Auditory rhythm facilitates perception and action in children at risk for developmental coordination disorder.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 May 2024
28 May 2024
Historique:
received:
08
12
2023
accepted:
15
05
2024
medline:
29
5
2024
pubmed:
29
5
2024
entrez:
28
5
2024
Statut:
epublish
Résumé
Developmental Coordination Disorder (DCD) is a common neurodevelopmental disorder featuring deficits in motor coordination and motor timing among children. Deficits in rhythmic tracking, including perceptually tracking and synchronizing action with auditory rhythms, have been studied in a wide range of motor disorders, providing a foundation for developing rehabilitation programs incorporating auditory rhythms. We tested whether DCD also features these auditory-motor deficits among 7-10 year-old children. In a speech recognition task with no overt motor component, modulating the speech rhythm interfered more with the performance of children at risk for DCD than typically developing (TD) children. A set of auditory-motor tapping tasks further showed that, although children at risk for DCD performed worse than TD children in general, the presence of an auditory rhythmic cue (isochronous metronome or music) facilitated the temporal consistency of tapping. Finally, accuracy in the recognition of rhythmically modulated speech and tapping consistency correlated with performance on the standardized motor assessment. Together, the results show auditory rhythmic regularity benefits auditory perception and auditory-motor coordination in children at risk for DCD. This provides a foundation for future clinical studies to develop evidence-based interventions involving auditory-motor rhythmic coordination for children with DCD.
Identifiants
pubmed: 38806554
doi: 10.1038/s41598-024-62322-6
pii: 10.1038/s41598-024-62322-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
12203Informations de copyright
© 2024. The Author(s).
Références
American Psychiatric Association. Diagnostic and statistical manual of mental disorders (5th ed.). https://doi.org/10.1176/appi.books.9780890425596 (2013)
Wilson, P. H. et al. Cognitive and neuroimaging findings in developmental coordination disorder: New insights from a systematic review of recent research. Dev. Med. Child Neurol. 59, 1117–1129 (2017).
pubmed: 28872667
doi: 10.1111/dmcn.13530
Bulten, R., Brown, D., Rodriguez, M. & Cairney, J. Effects of sedentary behaviour on internalizing problems in children with and without motor coordination problems. Mental Health Phys. Activity 18, 100325 (2020).
doi: 10.1016/j.mhpa.2020.100325
Cairney, J., Veldhuizen, S. & Szatmari, P. Motor coordination and emotional–behavioral problems in children. Curr. Opin. Psychiatry 23, 324–329 (2010).
pubmed: 20520549
doi: 10.1097/YCO.0b013e32833aa0aa
Cairney, J., Rigoli, D. & Piek, J. Developmental coordination disorder and internalizing problems in children: The environmental stress hypothesis elaborated. Dev. Rev. 33, 224–238 (2013).
doi: 10.1016/j.dr.2013.07.002
Lingam, R. et al. Mental health difficulties in children with developmental coordination disorder. Pediatrics 129, e882-891 (2012).
pubmed: 22451706
doi: 10.1542/peds.2011-1556
Rivilis, I. et al. Physical activity and fitness in children with developmental coordination disorder: A systematic review. Res. Dev. Disabil. 32, 894–910 (2011).
pubmed: 21310588
doi: 10.1016/j.ridd.2011.01.017
Kirby, A., Sugden, D. & Purcell, C. Diagnosing developmental coordination disorders. Arch. Dis. Child 99, 292–296 (2014).
pubmed: 24255567
doi: 10.1136/archdischild-2012-303569
Volman, M. & Geuze, R. H. Relative phase stability of bimanual and visuomanual rhythmic coordination patterns in children with a developmental coordination disorder. Human Movem. Sci. 17, 541–572 (1998).
doi: 10.1016/S0167-9457(98)00013-X
de Castelnau, P., Albaret, J.-M., Chaix, Y. & Zanone, P.-G. Developmental coordination disorder pertains to a deficit in perceptuo-motor synchronization independent of attentional capacities. Hum. Mov. Sci. 26, 477–490 (2007).
