot were recorded using an infrared motion-capture system with reflective markers on corresponding head and body locations. We used dynamic time warping to quantify the degree to which the participant’s and robot’s movement were aligned across the movement cycle. Results revealed differences between autism and neurotypical participants in imitative accuracy, primarily in the movements requiring unilateral extension of the arm. Imitative gesturing is a building block to later development of social-communication skills; difficulty with reproduction and functional use of gestures may negatively impact social engagement, and in turn, learning opportunities. It is important to understand the underlying motor control and sensorimotor integration mechanisms that support imitative gesturing in ASD in order to identify appropriate intervention targets.
Metrics
References
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., Text Revision). Washington, DC: American Psychiatric Publishing.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.
Anzulewicz, A., Sobota, K. & Delafield-Butt, J. (2016) Toward the Autism Motor Signature: Gesture patterns during smart tablet gameplay identify children with autism. Scientific Reports, 6. https://doi.org/10.1038/srep31107
Bates, E., Benigni, L., Bretherton, I., Camaioni, L., & Volterra, V. (1979). The emergence of symbols: Cognition and communication in infancy. New York: Academic Press.
Bates, D., Mächler, M., Bolker, B., & Walker, S. (2015). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1–27.1.
Bekele, E., Crittendon, J. A., Swanson, A., Sarkar, N., & Warren, Z. E. (2013). Pilot clinical application of an adaptive robotic system for young children with autism. Autism, 18(5), 598-608. https://doi.org/10.1177%2F1362361313479454
Berndt, D. J., Clifford, J. (1994). Using dynamic time warping to find patterns in time series. Proceedings of the 3rd International Conference on Knowledge Discovery and Data Mining, AAAI Technical Report, 359-370.
Bhat, A. N., Landa, R. J., & Galloway, J. C. C. (2011). Current perspectives on motor functioning in infants, children, and adults with Autism Spectrum Disorders. Physical Therapy, 91, 1116-1129. https://doi.org/10.2522/ptj.20100294
Borghi, A. M., & Cangelosi, A. (2014). Action and language integration: From humans to cognitive robots. Topics in Cognitive Science, 6(3), 344-358. https://doi.org/10.1111/tops.12103
Boucenna, S., Cohen, D., Meltzoff, A. N., Gaussier, P., & Chetouani, M. (2016). Robots learn to recognize individuals from imitative encounters with people and avatars. Scientific Reports, 6, 19908. https://doi.org/10.1038/srep19908
Bugnariu, N., & Fung, J. (2010). Virtual environments and sensory integration: Effects of aging and stroke. Schedae, 1, 59-76.
Bugnariu, N., Young, C., Rockenbach, K., Patterson, R., Garver, C., Beltran, M., . . . Popa, D. (2013). Human-robot interaction as a tool to evaluate and quantify motor imitation behavior in children with Autism Spectrum Disorders. IEEE Proc. 10th International Conference on Virtual Rehabilitation (ICVR 2013), 57-62. https://doi.org/10.1109/ICVR.2013.6662088
Cangelosi, A., & Schlesinger, M. (2015). Motor-skill acquisition. In Developmental robotics: From babies to robots (pp. 147-184). Cambridge, MA: MIT Press.
de Marchena, A., Kim, E. S., Bagdasarov, A., Parish-Morris, J., Maddox, B. B., Brodkin, E. S., & Schultz, R. T. (2018). Atypicalities of Gesture Form and Function in Autistic Adults. Journal of Autism & Developmental Disorders. https://doi.org/10.1007/s10803-018-3829-x
DeFilippis, M., & Wagner, K. D. (2016). Treatment of Autism Spectrum Disorder in Children and Adolescents. Psychopharmacology bulletin, 46(2), 18–41.
