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Temporal Processing Instability with Millisecond Accuracy is a Cardinal Feature of Sensorimotor Impairments in Autism Spectrum Disorder: Analysis Using the Synchronized Finger-Tapping Task

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Abstract

To identify a specific sensorimotor impairment feature of autism spectrum disorder (ASD), we focused on temporal processing with millisecond accuracy. A synchronized finger-tapping task was used to characterize temporal processing in individuals with ASD as compared to typically developing (TD) individuals. We found that individuals with ASD showed more variability in temporal processing parameters than TD individuals. In addition, temporal processing instability was related to altered motor performance. Further, receiver operating characteristic (ROC) curve analyses indicated that altered temporal processing can be useful for distinguishing between individuals with and without ASD. These results suggest that instability of temporal processing with millisecond accuracy is a fundamental feature of sensorimotor impairments in ASD.

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References

  • Ackermann, H., Mathiak, K., & Riecker, A. (2007). The contribution of the cerebellum to speech production and speech perception: Clinical and functional imaging data. The Cerebellum, 6, 202–213.

    Article  PubMed  Google Scholar 

  • Allen, G., & Courchesne, E. (2003). Differential effects of developmental cerebellar abnormality on cognitive and motor functions in the cerebellum: An fMRI study of autism. The American Journal of Psychiatry, 160, 262–273.

    Article  PubMed  Google Scholar 

  • Association, A. P. (2013). Diagnostic and statistical manual of mental disorders (DSM-5®). Washington, DC: American Psychiatric Pub.

    Book  Google Scholar 

  • Bauman, M. L., & Kemper, T. L. (1994). Neuroanatomic observations of the brain in autism. The Neurobiology of Autism, 612, 119–145.

    Google Scholar 

  • Bölte, S., & Poustka, F. (2002). The relation between general cognitive level and adaptive behavior domains in individuals with autism with and without co-morbid mental retardation. Child Psychiatry and Human Development, 33, 165–172.

    Article  PubMed  Google Scholar 

  • Bosl, W., Tierney, A., Tager-Flusberg, H., & Nelson, C. (2011). EEG complexity as a biomarker for autism spectrum disorder risk. BMC Medicine 9, 18 doi:10.1186/1741-7015-9-18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Buckner, R. L. (2013). The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron, 80, 807–815.

    Article  PubMed  Google Scholar 

  • Cao, M., Wang, Z., & He, Y. (2015). Connectomics in psychiatric research: advances and applications. Neuropsychiatric Disease and Treatment, 11, 2801–2810. doi:10.2147/ndt.s63470.

    PubMed  PubMed Central  Google Scholar 

  • Charman, T., Pickles, A., Simonoff, E., Chandler, S., Loucas, T., & Baird, G. (2011). IQ in children with autism spectrum disorders: Data from the Special Needs and Autism Project (SNAP). Psychological Medicine, 41, 619–627.

    Article  PubMed  Google Scholar 

  • Chivate, R., Thakrar, P., Narang, J., Patkar, D., Kumar, S., Verma, M. PET/CT in Autism: A Diagnostic Tool. In Radiological Society of North America 2014 Scientific Assembly and Annual Meeting-Chicago IL, 2014.

  • Courchesne, E., Saitoh, O., Townsend, J., Yeung-Courchesne, R., Press, G., Lincoln, A., et al. (1994). Cerebellar hypoplasia and hyperplasia in infantile autism. Lancet, 343, 63–64.

    Article  PubMed  Google Scholar 

  • De Bildt, A., Sytema, S., Kraijer, D., & Minderaa, R. (2005). Prevalence of pervasive developmental disorders in children and adolescents with mental retardation. Journal of Child Psychology and Psychiatry, 46, 275–286.

    Article  PubMed  Google Scholar 

  • Faul, F., Erdfelder, E., Buchner, A., & Lang, A.-G. (2009). Statistical power analyses using G* Power 3.1: Tests for correlation and regression analyses. Behavior Research Methods, 41, 1149–1160.

    Article  PubMed  Google Scholar 

  • Fournier, K. A., Hass, C. J., Naik, S. K., Lodha, N., & Cauraugh, J. H. (2010). Motor coordination in autism spectrum disorders: A synthesis and meta-analysis. Journal of Autism and Developmental Disorders, 40, 1227–1240.

    Article  PubMed  Google Scholar 

  • Glazebrook, C. M., Elliott, D., & Lyons, J. (2006). A kinematic analysis of how young adults with and without autism plan and control goal-directed movements. Motor Control-Champaign, 10, 244.