pubmed: 17475354
doi: 10.1016/j.humov.2007.03.001
Debrabant, J., Gheysen, F., Caeyenberghs, K., Van Waelvelde, H. & Vingerhoets, G. Neural underpinnings of impaired predictive motor timing in children with developmental coordination disorder. Res. Dev. Disabil. 34, 1478–1487 (2013).
pubmed: 23474999
doi: 10.1016/j.ridd.2013.02.008
Subara-Zukic, E. et al. Behavioral and neuroimaging research on developmental coordination disorder (DCD): A combined systematic review and meta-analysis of recent findings. Front. Psychol. https://doi.org/10.3389/fpsyg.2022.809455 (2022).
doi: 10.3389/fpsyg.2022.809455
pubmed: 35153960
pmcid: 8829815
Tran, H.-T., Li, Y.-C., Lin, H.-Y., Lee, S.-D. & Wang, P.-J. Sensory processing impairments in children with developmental coordination disorder. Children 9, 1443 (2022).
pubmed: 36291382
pmcid: 9600147
doi: 10.3390/children9101443
Estil, L., Ingvaldsen, R. & Whiting, H. Spatial and temporal constraints on performance in children with movement co-ordination problems. Exp. Brain Res. 147, 153–161 (2002).
pubmed: 12410330
doi: 10.1007/s00221-002-1193-7
Purcell, C., Wilmut, K. & Wann, J. P. The use of visually guided behaviour in children with developmental coordination disorder (DCD) when crossing a virtual road. Hum. Mov. Sci. 53, 37–44 (2017).
pubmed: 27939726
doi: 10.1016/j.humov.2016.11.007
Blais, M., Amarantini, D., Albaret, J.-M., Chaix, Y. & Tallet, J. Atypical inter-hemispheric communication correlates with altered motor inhibition during learning of a new bimanual coordination pattern in developmental coordination disorder. Dev. Sci. 21, e12563 (2018).
pubmed: 28440058
doi: 10.1111/desc.12563
Lê, M. et al. Procedural learning and retention of audio-verbal temporal sequence is altered in children with developmental coordination disorder but cortical thickness matters. Dev. Sci. 24, e13009 (2021).
pubmed: 32573893
doi: 10.1111/desc.13009
Cannon, J. J. & Patel, A. D. How beat perception co-opts motor neurophysiology. Trends Cogn. Sci. 25, 137–150 (2021).
pubmed: 33353800
doi: 10.1016/j.tics.2020.11.002
Fujioka, T., Trainor, L. J., Large, E. W. & Ross, B. Internalized timing of isochronous sounds is represented in neuromagnetic beta oscillations. J. Neurosci. 32, 1791–1802 (2012).
pubmed: 22302818
pmcid: 6703342
doi: 10.1523/JNEUROSCI.4107-11.2012
Patel, A. D. & Iversen, J. R. The evolutionary neuroscience of musical beat perception: The action simulation for auditory prediction (ASAP) hypothesis. Front. Syst. Neurosci. https://doi.org/10.3389/fnsys.2014.00057 (2014).
doi: 10.3389/fnsys.2014.00057
pubmed: 24860439
pmcid: 4026735
Grahn, J. A. & Brett, M. Rhythm and beat perception in motor areas of the brain. J. Cogn. Neurosci. 19, 893–906 (2007).
pubmed: 17488212
doi: 10.1162/jocn.2007.19.5.893
Morillon, B. & Baillet, S. Motor origin of temporal predictions in auditory attention. Proc. Nat. Acad. Sci. 114, E8913–E8921 (2017).
pubmed: 28973923
pmcid: 5651745
doi: 10.1073/pnas.1705373114
Nozaradan, S., Zerouali, Y., Peretz, I. & Mouraux, A. Capturing with EEG the neural entrainment and coupling underlying sensorimotor synchronization to the beat. Cereb. Cortex 25, 736–747 (2015).
