Skip to main content
Log in

Developmental contributions to motor sequence learning

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Little is known about how children acquire new motor sequences. In particular, it is not clear if the same learning progression observed in adults is also present in childhood nor whether motor skills are acquired in a similar fashion across development. In the present study we used the multi-finger sequencing task (MFST), a variant of the serial reaction time (SRT) task, to study motor sequence learning, across two consecutive days, in three cross-sectional samples of children aged 6, 8, and 10 years, and a control sample of adults. In the MFST, participants reproduced 10-element sequences of key presses on an electronic keyboard, using four fingers of the right hand. Each block of practice included 10 intermixed trials of a Repeated (REP) sequence and four trials of Random (RAN) sequences. Performance was assessed by examining changes in accuracy, a component of the task that requires the association of the visual stimulus with the motor response, and response synchronization, a component that requires fine-grained sensorimotor integration and timing. Additionally, participants completed Recognition and Recall tests, to assess explicit knowledge of the repeated sequence. Overall, results showed a developmental progression in motor sequence learning within and across days of practice. Interestingly, the two behavioral measures showed different developmental trajectories. For accuracy, differences were greatest for the two youngest groups early in learning, and these groups also showed the greatest rate of improvement. However, by the end of Day 2, only the 6-year-olds still lagged behind all other groups. For response synchronization, all child groups differed from adults early in learning, but both child and adult groups showed similar rates of improvement across blocks of practice. By the end of Day 2, 10-year-olds reached adult levels of performance, whereas 6- and 8-year-olds did not. Taken together, the dissociation observed with our two behavioral measures of sequence learning is consistent with the hypothesis that accuracy or finger-stimulus association may rely on cortical pathways that show the greatest maturation between ages 6 and 10; whereas motor timing and sensorimotor integration may rely on subcortical pathways that continue to develop into young adulthood. Despite developmental differences across blocks of practice on both behavioral measures, there were no significant group differences for either the Recognition or Recall tests. We suggest that explicit knowledge of the MFST is not directly linked to task performance, thus challenging the implicit–explicit distinction in pediatric SRT studies assessing the developmental invariance model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Badan M, Hauert C-A, Mounoud P (2000) Sequential pointing in children and adults. J Exp Child Psychol 75:43–69

    Article  PubMed  CAS  Google Scholar 

  • Barnea-Goraly N, Menon V, Eckert M, Tamm L, Bammer R, Karchemskiy DantC, Reiss A (2005) White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb Cortex 15:1848–1854

    Article  PubMed  Google Scholar 

  • Contreras-Vidal J, Bo J, Boudreau J, Clark J (2005) Development of visuomotor representations for hand movement in young children. Exp Brain Res 162:155–164

    Article  PubMed  Google Scholar 

  • De Guise E, Lassonde M (2001) Callosal contributions to procedural learning in children. Dev Neuropsychol 19:253–272

    Article  PubMed  Google Scholar 

  • Denckla M (1973) Development of speed in repetitive and successive finger-movements in normal children. Dev Med Child Neurol 15:635–645

    PubMed  CAS  Google Scholar 

  • Dorfberger S, Adi-Japha E, Karni A (2007) Reduced susceptibility to interference in the consolidation of motor memory before adolescence. PLoS ONE 2:e240

    Article  PubMed  Google Scholar 

  • Doyon J, Benali H (2005) Reorganization and plasticity in the adult human brain during learning of motor skills. Curr Opin Neurobiol 15:161–167

    Article  PubMed  CAS  Google Scholar 

  • Ferrel C, Bard C, Fleury M (2001) Coordination in childhood: modifications of visuomotor representations in 6- to 11-year-old children. Exp Brain Res 138:313–321

    Article  PubMed  CAS  Google Scholar 

  • Fischer S, Hallschmid M, Elsner AL, Born J (2002) Sleep forms memory for finger skills. Proc Natl Acad Sci USA 99:11987–11991

    Article  PubMed  CAS  Google Scholar 

  • Fischer S, Wilhelm I, Born J (2007) Developmental differences in sleep's role for implicit offline learning: comparing children with adults. J Cogn Neurosci 19:214–227

    Article  PubMed  Google Scholar 

  • Garvey M, Ziemann U, Bartko J, Denckla M, Barker C, Wassermann E (2003) Cortical correlates of neuromotor development in healthy children. Clin Neurophysiol 114:1662–1670