    Article  Google Scholar 

  • Gowen, E., & Hamilton, A. (2013). Motor abilities in autism: A review using a computational context. Journal of Autism and Developmental Disorders, 43, 323–344. doi:10.1007/s10803-012-1574-0.

    Article  PubMed  Google Scholar 

  • Green, D., Baird, G., Barnett, A. L., Henderson, L., Huber, J., & Henderson, S. E. (2002). The severity and nature of motor impairment in Asperger’s syndrome: A comparison with specific developmental disorder of motor function. Journal of Child Psychology and Psychiatry, 43, 655–668.

    Article  PubMed  Google Scholar 

  • Hessl, D., Nguyen, D. V., Green, C., Chavez, A., Tassone, F., Hagerman, R. J., et al. (2009). A solution to limitations of cognitive testing in children with intellectual disabilities: The case of fragile X syndrome. Journal of Neurodevelopmental Disorders, 1, 33–45. doi:10.1007/s11689-008-9001-8.

    Article  PubMed  Google Scholar 

  • Hoppenbrouwers, S. S., Schutter, D. J., Fitzgerald, P. B., Chen, R., & Daskalakis, Z. J. (2008). The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: A review. Brain Research Reviews, 59, 185–200.

    Article  PubMed  Google Scholar 

  • Ivry, R. B., Keele, S., & Diener, H. (1988). Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale, 73, 167–180.

    Article  PubMed  Google Scholar 

  • Ivry, R. B., & Spencer, R. M. (2004). The neural representation of time. Current Opinion in Neurobiology, 14, 225–232.

    Article  PubMed  Google Scholar 

  • Kemper, T. L., & Bauman, M. (1998). Neuropathology of infantile autism. Journal of Neuropathology and Experimental Neurology. 57, 645–652.

    Article  PubMed  Google Scholar 

  • Kirby, A., Sugden, D., & Purcell, C. (2014). Diagnosing developmental coordination disorders. Archives of Disease in Childhood, 99, 292–296. doi:10.1136/archdischild-2012-303569.

    Article  PubMed  Google Scholar 

  • La Malfa, G., Lassi, S., Bertelli, M., Salvini, R., & Placidi, G. (2004). Autism and intellectual disability: A study of prevalence on a sample of the Italian population. Journal of Intellectual Disability Research, 48, 262–267.

    Article  PubMed  Google Scholar 

  • Lewis, P. A., & Miall, R. C. (2003). Distinct systems for automatic and cognitively controlled time measurement: Evidence from neuroimaging. Current Opinion in Neurobiology, 13, 250–255.

    Article  PubMed  Google Scholar 

  • Loras, H., Stensdotter, A. K., Ohberg, F., & Sigmundsson, H. (2013). Individual differences in motor timing and its relation to cognitive and fine motor skills. PLoS ONE, 8, e69353. doi:10.1371/journal.pone.0069353.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marco, E. J., Hinkley, L. B., Hill, S. S., & Nagarajan, S. S. (2011). Sensory processing in autism: A review of neurophysiologic findings. Pediatric Research, 69, 48r–54r. doi:10.1203/PDR.0b013e3182130c54.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marko, M. K., Crocetti, D., Hulst, T., Donchin, O., Shadmehr, R., & Mostofsky, S. H. (2015). Behavioural and neural basis of anomalous motor learning in children with autism. Brain, 138, 784–797. doi:10.1093/brain/awu394.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin, R., Tigera, C., Denckla, M. B., E. MARK MAHONE (2010). Factor structure of paediatric timed motor examination and its relationship with IQ. Developmental medicine and child neurology 52.

  • Maschke, M., Gomez, C. M., Ebner, T. J., & Konczak, J. (2004). Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. Journal of neurophysiology, 91, 230–238.

    Article  PubMed  Google Scholar 

  • Mates, J. (1994). A model of synchronization of motor acts to a stimulus sequence. Biological cybernetics, 70, 463–473.

    Article  PubMed  Google Scholar 

  • Matson, J. L., Dempsey, T., & Fodstad, J. C. (2009). The effect of Autism Spectrum Disorders on adaptive independent living skills in adults with severe intellectual disability. Research in developmental disabilities, 30, 1203–1211. doi:10.1016/j.ridd.2009.04.001.

    Article  PubMed  Google Scholar 

  • Mauk, M., Medina, J., Nores, W., & Ohyama, T. (2000). Cerebellar function: coordination, learning or timing? Current biology: CB, 10, R522-R525.