Dewey, D., Cantell, M., & Crawford, S. G. (2007). Motor and gestural performance in children with autism spectrum disorders, developmental coordination disorders, and/or attention deficit hyperactivity disorder. Journal of the International Neuropsychological Society, 13, 246-256. https://doi.org/10.1017/S1355617707070270
Diehl, J. J., Schmitt, L. M., Villano, M., & Crowell, C. R. (2012) The clinical use of robots for individuals with Autism Spectrum Disorders: A critical review. Research in Autism Spectrum Disorders, 6(1), 249-262. https://doi.org/10.1016/j.rasd.2011.05.006
Ellawadi, A. B., & Weismer, S. E. (2014). Assessing gestures in young children with autism spectrum disorders. Journal of Speech Language and Hearing Research, 57(2), 524-531. https://doi.org/10.1044/2013_JSLHR-L-12-0244
Gonzalez, D. A., Glazebrook, C. M., Studenka, B. E., & Lyons, J. (2013). Motor interactions with another person: Do individuals with autism spectrum disorder plan ahead? Frontiers in Integrative Neuroscience, 7(23). https://doi.org/10.3389/fnint.2013.00023
Green, D., Charman, T., Pickles, A., Chandler, S., Loucas, T., Simonoff, E., & Baird, G. (2009). Impairment in movement skills of children with autistic spectrum disorders. Developmental Medicine & Child Neurology, 51(4), 311-316. https://doi.org/10.1111/j.1469-8749.2008.03242.x
Haswell, C. C., Izawa, J., Dowell, L. R., Mostofsky, S. H., & Shadmehr, R. (2009). Representation of internal models of action in the autistic brain. Nature Neuroscience, 12(8), 970-972. https://doi.org/10.1038/nn.2356
Hopkins, I. M., Gower, M. W., Perez, T. A., Smith, D. S., Amthor, F. R., Wimsatt, F. C., & Biasini, F. J. (2011). Avatar assistant: Improving social skills in students with an ASD through a computer-based intervention. Journal of Autism and Developmental Disorders, 41(11), 1543-1555. https://doi.org/10.1007/s10803-011-1179-z
Hughes, C. (1996). Brief report: Planning problems in autism at the level of motor control. Journal of Autism and Developmental Disorders, 26(1), 99-107. https://doi.org/10.1007/BF02276237
Iacoboni, M. (2005). Neural mechanisms of imitation. Current Opinion in Neurobiology, 15, 632–637. https://doi.org/10.1016/j.conb.2005.10.010
Ingersoll, B., Lewis, E., & Kroman, E. (2007). Teaching the imitation and spontaneous use of descriptive gestures in young children with autism using a naturalistic behavior intervention. Journal of Autism and Developmental Disorders, 37(8), 1446-1456. https://doi.org/10.1007/s10803-006-0221-z
Izawa, J., Pekny, S. E., Marko, M. K., Haswell, C. C., Shadmehr, R., & Mostofsky, S. H. (2012). Motor learning relies on integrated sensory inputs in ADHD, but over-selectively on proprioception in autism spectrum conditions. Autism Research, 5(2), 124-136. https://doi.org/10.1002/aur.1222
Jones, S. S. (2009). Development of imitation in infancy. Philosophical Transactions of the Royal Society B, 364, 2325-2335. https://doi.org/10.1098/rstb.2009.0045
Kandalaft, M. R., Didehbani, N., Krawczyk, D. C., Allen, T. T., & Chapman, S. B. (2013). Virtual reality social cognition training for young adults with high-functioning autism. Journal of Autism and Developmental Disorders, 43(1), 34-44. https://doi.org/10.1007/s10803-012-1544-6
Koul, A., Soriano, M., Tversky, B., Becchio, C., & Cavallo, A. (2019). The kinematics that you do not expect: Integrating prior information and kinematics to understand intentions. Cognition, 182, 213-219. https://doi.org/10.1016/j.cognition.2018.10.006
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. (2017). lmerTest package: tests in linear mixed effects models. Journal of statistical software, 82(1), 1-26. https://doi.org/10.18637/jss.v082.i13
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2012). Autism Diagnostic Observation Schedule–2nd edition. Los Angeles, CA: Western Psychological Services.