    Article  PubMed  CAS  Google Scholar 

  • Gogtay N, Giedd J, Lusk L, Hayashi K, Greenstein D, Vaituzis A, Nugent T, Merman D, Clasen L, Toga A, Rapoport J, Thompson P (2004) Dynamic mapping of human cortical development during childhood and through early adulthood. Proc Natl Acad Sci USA 101:8174–8179

    Article  PubMed  CAS  Google Scholar 

  • Hager-Ross C, Schieber M (2000) Quantifying the independence of human finger movements: comparisons of digits, hands and movement frequencies. J Neurosci 20:8542–8550

    PubMed  CAS  Google Scholar 

  • Hikosaka O, Nakahara H, Rand M, Sakai K, Lu X, Nakamura K, Miyauchi S, Doya K (1999) Parallel neural networks for learning sequential procedures. Trends Neurosci 22:464–471

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka O, Nakamura H, Sakai K, Nakahara H (2002) Central mechanisms of motor skill learning. Curr Opin Neurobiol 12:217–222

    Article  PubMed  CAS  Google Scholar 

  • Johnson J, Newport E (1989) Critical period effects in second language learning: the influence of maturational state on the acquisition of English as a second language. Cogn Psychol 21:60–99

    Article  PubMed  CAS  Google Scholar 

  • Karni A, Meyer G, Rey-Hipolito C, Jezzard P, Adams M, Tuner R, Ungerleider L (1998) The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. Proc Natl Acad Sci USA 95:861–868

    Article  PubMed  CAS  Google Scholar 

  • Knudsen E (2004) Sensitive periods in the development of the brain and behavior. J Cogn Neurosci 16:1412–1425

    Article  PubMed  Google Scholar 

  • Kooistra L, Crawford S, Dewey D, Cantell M, Kaplan B (2005) Motor correlates of ADHD: contribution of reading disability and oppositional defiant disorder. J Learn Disabil 38:195–206

    Article  PubMed  Google Scholar 

  • Korman M, Raz N, Flash T, Karni A (2003) Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance. Proc Natl Acad Sci USA 100:12492–12497

    Article  PubMed  CAS  Google Scholar 

  • Krakauer J, Shadmehr R (2006) Consolidation of motor memory. Trends Neurosci 29:58–64

    Article  PubMed  CAS  Google Scholar 

  • Kuhtz-Buschbeck J, Stolze H, Johnk K, Boczek-Funcke A, Illert M (1998) Development of prehension movements in children: a kinematic study. Exp Brain Res 122:424–432

    Article  PubMed  CAS  Google Scholar 

  • Lang C, Schieber M (2004) Human finger independence: limitations due to passive mechanical coupling versus active neuromuscular control. J Neurophysiol 92:2802–2810

    Article  PubMed  Google Scholar 

  • Mackie S, Shaw P, Lenroot R, Pierson R, Greenstein D, Nugent T, Sharp W, Giedd J, Rapoport J (2007) Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am J Psychiatry 164:647–655

    Article  PubMed  Google Scholar 

  • Meulemans T, Van der Linden M, Perruchet P (1998) Implicit sequence learning in children. J Exp Child Psychol 69:199–221

    Article  PubMed  CAS  Google Scholar 

  • Nissen M, Bullemer P (1987) Attentional requirements of learning: evidence from performance measures. Cogn Psychol 19:1–32

    Article  Google Scholar 

  • O’Driscoll G, Depatie L, Holahan A, Savion-Lemieux T, Barr R, Jolicoeur C, Douglas V (2005) Executive functions and methylphenidate response in subtypes of attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1452–1460

    Article  PubMed  CAS  Google Scholar 

  • Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • Paus T, Zijdenbos A, Worsley K, Collins D (1999) Structural maturation of neural pathways in children and adolescents: in vivo study. Science 283:1908–1911

    Article  PubMed  CAS  Google Scholar 

  • Paus T, Collins D, Evans A, Leonard G, Pike B, Zijdenbos A (2001) Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull 54:255–266

    Article  PubMed  CAS  Google Scholar 

  • Pitcher T, Piek J, Hay D (2003) Fine and gross motor ability in males with ADHD. Dev Med Child Neurol 45:525–535

    Article  PubMed  Google Scholar 

  • Reber A (1993) Implicit learning and tacit knowledge: an essay on the cognitive unconscious. Oxford University Press, New York

    Google Scholar 

  • Reilly K, Hammond G (2000) Independence of force production by digits of the human hand. Neurosci Lett 290:53–56

    Article  PubMed  CAS  Google Scholar 

  • Reilly K, Hammond G (2006) Intrinsic hand muscles and digit independence on the preferred and non-preferred hands of humans. Exp Brain Res 173:564–571