    Article  Google Scholar 

  • Medina, J. F. (2011). The multiple roles of Purkinje cells in sensori-motor calibration: to predict, teach and command. Current opinion in neurobiology, 21, 616–622.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mosconi, M. W., et al. (2013). Saccade adaptation abnormalities implicate dysfunction of cerebellar-dependent learning mechanisms in Autism Spectrum Disorders (ASD). PLoS One, 8, e63709. doi:10.1371/journal.pone.0063709.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mosconi, M. W., Mohanty, S., Greene, R. K., Cook, E. H., Vaillancourt, D. E., & Sweeney, J. A. (2015). Feedforward and feedback motor control abnormalities implicate cerebellar dysfunctions in autism spectrum disorder. The Journal of neuroscience: the official journal of the Society for Neuroscience 35.

  • Mosconi, M. W., & Sweeney, J. A. (2015). Sensorimotor dysfunctions as primary features of autism spectrum disorders. Sci China Life Sci, 58, 1016–1023. doi:10.1007/s11427-015-4894-4.

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller, F., & Dichgans, J. (1994). Dyscoordination of pinch and lift forces during grasp in patients with cerebellar lesions. Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale, 101, 485–492.

    Article  PubMed  Google Scholar 

  • Nazarali, N., Glazebrook, C. M., & Elliott, D. (2009). Movement planning and reprogramming in individuals with autism. Journal of Autism and Developmental Disorders, 39, 1401–1411.

    Article  PubMed  Google Scholar 

  • Ohmae, S., Uematsu, A., & Tanaka, M. (2013). Temporally specific sensory signals for the detection of stimulus omission in the primate deep cerebellar nuclei. The Journal of Neuroscience, 33, 15432–15441.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., Young, G. S., Goldring, S., Greiss-Hess, L., Herrera, A. M., Steele, J., et al. (2008). Gross motor development, movement abnormalities, and early identification of autism. Journal of Autism and Developmental Disorders, 38, 644–656.

    Article  PubMed  Google Scholar 

  • Ozonoff, S., Rogers, S. J., Farnham, J. M., & Pennington, B. F. (1993). Can standard measures identify subclinical markers of autism?. Journal of autism and developmental disorders, 23, 429–441.

    Article  PubMed  Google Scholar 

  • Pencina, M. J., D’Agostino, R. B., & Vasan, R. S. (2008). Evaluating the added predictive ability of a new marker: From area under the ROC curve to reclassification and beyond. Statistics in Medicine, 27, 157–172.

    Article  PubMed  Google Scholar 

  • Penhune, V. B., Zattore, R. J., & Evans, A. C. (1998). Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. Journal of Cognitive Neuroscience, 10, 752–765.

    Article  PubMed  Google Scholar 

  • Piochon, C., et al. (2014). Cerebellar plasticity and motor learning deficits in a copy-number variation mouse model of autism. Nature Communications, 5, 5586. doi:10.1038/ncomms6586.

    Article  PubMed  PubMed Central  Google Scholar 

  • Postorino, V., et al. (2016). Intellectual disability in Autism Spectrum Disorder: Investigation of prevalence in an Italian sample of children and adolescents. Research in Developmental Disabilities, 48, 193–201.

    Article  PubMed  Google Scholar 

  • Provost, B., Lopez, B. R., & Heimerl, S. (2007). A comparison of motor delays in young children: autism spectrum disorder, developmental delay, and developmental concerns. Journal of Autism and Developmental Disorders, 37, 321–328.

    Article  PubMed  Google Scholar 

  • Rao, S. M., Harrington, D. L., Haaland, K. Y., Bobholz, J. A., Cox, R. W., & Binder, J. R. (1997). Distributed neural systems underlying the timing of movements. The Journal of Neuroscience, 17, 5528–5535.

    PubMed  Google Scholar 

  • Raymond, J. L., Lisberger, S. G., & Mauk, M. D. (1996). The cerebellum: A neuronal learning machine? Science, 272, 1126–1131.

    Article  PubMed  Google Scholar 

  • Repp, B. H., & Su, Y. H. (2013). Sensorimotor synchronization: A review of recent research (2006–2012). Psychonomic Bulletin & Review, 20, 403–452. doi:10.3758/s13423-012-0371-2.

    Article  Google Scholar 

  • Rinehart, N. J., et al. (2006). Gait function in newly diagnosed children with autism: cerebellar and basal ganglia related motor disorder. Developmental Medicine and Child Neurology, 48, 819–824.

    Article  PubMed  Google Scholar 

  • Sano, Y., et al. (2016). Quantifying Parkinson’s disease finger-tapping severity by extracting and synthesizing finger motion properties. Medical & Biological Engineering & Computing, 54, 953–965.

    Article  Google Scholar 

  • Schwartze, M., Keller, P. E., & Kotz, S. A. (2016). Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients. Behavioural Brain Research, 312, 285–293.