MacNeil, L. K., & Mostofsky, S. H. (2012). Specificity of dyspraxia in children with autism. Neuropsychology, 26(2), 165-171. https://doi.org/10.1037/a0026955
McAuliffe, D., Pillai, A. S., Tiedemann, A., Mostofsky, S. H., & Ewen, J. B. (2017). Dyspraxia in ASD: Impaired coordination of movement elements. Autism Res, 10(4), 648-652. https://doi.org/10.1002/aur.1693
Martineau, J., Andersson, F., Barthelemy, C., Cottier, J. P., & Destrieux, C. (2010). Atypical activation of the mirror neuron system during perception of hand motion in autism. Brain Research, 1320, 168-175. https://doi.org/10.1016/j.brainres.2010.01.035
Meltzoff, A., & Moore, M. K. (1983). The origin of imitation in infancy: Paradigm, phenomena, and theories. Advances in Infancy Research, 2, 265-301.
Miller, H.L., Sherrod, G.M., Mauk, J.E. Fears, N. E., Hynan, L. S., Tamplain, P. M. (2021) Shared Features or Co-occurrence? Evaluating Symptoms of Developmental Coordination Disorder in Children and Adolescents with Autism Spectrum Disorder. Journal of Autism & Developmental Disorders, 51, 3443–3455. https://doi.org/10.1007/s10803-020-04766-z
Minshew, N. J., Sung, K., Jones, B. L., & Furman, J. M. (2004). Underdevelopment of the postural control system in autism. Neurology, 63(11), 2056-2061. https://doi.org/10.1212/01.WNL.0000145771.98657.62
Mostofsky, S. H., Dubey, P., Jerath, V. K., Jansiewicz, E. M., Goldberg, M. C., & Denckla, M. B. (2006). Developmental dyspraxia is not limited to imitation in children with autism spectrum disorders. Journal of the International Neuropsychological Society, 12(3), 314-326. https://doi.org/10.1017/S1355617706060437
Mostofsky, S. H., & Ewen, J. B. (2011). Altered connectivity and action model formation in autism is autism. Neuroscientist, 17(4), 437-448. https://doi.org/10.1177/1073858410392381
Pillai, A. S., McAuliffe, D., Lakshmanan, B. M., Mostofsky, S. H., Crone, N. E., & Ewen, J. B. (2018). Altered task-related modulation of long-range connectivity in children with autism. Autism Research, 11(2), 245-257. https://doi.org/10.1002/aur.1858
Rab, G., Petuskey, K., & Bagley, A. (2002). A method for determination of upper extremity kinematics. Gait & Posture, 15(2), 113-119. https://doi.org/10.1016/S0966-6362(01)00155-2
Ranatunga, I., Beltran, M., Torres, N. A., Patterson, R., Bugnariu, N., Garver, C., Popa, D. (2013). Human-robot upper body gesture imitation analysis for Autism Spectrum Disorders. Lecture Notes in Computer Science: Social Robotics, 823, 218-228. https://doi.org/10.1007/978-3-319-02675-6_22
Ranatunga, I., Torres, N. A., Patterson, R., Bugnariu, N., Stevenson, M., Popa, D. (2012). RoDiCA: A human-robot interaction system for treatment of childhood Autism Spectrum Disorders. ACM International Proc. 5th International Conference on Pervasive Technologies Related to Assistive Environments, 1-6. https://doi.org/10.1145/2413097.2413160
Rogers, S. J. (1999). An examination of the imitation deficit in autism. In J. Nadel & G. Butterworth (Eds.), Imitation in Infancy (pp. 254-283). New York: Cambridge University Press.
