Developmental Trajectories of Hand Movements in Typical Infants and Those at Risk of Developmental Disorders: An Observational Study of Kinematics during the First Year of Life.
Ouss, Lisa; Le Normand, Marie-Thérèse; Bailly, Kevinet al.
developmental trajectories; early hospitalization; hand movement; infant at risk; orality disorder; preterm; visually impaired mother; west syndrome
Abstract :
[en] Highlights The kinematics of hand movements (spatial use, curvature, acceleration, and velocity) of infants with their mothers in an interactive setting are significantly associated with age in cohorts of typical and at-risk infantsdiffer significantly at 5-6 months of age, depending on the context: relating either with an object or a person.Environmental and developmental factors shape the developmental trajectories of hand movements in different cohorts: environment for infants with VIMs; stage of development for premature infants and those with West syndrome; and both factors for infants with orality disorders.The curvature of hand movements specifically reflects atypical development in infants with West syndrome when developmental age is considered. We aimed to discriminate between typical and atypical developmental trajectory patterns of at-risk infants in an interactive setting in this observational and longitudinal study, with the assumption that hand movements (HM) reflect preverbal communication and its disorders. We examined the developmental trajectories of HM in five cohorts of at-risk infants and one control cohort, followed from ages 2 to 10 months: 25 West syndrome (WS), 13 preterm birth (PB), 16 orality disorder (OD), 14 with visually impaired mothers (VIM), 7 early hospitalization (EH), and 19 typically developing infants (TD). Video-recorded data were collected in three different structured interactive contexts. Descriptors of the hand motion were used to examine the extent to which HM were associated with age and cohort. We obtained four principal results: (i) the kinematics of HM (spatial use, curvature, acceleration, and velocity) were significantly associated with age in all cohorts; (ii) HM significantly differed at 5-6 months of age in TD infants, depending on the context; (iii) environmental and developmental factors shaped the developmental trajectories of HM in different cohorts: environment for VIM, development for PB and WS, and both factors for OD and; (iv) the curvatures of HM showed atypical development in WS infants when developmental age was considered. These findings support the importance of using kinematics of HM to identify very early developmental disorders in an interactive context and would allow early prevention and intervention for at-risk infants.
Disciplines :
Psychiatry
Author, co-author :
Ouss, Lisa ; Department of Child and Adolescent Psychiatry, Necker-Enfants-Malades Hospital, APHP Assistance Publique-Hopitaux De Paris, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France. ; UMR 1129 Infantile Epilepsies and Brain Plasticity, Institut National de la Santé et de la Recherche Médicale, CEA, Université Paris Descartes, Paris, France.
Le Normand, Marie-Thérèse; Institut National de la Santé et de la Recherche Médicale & Laboratoire de Psychopathologie et Processus de Santé, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France.
Bailly, Kevin; Institut des Systèmes Intelligents et de Robotique, Centre National de la Recherche Scientifique UMR 7222, Université Pierre et Marie Curie Univ Paris 06, Sorbonne Universités, Paris, France.
Leitgel Gille, Marluce; Department of Child and Adolescent Psychiatry, Necker-Enfants-Malades Hospital, APHP Assistance Publique-Hopitaux De Paris, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France.
Gosme, Christelle; Department of Child and Adolescent Psychiatry, Necker-Enfants-Malades Hospital, APHP Assistance Publique-Hopitaux De Paris, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France.
Simas, Roberta; Department of Child and Adolescent Psychiatry, Necker-Enfants-Malades Hospital, APHP Assistance Publique-Hopitaux De Paris, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France.
Wenke, Julia; EA 3522, CRPMS, ED 450 Recherches en Psychanalyse et Psychopathologie, Université Paris Diderot, Université Sorbonne Paris Cité, Paris, France.
Jeudon, Xavier; Cellule Vidéo de l'Hôpital Necker Enfants Malades, Association A l'Aube de la Vie, Paris, France.