    Article  PubMed  Google Scholar 

  • Serrien, D. J., & Wiesendanger, M. (1999). Grip-load force coordination in cerebellar patients. Experimental Brain Research. Experimentelle Hirnforschung. Experimentation Cerebrale, 128, 76–80.

    Article  PubMed  Google Scholar 

  • Shima, K., Tsuji, T., Kandori, A., Yokoe, M., & Sakoda, S. (2009). Measurement and evaluation of finger tapping movements using log-linearized Gaussian mixture networks. Sensors, 9, 2187–2201.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stanley-Cary, C., Rinehart, N., Tonge, B., White, O., & Fielding, J. (2011). Greater disruption to control of voluntary saccades in autistic disorder than Asperger’s disorder: evidence for greater cerebellar involvement in autism? Cerebellum, 10, 70–80. doi:10.1007/s12311-010-0229-y.

    Article  PubMed  Google Scholar 

  • Takarae, Y., Minshew, N., Luna, B., & Sweeney, J. (2004a). Oculomotor abnormalities parallel cerebellar histopathology in autism. Journal of Neurology, Neurosurgery, and Psychiatry, 75, 1359–1361.

    Article  PubMed  PubMed Central  Google Scholar 

  • Takarae, Y., Minshew, N. J., Luna, B., Krisky, C. M., & Sweeney, J. A. (2004b). Pursuit eye movement deficits in autism. Brain, 127, 2584–2594. doi:10.1093/brain/awh307.

    Article  PubMed  Google Scholar 

  • Thaut, M. H., & Kenyon, G. P. (2003). Rapid motor adaptations to subliminal frequency shifts during syncopated rhythmic sensorimotor synchronization. Human Movement Science, 22, 321–338.

    Article  PubMed  Google Scholar 

  • Thaut, M. H., Miller, R. A., & Schauer, L. M. (1998). Multiple synchronization strategies in rhythmic sensorimotor tasks: Phase vs period correction. Biological Cybernetics, 79, 241–250.

    Article  PubMed  Google Scholar 

  • Théoret, H., Haque, J., & Pascual-Leone, A. (2001). Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neuroscience Letters, 306, 29–32.

    Article  PubMed  Google Scholar 

  • Tsai, P. T., et al. (2012). Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature, 488, 647–651.

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Fels, I. M., te Wierike, S. C., Hartman, E., Elferink-Gemser, M. T., Smith, J., & Visscher, C. (2015). The relationship between motor skills and cognitive skills in 4–16 year old typically developing children: A systematic review. Journal of Science and Medicine in Sport/Sports Medicine Australia, 18, 697–703.

    Article  Google Scholar 

  • Vernazza-Martin, S., et al. (2005). Goal directed locomotion and balance control in autistic children. Journal of Autism and Developmental Disorders, 35, 91–102.

    Article  PubMed  Google Scholar 

  • Wang, Z., Magnon, G. C., White, S. P., Greene, R. K., Vaillancourt, D. E., & Mosconi, M. W. (2015). Individuals with autism spectrum disorder show abnormalities during initial and subsequent phases of precision gripping. Journal of Neurophysiology, 113, 1989–2001.

    Article  PubMed  Google Scholar 

  • Wing, A. M., & Kristofferson, A. B. (1973). Response delays and the timing of discrete motor responses. Perception & Psychophysics, 14, 5–12.

    Article  Google Scholar 

  • Wolpert, D. M., Miall, R. C., & Kawato, M. (1998). Internal models in the cerebellum. Trends in Cognitive Sciences, 2, 338–347.

    Article  PubMed  Google Scholar 

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Acknowledgments

We gratefully acknowledge the cooperation of all participants and their families, and also the school officials involved in this study. We thank K. Hashimoto, M. Kakehashi, K. Yamaoka, M. Walters, Y. Ohnishi, and members of Okamura’s lab for their helpful advice and discussions. We also thank Rachel James, Ph.D., from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

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The authors did not receive any financial support for this study.

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CM and HO desinged the study. KS contributed the experimental tool. CM performed the data collection. CM and EH analyzed the data. CM, EH, KS and HO wrote the paper.

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Correspondence to Hitoshi Okamura.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee, and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Morimoto, C., Hida, E., Shima, K. et al. Temporal Processing Instability with Millisecond Accuracy is a Cardinal Feature of Sensorimotor Impairments in Autism Spectrum Disorder: Analysis Using the Synchronized Finger-Tapping Task. J Autism Dev Disord 48, 351–360 (2018). https://doi.org/10.1007/s10803-017-3334-7

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