Rogers, S. J., Bennetto, L., McEvoy, R., & Pennington, B. F. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67, 2060-2073. https://doi.org/10.1111/j.1467-8624.1996.tb01843.x
Rogers, S. J., Hepburn, S. L., Stackhouse, T., & Wehner, E. (2003). Imitation performance in toddlers with autism and those with other developmental disorders. Journal of Child Psychology and Psychiatry, 44(5), 763-781. https://doi.org/10.1111/1469-7610.00162
Romero, V., Fitzpatrick, P., Roulier, S., Duncan, A., Richardson, M. J., & Schmidt, R. C. (2018). Evidence of embodied social competence during conversation in high functioning children with autism spectrum disorder. PLoS One, 13(3), e0193906. https://doi.org/10.1371/journal.pone.0193906
Rutter, M., Bailey, A., & Lord, C. (2003). The social communication questionnaire: Manual. Western Psychological Services.
Rutter, M., LeCouteur, A., & Lord, C. (2003). Autism Diagnostic Interview-Revised. Los Angeles, CA: Western Psychological Services.
Salowitz, N. M. G., Eccarius, P., Karst, J., Carson, A., Schohl, K., Stevens, S., ... Scheidt, R. A. (2013). Brief report: Visuo-spatial guidance of movement during gesture imitation and mirror drawing in children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43, 985-995. https://doi.org/10.1007/s10803-012-1631-8
Scharoun, S. M., & Bryden, P. J. (2016). Anticipatory planning in children with autism spectrum disorder: An assessment of independent and joint action tasks. Frontiers in Integrative Neuroscience, 10(29). https://doi.org/10.3389/fnint.2016.00029
Simon, S. R. (2004). Quantification of human motion: gait analysis–benefits and limitations to its application to clinical problems. Journal of Biomechanics, 37(12), 1869-1880. https://doi.org/10.1016/j.jbiomech.2004.02.047
Smith, I. M., & Bryson, S. E. (2007). Gesture imitation in autism: II. Symbolic gestures and pantomimed object use. Cognitive Neuropsychology, 27(7), 679-700. https://doi.org/10.1080/02643290701669703
Smith, I. M., & Bryson, S. (1994). Imitation and action in autism: A critical review. Psychological Bulletin, 116, 259– 273. https://psycnet.apa.org/doi/10.1037/0033-2909.116.2.259
So, W. C., Wong, M. K., Lam, C. K., Lam, W. Y., Chui, A. T., Lee, T. L., . . . Fok, D. C. (2017). Using a social robot to teach gestural recognition and production in children with autism spectrum disorders. Disability and Rehabilitation: Assistive Technology, 1-13. https://doi.org/10.1080/17483107.2017.1344886
Srinivasan, S. M., Eigsti, I. M., Neelly, L., & Bhat, A. N. (2016). The effects of embodied rhythm and robotic interventions on the spontaneous and responsive social attention patterns of children with autism spectrum disorder (ASD): A pilot randomized controlled trial. Research in Autism Spectrum Disorders, 27, 54-72. https://doi.org/10.1016/j.rasd.2016.01.004
Toth, K., Munson, J., Meltzoff, A. N., & Dawson, G. (2006). Early predictors of communication development in young children with autism spectrum disorder: Joint attention, imitation, and toy play. Journal of Autism and Developmental Disorders, 36, 993-1005. https://doi.org/10.1007/s10803-006-0137-7
Tunçgenç, B., Pacheco, C., Rochowiak, R., Nicholas, R., Rengarajan, S., Zou, E., ... & Mostofsky, S. H. (2021). Computerized Assessment of Motor Imitation as a Scalable Method for Distinguishing Children With Autism. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 6(3), 321-328. https://doi.org/10.1016/j.bpsc.2020.09.001