Thepot, Stéphanie; Ariana Pharmaceuticals, Paris, France.
Da Silva, Telma; Ariana Pharmaceuticals, Paris, France.
Clady, Xavier; Department of Visual Information, Vision Institute, Centre National de la Recherche Scientifique UMR S968, Institut National de la Santé et de la Recherche Médicale UMRS 7210, Université Pierre et Marie Curie Univ Paris 06, Sorbonne Universités, Paris, France.
Thoueille, Edith; SAPPH, Fondation Hospitalière Sainte Marie, Paris, France.
Afshar, Mohammad; Ariana Pharmaceuticals, Paris, France.
Golse, Bernard; Department of Child and Adolescent Psychiatry, Necker-Enfants-Malades Hospital, APHP Assistance Publique-Hopitaux De Paris, Université Paris Descartes, Université Sorbonne Paris Cité, Paris, France.
Guergova-Kuras, Mariana; Ariana Pharmaceuticals, Paris, France.
Developmental Trajectories of Hand Movements in Typical Infants and Those at Risk of Developmental Disorders: An Observational Study of Kinematics during the First Year of Life.
Adde, L., Helbostad, J. L., Jensenius, A. R., Taraldsen, G., and Støen, R. (2009). Using computer-based video analysis in the study of fidgety movements. Early Hum. Dev. 85, 541-547. doi: 10.1016/j.earlhumdev.2009.05.003
Adrien, J. L., Lenoir, P., Martineau, J., Perrot, A., Hameury, L., Larmande, C., et al. (1993). Blind ratings of early symptoms of autism based upon family home movies. J. Am. Acad. Child Adolesc. Psychiatry 32, 617-626. doi: 10.1097/00004583-199305000-00019
Ambady, N., and Rosenthal, R. (1992). Thin slices of expressive behavior as predictors of interpersonal consequences: a meta-analysis. Psychol. Bull. 111, 256-274. doi: 10.1037/0033-2909.111.2.256
Avril, M., Leclère, C., Viaux, S., Michelet, S., Achard, C., Missonnier, S., et al. (2014). Social signal processing for studying parent-infant interaction. Front. Psychol. 5:1437. doi: 10.3389/fpsyg.2014.01437
Beccaria, E., Martino, M., Briatore, E., Podestà, B., Pomero, G., Micciolo, R., et al. (2012). Poor repertoire General Movements predict some aspects of development outcome at 2 years in very preterm infants. Early Hum. Dev. 88, 393-396. doi: 10.1016/j.earlhumdev.2011.10.002
Beers, A. N., McBoyle, M., Kakande, E., Dar Santos, R. C., and Kozak, F. K. (2014). Autism and peripheral hearing loss: a systematic review. Int. J. Pediatr. Otorhinolaryngol. 78, 96-101. doi: 10.1016/j.ijporl.2013.10.063
Benasich, A. A., Choudhury, N. A., Realpe-Bonilla, T., and Roesler, C. P. (2014). Plasticity in developing brain: active auditory exposure impacts prelinguistic acoustic mapping. J. Neurosci. Off. J. Soc. Neurosci. 34, 13349-13363. doi: 10.1523/JNEUROSCI.0972-14.2014
Berthier, N. E., and Keen, R. (2006). Development of reaching in infancy. Exp. Brain Res. 169, 507-518. doi: 10.1007/s00221-005-0169-9
Bhat, A. N., and Galloway, J. C. (2006). Toy-oriented changes during early arm movements: hand kinematics. Infant Behav. Dev. 29, 358-372. doi: 10.1016/j.infbeh.2006.01.005
Bhat, A. N., Galloway, J. C., and Landa, R. J. (2012). Relation between early motor delay and later communication delay in infants at risk for autism. Infant Behav. Dev. 35, 838-846. doi: 10.1016/j.infbeh.2012.07.019