pubmed: 24108804
doi: 10.1093/cercor/bht261
Lima, C. F., Krishnan, S. & Scott, S. K. Roles of supplementary motor areas in auditory processing and auditory imagery. Trends Neurosci. 39, 527–542 (2016).
pubmed: 27381836
pmcid: 5441995
doi: 10.1016/j.tins.2016.06.003
Chang, A. et al. Inferior auditory time perception in children with motor difficulties. Child Dev. https://doi.org/10.1111/cdev.13537 (2021).
doi: 10.1111/cdev.13537
pubmed: 34291830
pmcid: 8599623
Cirelli, L. K., Einarson, K. M. & Trainor, L. J. Interpersonal synchrony increases prosocial behavior in infants. Dev. Sci. 17, 1003–1011 (2014).
pubmed: 25513669
doi: 10.1111/desc.12193
Stupacher, J., Mikkelsen, J. & Vuust, P. Higher empathy is associated with stronger social bonding when moving together with music. Psychol. Music 50, 1511–1526 (2022).
pubmed: 36097608
doi: 10.1177/03057356211050681
Wiltermuth, S. S. & Heath, C. Synchrony and cooperation. Psychol. Sci. 20, 1–5 (2009).
pubmed: 19152536
doi: 10.1111/j.1467-9280.2008.02253.x
Trainor, L. J., Chang, A., Cairney, J. & Li, Y.-C. Is auditory perceptual timing a core deficit of developmental coordination disorder?. Ann. N. Y. Acad. Sci. https://doi.org/10.1111/nyas.13701 (2018).
doi: 10.1111/nyas.13701
pubmed: 29741273
pmcid: 6099217
Rosenblum, S. & Regev, N. Timing abilities among children with developmental coordination disorders (DCD) in comparison to children with typical development. Res. Dev. Disabil. 34, 218–227 (2013).
pubmed: 22960066
doi: 10.1016/j.ridd.2012.07.011
Williams, H. G., Woollacott, M. H. & Ivry, R. Timing and motor control in clumsy children. J. Motor Behav. 24, 165–172 (1992).
doi: 10.1080/00222895.1992.9941612
Whitall, J. et al. Auditory-motor coupling of bilateral finger tapping in children with and without DCD compared to adults. Human Mov. Sci. 27, 914–931 (2008).
doi: 10.1016/j.humov.2007.11.007
Puyjarinet, F., Bégel, V., Lopez, R., Dellacherie, D. & Dalla Bella, S. Children and adults with attention-deficit/hyperactivity disorder cannot move to the beat. Sci. Rep. 7, 11550 (2017).
pubmed: 28912422
pmcid: 5599521
doi: 10.1038/s41598-017-11295-w
Adams, I. L. J., Lust, J. M., Wilson, P. H. & Steenbergen, B. Compromised motor control in children with DCD: a deficit in the internal model?—A systematic review. Neurosci. Biobehav. Rev. 47, 225–244 (2014).
pubmed: 25193246
doi: 10.1016/j.neubiorev.2014.08.011
Repp, B. H. Tapping in synchrony with a perturbed metronome: The phase correction response to small and large phase shifts as a function of tempo. J. Motor Behav. 43, 213–227 (2011).
doi: 10.1080/00222895.2011.561377
Large, E. W. & Jones, M. R. The dynamics of attending: How people track time-varying events. Psychol. Rev. 106, 119–159 (1999).
doi: 10.1037/0033-295X.106.1.119
Haegens, S. & Zion Golumbic, E. Rhythmic facilitation of sensory processing: A critical review. Neurosci. Biobehav. Rev. 86, 150–165 (2018).
pubmed: 29223770
doi: 10.1016/j.neubiorev.2017.12.002
Poeppel, D. & Assaneo, M. F. Speech rhythms and their neural foundations. Nat. Rev. Neurosci. 21, 322–334 (2020).