Veness, C., Prior, M., Bavin, E., Eadeie, P., Cini, E., & Reilly, S. (2012). Early indicators of autism spectrum disorders at 12 and 24 months of age: a prospective, longitudinal comparative study. Autism, 16(2), 163-177. https://doi.org/10.1177%2F1362361311399936
Vivanti, G., & Rogers, S. J. (2014). Autism and the mirror neuron system: insights from learning and teaching. Philosophical transactions of the Royal Society of London. Series B, Biological sciences, 369(1644). https://doi.org/10.1098/rstb.2013.0184
Wang, Y., & Quadflieg, S. (2015). In our own image? Emotional and neural processing differences when observing human-human vs human-robot interactions. Social cognitive and affective neuroscience, 10(11), 1515–1524. https://doi.org/10.1093/scan/nsv043
Warren, Z., Zheng, Z., Das, S., Young, E. M., Swanson, A., Weitlauf, A., & Sarkar, N. (2015a). Brief report: Development of a robotic intervention platform for young children with ASD. Journal of Autism and Developmental Disorders, 45(12), 3870-3876. https://doi.org/10.1007/s10803-014-2334-0
Warren, Z. E., Zheng, Z., Swanson, A. R., Bekele, E., Zhang, L., Crittendon, J. A., ... Sarkar, N. (2015b). Can robotic interaction improve joint attention skills? Journal of Autism and Developmental Disorders, 45(11), 3726-3734. https://doi.org/10.1007/s10803-013-1918-4
Watson, L. R., Crais, E. R., Baranek, G. T., Dykstra, J. R., & Wilson, K. P. (2013). Communicative gesture use in infants with and without autism: a retrospective home video study. American journal of speech-language pathology, 22(1), 25–39. https://doi.org/10.1044/1058-0360(2012/11-0145)
Wechsler, D. (2011). WASI-II: Wechsler abbreviated scale of intelligence. Pearson Assessments.
Wijayasinghe, I. B., Ranatunga, I., Balakrishnan, N., Bugnariu, N., Popa, D. (2016). Human-robot gesture analysis for objective assessment of Autism Spectrum Disorder. International Journal of Social Robotics, 8, 695. https://doi.org/10.1007/s12369-016-0379-2
Wild, K. S., Poliakoff, E., Jerrison, A., & Gowen, E. (2012). Goal-directed and goal-less imitation in autism spectrum disorder. Journal of Autism and Developmental Disorders, 42(8), 1739-1749. https://doi.org/10.1007/s10803-011-1417-4
Williams, J. H. G., Whiten, A., & Singh, T. (2004). A systematic review of action imitation in autism spectrum disorder. Journal of Autism and Developmental Disorders, 34(3), 285-299. https://doi.org/10.1023/B:JADD.0000029551.56735.3a
Williams, J. H. G., Whiten, A., Suddendorf, T., & Perrett, D. I. (2001). Imitation, mirror neurons, and autism. Neuroscience and Biobehavioral Reviews, 25, 287-295. https://doi.org/10.1016/S0149-7634(01)00014-8
Young, G. S., Rogers, S. J., Hutman, T., Rozga, A., Sigman, M., & Ozonoff, S. (2011). Imitation from 12 to 24 months in autism and typical development: a longitudinal Rasch analysis. Developmental Psychology, 47(6), 1565-1578. https://doi.org/10.1037/a0025418
Zheng, Z., Young, E. M., Swanson, A. R., Weitlauf, A. S., Warren, Z. E., & Sarkar, N. (2016). Robot-mediated imitation skill training for children with autism. IEEE Transactions on Neural Systems and Rehabilitation Engineering: A Publication of the IEEE Engineering in Medicine and Biology Society, 24(6), 682-691. https://doi.org/10.1109/TNSRE.2015.2475724
Downloads
Posted
Categories
License
Copyright (c) 2021 Nicholas Fears, Gabriela Sherrod, Danielle Blankenship, Rita Patterson, Linda Hynan, Indika Wijayasinghe, Dan Popa, Nicoleta Bugnariu, Haylie L Miller
This work is licensed under a Creative Commons Attribution 4.0 International License.