Crais, E., Douglas, D. D., and Campbell, C. C. (2004). The Intersection of the development of gestures and intentionality. J. Speech Lang. Hear. Res. 47, 678. doi: 10.1044/1092-4388(2004/052)
Czyz, J., Ristic, B., and Macq, B. (2005). "A color-based particle filter for joint detection and tracking of multiple objects," in ICASSP (Philadelphia), 217-220
D'Onofrio, B. M., Class, Q. A., Rickert, M. E., Larsson, H., Langstrom, N., and Lichtenstein, P. (2013). Preterm birth and mortality and morbidity: a population-based quasi-experimental study. JAMA Psychiatry 70, 1231-1240. doi: 10.1001/jamapsychiatry.2013.2107
D'Souza, H., and Karmiloff-Smith, A. (2017). Neurodevelopmental disorders. WIREs Cogn. Sci. 8:e1398. doi: 10.1002/wcs.1398
de'Sperati, C., and Viviani, P. (1997). The relationship between curvature and velocity in two-dimensional smooth pursuit eye movements. J. Neurosci. 17, 3932-3945
Einspieler, C., Marschik, P. B., Bos, A. F., Ferrari, F., Cioni, G., and Prechtl, H. F. (2012). Early markers for cerebral palsy: insights from the assessment of general movements. Future Neurol. 7, 709-717. doi: 10.2217/fnl.12.60
Esposito, G., Venuti, P., Maestro, S., and Muratori, F. (2009). An exploration of symmetry in early autism spectrum disorders: analysis of lying. Brain Dev. 31, 131-138. doi: 10.1016/j.braindev.2008.04.005
Fallang, B., Saugstad, O. D., and Hadders-Algra, M. (2000). Goal directed reaching and postural control in supine position in healthy infants. Behav. Brain Res. 115, 9-18. doi: 10.1016/S0166-4328(00)00231-X
Fucile, S., Gisel, E., and Lau, C. (2002). Oral stimulation accelerates the transition from tube to oral feeding in preterm infants. J. Pediatr. 141, 230-236. doi: 10.1067/mpd.2002.125731
Gentilucci, M., and Corballis, M. C. (2006). From manual gesture to speech: a gradual transition. Neurosci. Biobehav. Rev. 30, 949-960. doi: 10.1016/j.neubiorev.2006.02.004
Gima, H., Ohgi, S., Morita, S., Karasuno, H., Fujiwara, T., and Abe, K. (2011). A dynamical system analysis of the development of spontaneous lower extremity movements in newborn and young infants. J. Physiol. Anthropol. 30, 179-186. doi: 10.2114/jpa2.30.179
Gonçalves, R. V., Figueiredo, E. M., Mourão, C. B., Colosimo, E. A., Fonseca, S. T., and Mancini, M. C. (2013). Development of infant reaching behaviors: kinematic changes in touching and hitting. Infant Behav. Dev. 36, 825-832. doi: 10.1016/j.infbeh.2013.09.009
Goodwin, M. S., Intille, S. S., Albinali, F., and Velicer, W. F. (2011). Automated detection of stereotypical motor movements. J. Autism Dev. Disord. 41, 770-782. doi: 10.1007/s10803-010-1102-z
Guidetti, M., and Nicoladis, E. (2008). Introduction to special issue: gestures and communicative development. First Lang. 28, 107-115. doi: 10.1177/0142723708088914
Hadders-Algra, M. (2004). General movements: a window for early identification of children at high risk for developmental disorders. J. Pediatr. 145, S12-S18. doi: 10.1016/j.jpeds.2004.05.017
Hadders-Algra, M., and Groothuis, A. M. (1999). Quality of general movements in infancy is related to neurological dysfunction, ADHD, and aggressive behaviour. Dev. Med. Child Neurol. 41, 381-391. doi: 10.1017/S0012162299000845
Halverson, H. M. (1933). The acquisition of skill in infancy. Pedagog. Semin. J. Genet. Psychol. 43, 3-48. doi: 10.1080/08856559.1933.10533118