pubmed: 32376899
doi: 10.1038/s41583-020-0304-4
Damm, L., Varoqui, D., De Cock, V. C., Dalla Bella, S. & Bardy, B. Why do we move to the beat? A multi-scale approach, from physical principles to brain dynamics. Neurosci. Biobeh. Rev. 112, 553–584 (2020).
doi: 10.1016/j.neubiorev.2019.12.024
Corriveau, K. H. & Goswami, U. Rhythmic motor entrainment in children with speech and language impairments: Tapping to the beat. Cortex 45, 119–130 (2009).
pubmed: 19046744
doi: 10.1016/j.cortex.2007.09.008
McAuley, J. D., Shen, Y., Dec, S. & Kidd, G. R. Altering the rhythm of target and background talkers differentially affects speech understanding. Atten. Percept Psychophys. 82, 3222–3233 (2020).
pubmed: 32458224
pmcid: 10575213
doi: 10.3758/s13414-020-02064-5
McAuley, J. D., Shen, Y., Smith, T. & Kidd, G. R. Effects of speech-rhythm disruption on selective listening with a single background talker. Atten. Percept Psychophys. https://doi.org/10.3758/s13414-021-02298-x (2021).
doi: 10.3758/s13414-021-02298-x
pubmed: 33782913
Wilson, P. H., Ruddock, S., Smits-Engelsman, B., Polatajko, H. & Blank, R. Understanding performance deficits in developmental coordination disorder: a meta-analysis of recent research. Dev. Med. Child Neurol. 55, 217–228 (2013).
pubmed: 23106668
doi: 10.1111/j.1469-8749.2012.04436.x
Cairney, J. et al. The coordination and activity tracking in children (CATCH) study: Rationale and design. BMC Public Health 15, 1266 (2015).
pubmed: 26692206
pmcid: 4687347
doi: 10.1186/s12889-015-2582-8
Blank, R., Smits-Engelsman, B., Polatajko, H., Wilson, P., European Academy for Childhood Disability. European academy for childhood disability (EACD): Recommendations on the definition, diagnosis and intervention of developmental coordination disorder (long version). Dev. Med. Child Neurol. 54, 54–93 (2012).
pubmed: 22171930
doi: 10.1111/j.1469-8749.2011.04171.x
Cairney, J. et al. Cohort profile: the Canadian coordination and activity tracking in children (CATCH) longitudinal cohort. BMJ Open 9, e029784 (2019).
pubmed: 31501117
pmcid: 6738750
doi: 10.1136/bmjopen-2019-029784
Bolia, R., Nelson, W., Ericson, M. & Simpson, B. A speech corpus for multitalker communications research. J. Acoustical Soc. Am. 107, 1065–1066 (2000).
doi: 10.1121/1.428288
Iversen, J. & Patel, A. The Beat Alignment Test (BAT): Surveying beat processing abilities in the general population. Proceedings of the 10{th International Conference on Music Perception and Cognition (ICMPC10) (2008).
Kaufman, A. S., Flanagan, D. P., Alfonso, V. C. & Mascolo, J. T. Review of wechsler intelligence scale for children fourth edition (WISC-IV). J. Psychoedu. Ass. 24, 278–295 (2006).
doi: 10.1177/0734282906288389
Wechsler, D. Wechsler Intelligence Scale for Children, 4th Edn. PsychCorp. (2003).
