Skip to main content
Log in

Both sleep and wakefulness support consolidation of continuous, goal-directed, visuomotor skill

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

Abstract

Sleep has been shown to benefit memory consolidation for certain motor skills, but it remains unclear if this relationship exists for motor skills with direct rehabilitation applications. We aimed to determine the neurobehavioral relationship between finger-tracking skill development and sleep following skill training in young, healthy subjects. Forty subjects received tracking training in the morning (n = 20) or the evening (n = 20). Measures of tracking skill and cortical excitability were collected before and after training. Following training, tracking skill and measures of cortical excitability were assessed at two additional follow-up visits (12 and 24 h post-training) for each subject following an episode of sleep or waking activity. Two-way repeated-measures ANOVAs with Bonferroni-adjusted post hoc tests were conducted for tracking accuracy and measures of cortical excitability. Skill performance improved after training and continued to develop offline during the first post-training interval (12 h). This development was not further enhanced by sleep during this interval. Level of skill improvement was maintained for at least one day in both training groups. Cortical excitability was reduced following training and was related to level of skill performance at follow-up assessment. These data suggest offline memory consolidation of a continuous, visuospatial, finger-tracking skill is not dependent on sleep. These findings are in agreement with recent literature, indicating characteristics of a motor skill may be sensitive to the beneficial effect of sleep on post-training information processing.

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

Similar content being viewed by others

References

  • Baraduc P, Lang N, Rothwell JC, Wolpert DM (2004) Consolidation of dynamic motor learning is not disrupted by rTMS of primary motor cortex. Curr Biol 14:252–256

    PubMed  CAS  Google Scholar 

  • Bergmann TO, Groppa S, Seeger M, Molle M, Marshall L, Siebner HR, Bergmann TO, Groppa S, Seeger M, Molle M, Marshall L, Siebner HR (2009) Acute changes in motor cortical excitability during slow oscillatory and constant anodal transcranial direct current stimulation. J Neurophysiol 102:2303–2311

    Article  PubMed  Google Scholar 

  • Bhatt E, Nagpal A, Greer KH, Grunewald TK, Steele JL, Wiemiller JW, Lewis SM, Carey JR, Bhatt E, Nagpal A, Greer KH, Grunewald TK, Steele JL, Wiemiller JW, Lewis SM, Carey JR (2007) Effect of finger tracking combined with electrical stimulation on brain reorganization and hand function in subjects with stroke. Exp Brain Res 182:435–447

    Article  PubMed  Google Scholar 

  • Borich M, Furlong M, Holsman D, Kimberley TJ (2011) Goal-directed visuomotor skill learning: off-line enhancement and the importance of the primary motor cortex. Restor Neurol Neurosci 29:105–113

    PubMed  Google Scholar 

  • Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiat Res 28:193–213

    Article  CAS  Google Scholar 

  • Cai DJ, Rickard TC, Cai DJ, Rickard TC (2009) Reconsidering the role of sleep for motor memory. Behav Neurosci 123:1153–1157

    Article  PubMed  Google Scholar 

  • Carey J, Bogard C, King B, Suman V (1994) Finger-movement tracking scores in healthy subjects. Percept Mot Skills 79:563–576

    Article  PubMed  CAS  Google Scholar 

  • Carey J, Bogard C, Youdas J, Suman V (1995) Stimulus-response compatibility effects in a manual tracking task. Percept Mot Skills 81:1155–1170

    Article  PubMed  CAS  Google Scholar 

  • Carey JR, Kimberley TJ, Lewis SM, Auerbach E, Dorsey L, Rundquist P, Ugurbil K (2002) Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125:773–788

    Article  PubMed  Google Scholar 

  • Carey JR, Fregni F, Pascual-Leone A (2006) rTMS combined with motor learning training in healthy subjects. Restor Neurol Neurosci 24:191–199

    PubMed  Google Scholar 

  • Chen R, Tam A, Butefisch C, Corwell B, Ziemann U, Rothwell JC, Cohen LG (1998) Intracortical inhibition and facilitation in different representations of the human motor cortex. J Neurophysiol 80:2870–2881

    PubMed  CAS  Google Scholar 

  • Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123

    PubMed  CAS  Google Scholar 

  • Cohen DA, Robertson EM (2007) Motor sequence consolidation: constrained by critical time windows or competing components. Exp Brain Res 177:440–446

    Article  PubMed  Google Scholar 

  • Cohen DA, Pascual-Leone A, Press DZ, Robertson EM (2005) Off-line learning of motor skill memory: a double dissociation of goal and movement. Proc Nat Acad Sci USA 102:18237–18241

    Article  PubMed  CAS  Google Scholar 

  • Doyon J, Korman M, Morin A, Dostie V, Hadj Tahar A, Benali H, Karni A, Ungerleider LG, Carrier J (2009) Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning. Exp Brain Res 195:15–26

    Google Scholar 

  • Ferraro FR, Balota DA, Connor LT, Ferraro FR, Balota DA, Connor LT (1993) Implicit memory and the formation of new associations in nondemented Parkinson’s disease individuals and individuals with senile dementia of the Alzheimer type: a serial reaction time (SRT) investigation. Brain Cogn 21:163–180