Hitzert, M. M., van Geert, P. L., Hunnius, S., Van Braeckel, K. N., Bos, A. F., and Geuze, R. H. (2015). Associations between developmental trajectories of movement variety and visual attention in fullterm and preterm infants during the first six months postterm. Early Hum. Dev. 91, 89-96. doi: 10.1016/j.earlhumdev.2014.12.006
Hue, C. (2003). Méthodes Séquentielles de Monte Carlo pour le Filtrage Non linéaire Multi-Objets Dans un Environnement Bruité. Applications au Pistage Multi-Cibles et à la Trajectographie D'entités Dans des Séquences D'images 2D. Ph. D., thesis, Université de Rennes 1
Isard, M., and Blake, A. (1998). Condensation-conditional density propagation for visual tracking. Int. J. Comput. Vis. 29, 5-28. doi: 10.1023/A:1008078328650
Ismail, F. Y., Fatemi, A., and Johnston, M. V. (2017). Cerebral plasticity: windows of opportunity in the developing brain. Eur. J. Paediatr. Neurol. EJPN Off. J. Eur. Paediatr. Neurol. Soc. 21, 23-48. doi: 10.1016/j.ejpn.2016.07.007
Iverson, J. M. (2010). Developing language in a developing body: the relationship between motor development and language development. J. Child Lang. 37, 229. doi: 10.1017/S0305000909990432
Iverson, J. M., and Goldin-Meadow, S. (2005). Gesture paves the way for language development. Psychol. Sci. 16, 367-371. doi: 10.1111/j.0956-7976.2005.01542.x
Josse, D. (1997). Brunet-Lézine Révisé. Issy les Moulineaux: ECPA
Karch, D., Kim, K.-S., Wochner, K., Pietz, J., Dickhaus, H., and Philippi, H. (2008). Quantification of the segmental kinematics of spontaneous infant movements. J. Biomech. 41, 2860-2867. doi: 10.1016/j.jbiomech.2008.06.033
Kodric, J., Sustersic, B., and Paro-Panjan, D. (2010). Assessment of general movements and 2.5 year developmental outcomes: pilot results in a diverse preterm group. Eur. J. Paediatr. Neurol. 14, 131-137. doi: 10.1016/j.ejpn.2009.04.012
Konczak, J., and Dichgans, J. (1997). The development toward stereotypic arm kinematics during reaching in the first 3 years of life. Exp. Brain Res. 117, 346-354. doi: 10.1007/s002210050228
Konczak, J., Borutta, M., Topka, H., and Dichgans, J. (1995). The development of goal-directed reaching in infants: hand trajectory formation and joint torque control. Exp. Brain Res. 106, 156-168. doi: 10.1007/BF00241365
Landa, R., and Garrett-Mayer, E. (2006). Development in infants with autism spectrum disorders: a prospective study. J. Child Psychol. Psychiatry 47, 629-638. doi: 10.1111/j.1469-7610.2006.01531.x
Leclère, C., Avril, M., Viaux-Savelon, S., Bodeau, N., Achard, C., Missonnier, S., et al. (2016). Interaction and behaviour imaging: a novel method to measure mother-infant interaction using video 3D reconstruction. Transl. Psychiatry 6, e816. doi: 10.1038/tp.2016.82
Lederman, S. J., and Klatzky, R. L. (1987). Hand movements: a window into haptic object recognition. Cogn. Psychol. 19, 342-368. doi: 10.1016/0010-0285(87)90008-9
Lee, M.-H., Ranganathan, R., and Newell, K. M. (2011). Changes in object-oriented arm movements that precede the transition to goal-directed reaching in infancy. Dev. Psychobiol. 53, 685-693. doi: 10.1002/dev.20541