    Article  PubMed  Google Scholar 

  • Robertson E, Pascual-Leone A, Miall R (2004) Current concepts in procedural consolidation. Nat Rev Neurosci 5:1–6

    Article  CAS  Google Scholar 

  • Savion-Lemieux T, Penhune V (2005) The effects of practice and delay on motor skill learning and retention. Exp Brain Res 161:423–431

    Article  PubMed  Google Scholar 

  • Schlaug G (2001) The brain of musicians. A model for functional and structural adaptation. Ann N Y Acad Sci 930:281–299

    PubMed  CAS  Google Scholar 

  • Seger C (1997) Two forms of sequential implicit learning. Conscious Cogn 6:108–131

    Article  PubMed  CAS  Google Scholar 

  • Slobounov S, Chiang H, Johnston J, Ray W (2002) Modulated cortical control of individual fingers in experienced musicians: an EEG study. Clin Neurophysiol 113:2013–2024

    Article  PubMed  CAS  Google Scholar 

  • Smits-Engelsman B, Sugden D, Duysens J (2006) Developmental trends in speed accuracy trade-off in 6 to 10-year-old children performing rapid reciprocal and discrete aiming movements. Hum Mov Sci 25:37–49

    Article  PubMed  Google Scholar 

  • Sowell E, Thompson P, Holmes C, Jernigan T, Toga A (1999) In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859–861

    Article  PubMed  CAS  Google Scholar 

  • Sowell E, Thompson P, Leonard C, Welcome S, Kan E, Toga A (2004) Longitudinal mapping of cortical thickness and brain growth in normal children. J Neurosci 24:8223–8231

    Article  PubMed  CAS  Google Scholar 

  • Takahashi C, Nemet D, Rose-Gottron C, Larson J, Cooper D, Reinkensmeyer D (2003) Neuromotor noise limits motor performance, but not motor adaptation, in children. J Neurophysiol 90:703–711

    Article  PubMed  Google Scholar 

  • Thomas K, Nelson C (2001) Serial reaction time learning in preschool- and school-age children. J Exp Child Psychol 79:364–387

    Article  PubMed  CAS  Google Scholar 

  • Thomas K, Hunt R, Vizueta N, Sommer T, Durston S, Yang Y, Worden M (2004) Evidence of developmental differences in implicit sequence learning: an fMRI study of children and adults. J Cogn Neurosci 16:1339–1351

    Article  PubMed  Google Scholar 

  • Tober CL, Pollak SD (2005) Motor development of post-institutionalized children across time. Biennial Meeting of the Society for Research in Child Development, Atlanta, GA

    Google Scholar 

  • Walker M, Brakefield T, Seidman J, Morgan A, Hobson J, Stickgold R (2003) Sleep and the time course of motor skill learning. Learn Mem 10:275–284

    Article  PubMed  Google Scholar 

  • Watanabe D, Savion-Lemieux T, Penhune V (2007) The effect of early musical training on adult motor performance: evidence for a sensitive period in motor learning. Exp Brain Res 176:332–340

    Article  PubMed  Google Scholar 

  • Weber-Fox C, Neville H (2001) Sensitive periods differentiate processing of open- and closed-class words: an ERP study of bilinguals. J Speech Lang Hear Res 44:1338–1353

    Article  PubMed  CAS  Google Scholar 

  • Wilke M, Krageloh-Mann I, Holland S (2007) Global and local development of gray and white matter volume in normal children and adolescents. Exp Brain Res 178:296–307

    Article  PubMed  Google Scholar 

  • Wolff P, Gunnoe C, Cohen C (1983) Associated movements as a measure of developmental age. Dev Med Child Neurol 25:417–429

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the important contribution of Alejandro Endo in developing the stimulus delivery and data analysis software, as well as the assistance of Odelia Borten and Andrea Lee in data collection. Most importantly, we would like to thank the students, parents, and teachers of Lower Canada College for working with our team to conduct this study. Funds supporting the research came from the Natural Sciences and Engineering Research Council of Canada (VBP), the Fonds de la recherché en santé du Québec (VBP and TSL) and the Centre for Research in Human Development (TSL).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tal Savion-Lemieux.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Savion-Lemieux, T., Bailey, J.A. & Penhune, V.B. Developmental contributions to motor sequence learning. Exp Brain Res 195, 293–306 (2009). https://doi.org/10.1007/s00221-009-1786-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-009-1786-5

Keywords

Navigation