Conners, C. K., Sitarenios, G., Parker, J. D. A. & Epstein, J. N. The revised conners’ parent rating scale (CPRS-R): Factor structure, reliability, and criterion validity. J. Abnorm. Child Psychol. 26, 257–268 (1998).
pubmed: 9700518
doi: 10.1023/A:1022602400621
Dalla Bella, S. et al. BAASTA: Battery for the assessment of auditory sensorimotor and timing abilities. Behav. Res. 49, 1128–1145 (2017).
doi: 10.3758/s13428-016-0773-6
Falk, S., Müller, T. & Dalla Bella, S. Non-verbal sensorimotor timing deficits in children and adolescents who stutter. Front. Psychol. https://doi.org/10.3389/fpsyg.2015.00847 (2015).
doi: 10.3389/fpsyg.2015.00847
pubmed: 26217245
pmcid: 4491603
Ip, A., Mickelson, E. C. R. & Zwicker, J. G. Assessment, diagnosis, and management of developmental coordination disorder. Paediatr. Child Health 26, 375–378 (2021).
pubmed: 34552678
pmcid: 8448494
doi: 10.1093/pch/pxab047
Mcauley, J., Jones, M., Holub, S., Johnston, H. & Miller, N. The time of our lives: Life span development of timing and event tracking. J. Exp. Psychol. General 135, 348–367 (2006).
doi: 10.1037/0096-3445.135.3.348
Ireland, K., Parker, A., Foster, N. & Penhune, V. Rhythm and melody tasks for school-aged children with and without musical training: Age-equivalent scores and reliability. Front. Psychol. https://doi.org/10.3389/fpsyg.2018.00426 (2018).
doi: 10.3389/fpsyg.2018.00426
pubmed: 29867676
pmcid: 5962787
Barbato, G., Barini, E. M., Genta, G. & Levi, R. Features and performance of some outlier detection methods. J. Appl. Stat. 38, 2133–2149 (2011).
doi: 10.1080/02664763.2010.545119
Thaut, M. H. & Abiru, M. Rhythmic auditory stimulation in rehabilitation of movement disorders: A review of current research. Music Percep. 27, 263–269 (2010).
doi: 10.1525/mp.2010.27.4.263
Thompson, E. C., White-Schwoch, T., Tierney, A. & Kraus, N. Beat synchronization across the lifespan: Intersection of development and musical experience. PLOS ONE 10, e0128839 (2015).
pubmed: 26107927
pmcid: 4481101
doi: 10.1371/journal.pone.0128839
Carrer, L. R. J., Pompéia, S. & Miranda, M. C. Sensorimotor synchronization with music and metronome in school-aged children. Psychol. Music https://doi.org/10.1177/03057356221100286 (2022).
doi: 10.1177/03057356221100286
Flaugnacco, E. et al. Music training increases phonological awareness and reading skills in developmental dyslexia: A randomized control trial. PLOS ONE 10, e0138715 (2015).
pubmed: 26407242
pmcid: 4583182
doi: 10.1371/journal.pone.0138715
Fujii, S. & Schlaug, G. The harvard beat assessment test (H-BAT): A Battery for assessing beat perception and production and their dissociation. Front. Human Neurosci. 7, 771 (2013).
doi: 10.3389/fnhum.2013.00771
Lense, M. D., Ladányi, E., Rabinowitch, T.-C., Trainor, L. & Gordon, R. Rhythm and timing as vulnerabilities in neurodevelopmental disorders. Philos. Trans. Royal Soc. B Biol. Sci. 376, 20200327 (2021).
doi: 10.1098/rstb.2020.0327
Lino, F. & Chieffo, D. P. R. Developmental coordination disorder and most prevalent comorbidities: A narrative review. Children (Basel) 9, 1095 (2022).
pubmed: 35884081
Paquet, A., Olliac, B., Golse, B. & Vaivre-Douret, L. Nature of motor impairments in autism spectrum disorder: A comparison with developmental coordination disorder. J. Clin. Exp. Neuropsychol. 41, 1–14 (2019).
pubmed: 29923455
doi: 10.1080/13803395.2018.1483486
Thomson, J. & Goswami, U. Rhythmic processing in children with developmental dyslexia: Auditory and motor rhythms link to reading and spelling. J. physiol. Paris 102, 120–129 (2008).
pubmed: 18448317
doi: 10.1016/j.jphysparis.2008.03.007