Lobo, M. A., Kokkoni, E., Cunha, A. B., and Galloway, J. C. (2015). Infants born preterm demonstrate impaired object exploration behaviors throughout infancy and toddlerhood. Phys. Ther. 95, 51-64. doi: 10.2522/ptj.20130584
Lynch, A., Lee, H. M., Bhat, A., and Galloway, J. C. (2008). No stable arm preference during the pre-reaching period: a comparison of right and left hand kinematics with and without a toy present. Dev. Psychobiol. 50, 390-398. doi: 10.1002/dev.20297
Marcroft, C., Khan, A., Embleton, N. D., Trenell, M., and Plötz, T. (2014). Movement recognition technology as a method of assessing spontaneous general movements in high risk infants. Front. Neurol. 5:284. doi: 10.3389/fneur.2014.00284
Masten, A. S., and Cicchetti, D. (2010). Developmental cascades. Dev. Psychopathol. 22, 491-495. doi: 10.1017/S0954579410000222
Mathew, A., and Cook, M. (1990). The control of reaching movements by young infants. Child Dev. 61, 1238-1257. doi: 10.2307/1130891
Meinecke, L., Breitbach-Faller, N., Bartz, C., Damen, R., Rau, G., and Disselhorst-Klug, C. (2006). Movement analysis in the early detection of newborns at risk for developing spasticity due to infantile cerebral palsy. Hum. Mov. Sci. 25, 125-144. doi: 10.1016/j.humov.2005.09.012
Montgomery, K. J., Isenberg, N., and Haxby, J. V. (2007). Communicative hand gestures and object-directed hand movements activated the mirror neuron system. Soc. Cogn. Affect. Neurosci. 2, 114-122. doi: 10.1093/scan/nsm004
Mundy, P., Sullivan, L., and Mastergeorge, A. M. (2009). A parallel and distributed-processing model of joint attention, social cognition and autism. Autism Res. Off. J. Int. Soc. Autism Res. 2, 2-21. doi: 10.1002/aur.61
Ohgi, S., Morita, S., Loo, K. K., and Mizuike, C. (2008). Time series analysis of spontaneous upper-extremity movements of premature infants with brain injuries. Phys. Ther. 88, 1022-1033. doi: 10.2522/ptj.20070171
Ouss, L., Saint-Georges, C., Robel, L., Bodeau, N., Laznik, M.-C., Crespin, G. C., et al. (2014). Infant's engagement and emotion as predictors of autism or intellectual disability in West syndrome. Eur. Child Adolesc. Psychiatry 23, 143-149. doi: 10.1007/s00787-013-0430-x
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. J. Autism Dev. Disord. 38, 644-656. doi: 10.1007/s10803-007-0430-0
Peña, M., Arias, D., and Dehaene-Lambertz, G. (2014). Gaze following is accelerated in healthy preterm infants. Psychol. Sci. 25, 1884-1892. doi: 10.1177/0956797614544307
Phagava, H., Muratori, F., Einspieler, C., Maestro, S., Apicella, F., Guzzetta, A., et al. (2008). General movements in infants with autism spectrum disorders. Georgian Med. News, 156, 100-105
Philippi, H., Karch, D., Kang, K.-S., Wochner, K., Pietz, J., Dickhaus, H., et al. (2014). Computer-based analysis of general movements reveals stereotypies predicting cerebral palsy. Dev. Med. Child Neurol. 56, 960-967. doi: 10.1111/dmcn.12477
Prechtl, H. F. (1990). Qualitative changes of spontaneous movements in fetus and preterm infant are a marker of neurological dysfunction. Early Hum. Dev. 23, 151-158. doi: 10.1016/0378-3782(90)90011-7
Prechtl, H. F., Einspieler, C., Cioni, G., Bos, A. F., Ferrari, F., and Sontheimer, D. (1997). An early marker for neurological deficits after perinatal brain lesions. Lancet 349, 1361-1363. doi: 10.1016/S0140-6736(96)10182-3
Rogers, S. J., Vismara, L., Wagner, A. L., McCormick, C., Young, G., and Ozonoff, S. (2014). Autism treatment in the first year of life: a pilot study of infant start, a parent-implemented intervention for symptomatic infants. J. Autism Dev. Disord. 44, 2981-2995. doi: 10.1007/s10803-014-2202-y
Sameroff, A. J., and MacKenzie, M. J. (2003). Research strategies for capturing transactional models of development: the limits of the possible. Dev. Psychopathol. 15, 613-640. doi: 10.1017/S0954579403000312
Spittle, A. J., McGinley, J. L., Thompson, D., Clark, R., FitzGerald, T. L., Mentiplay, B. F., et al. (2016). Motor trajectories from birth to 5 years of children born at less than 30 weeks' gestation: early predictors and functional implications. Protocol for a prospective cohort study. J. Physiother. 62, 222-223. doi: 10.1016/j.jphys.2016.07.002
Teitelbaum, P., Teitelbaum, O., Nye, J., Fryman, J., and Maurer, R. G. (1998). Movement analysis in infancy may be useful for early diagnosis of autism. Proc. Natl. Acad. Sci. U.S.A. 95, 13982-13987. doi: 10.1073/pnas.95.23.13982
Thelen, E., Corbetta, D., and Spencer, J. P. (1996). Development of reaching during the first year: role of movement speed. J. Exp. Psychol. Hum. Percept. Perform. 22, 1059-1076. doi: 10.1037/0096-1523.22.5.1059
Thelen, E., Corbetta, D., Kamm, K., Spencer, J. P., Schneider, K., and Zernicke, R. F. (1993). The transition to reaching: mapping intention and intrinsic dynamics. Child Dev. 64, 1058-1098. doi: 10.2307/1131327
Thomas, M. S., Annaz, D., Ansari, D., Scerif, G., Jarrold, C., and Karmiloff-Smith, A. (2009). Using developmental trajectories to understand developmental disorders. J. Speech Lang. Hear. Res. 52, 336-358. doi: 10.1044/1092-4388(2009/07-0144)
Torres, E. B., Smith, B., Mistry, S., Brincker, M., and Whyatt, C. (2016). Neonatal diagnostics: toward dynamic growth charts of neuromotor control. Front. Pediatr. 4:121. doi: 10.3389/fped.2016.00121
Viviani, P., and Schneider, R. (1991). A developmental study of the relationship between geometry and kinematics in drawing movements. J. Exp. Psychol. Hum. Percept. Perform. 17, 198-218. doi: 10.1037/0096-1523.17.1.198
von Hofsten, C. (1991). Structuring of early reaching movements: a longitudinal study. J. Mot. Behav. 23, 280-292. doi: 10.1080/00222895.1991.9942039
Waldmeier, S., Grunt, S., Delgado-Eckert, E., Latzin, P., Steinlin, M., Fuhrer, K., et al. (2013). Correlation properties of spontaneous motor activity in healthy infants: a new computer-assisted method to evaluate neurological maturation. Exp. Brain Res. 227, 433-446. doi: 10.1007/s00221-013-3504-6
Zoia, S., Blason, L., D'Ottavio, G., Biancotto, M., Bulgheroni, M., and Castiello, U. (2013). The development of upper limb movements: from fetal to post-natal life. PLoS ONE 8:e80876. doi: 10.1371/journal.pone.0080876
Zwaigenbaum, L., Bryson, S., and Garon, N. (2013). Early identification of autism spectrum disorders. Behav. Brain Res. 251, 133-146. doi: 10.1016/j.bbr.2013.04.004
Zwaigenbaum, L., Bryson, S., Rogers, T., Roberts, W., Brian, J., and Szatmari, P. (2005). Behavioral manifestations of autism in the first year of life. Int. J. Dev. Neurosci. 23, 143-152. doi: 10.1016/j.ijdevneu.2004.05.001