    Article  PubMed  CAS  Google Scholar 

  • Field A (2009) Discovering statistics using SPSS: (and sex, drugs and rock’n’ roll). Sage, London

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Floyer-Lea A, Matthews PM (2004) Changing brain networks for visuomotor control with increased movement automaticity. J Neurophysiol 92:2405–2412

    Article  PubMed  CAS  Google Scholar 

  • Gallasch E, Christova M, Krenn M, Kossev A, Rafolt D, Gallasch E, Christova M, Krenn M, Kossev A, Rafolt D (2009) Changes in motor cortex excitability following training of a novel goal-directed motor task. Eur J Appl Physiol 105:47–54

    Article  PubMed  Google Scholar 

  • Goedert KM, Willingham DB, Goedert KM, Willingham DB (2002) Patterns of interference in sequence learning and prism adaptation inconsistent with the consolidation hypothesis. Learn Mem 9:279–292

    Article  PubMed  Google Scholar 

  • Hikosaka O, Miyasita K, Miyachi S, Sakai K, Lu X (1998) Differential roles of the frontal cortex, basal ganglia and cerebellum in visuomotor sequence learning. Neurobiol Learn Mem 70:137–149

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hoddes E, Zarcone V, Smythe H, Phillips R, Dement WC (1973) Quantification of sleepiness: a new approach. Psychophysiology 10:431–436

    Article  PubMed  CAS  Google Scholar 

  • Hotermans C, Peigneux P, de Noordhout AM, Moonen G, Maquet P, Hotermans C, Peigneux P, de Noordhout AM, Moonen G, Maquet P (2008) Repetitive transcranial magnetic stimulation over the primary motor cortex disrupts early boost but not delayed gains in performance in motor sequence learning. Eur J Neurosci 28:1216–1221

    Article  PubMed  Google Scholar 

  • Howell DC (2007) Statistical methods for psychology. Thomson Wadsworth, Belmont, California

    Google Scholar 

  • Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning [see comment]. Nature 430:78–81

    Article  PubMed  CAS  Google Scholar 

  • Inghilleri M, Berardelli A, Marchetti P, Manfredi M (1996) Effects of diazepam, baclofen and thiopental on the silent period evoked by transcranial magnetic stimulation in humans. Exp Brain Res 109:467–472

    Article  PubMed  CAS  Google Scholar 

  • Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14:540–545

    PubMed  CAS  Google Scholar 

  • Karni A, Meyer G, Jezzard P, Adams MM, Turner R, Ungerleider LG (1995) Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377:155–158

    Article  PubMed  CAS  Google Scholar 

  • Keisler A, Ashe J, Willingham DT, Keisler A, Ashe J, Willingham DT (2007) Time of day accounts for overnight improvement in sequence learning. Learn Mem 14:669–672

    Article  PubMed  Google Scholar 

  • Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey LL, Lojovich JM, Carey JR (2004) Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res 154:450–460

    Article  PubMed  Google Scholar 

  • Kimberley TJ, Borich MR, Prochaska KD, Mundfrom SL, Perkins AE, Poepping JM, Kimberley TJ, Borich MR, Prochaska KD, Mundfrom SL, Perkins AE, Poepping JM (2009) Establishing the definition and inter-rater reliability of cortical silent period calculation in subjects with focal hand dystonia and healthy controls. Neurosci Lett 464:84–87

    Article  PubMed  CAS  Google Scholar 

  • Koeneke S, Lutz K, Herwig U, Ziemann U, Jancke L (2006) Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability. Exp Brain Res 174:199–209

    Article  PubMed  CAS  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    PubMed  CAS  Google Scholar 

  • Kuriyama K, Stickgold R, Walker MP (2004) Sleep-dependent learning and motor-skill complexity. Learn Mem 11:705–713

    Article  PubMed  Google Scholar 

  • Maeda F, Gangitano M, Thall M, Pascual-Leone A, Maeda F, Gangitano M, Thall M, Pascual-Leone A (2002) Inter- and intra-individual variability of paired-pulse curves with transcranial magnetic stimulation (TMS). Clin Neurophysiol 113:376–382

    Article  PubMed  Google Scholar 

  • Massimini M, Tononi G, Huber R (2009) Slow waves, synaptic plasticity and information processing: insights from transcranial magnetic stimulation and high-density EEG experiments. Eur J Neurosci 29:1761–1770

    Article  PubMed  CAS  Google Scholar 

  • Matthews GRD, Westerman SJ, Stammers RB (2000) Human performance: cognition, stress and individual differences. Taylor and Francis, Philadelphia

    Google Scholar 

  • Morgenthaler T, Alessi C, Friedman L, Owens J, Kapur V, Boehlecke B, Brown T, Chesson A Jr, Coleman J, Lee-Chiong T, Pancer J, Swick TJ, Standards of Practice C, American Academy of Sleep M (2007) Practice parameters for the use of actigraphy in the assessment of sleep and sleep disorders: an update for 2007. Sleep 30:519–529

    Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644

    Article  PubMed  CAS  Google Scholar 

  • Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  PubMed  CAS  Google Scholar 

  • Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F, Benali H, Maquet P, Doyon J, Orban P, Peigneux P, Lungu O, Albouy G, Breton E, Laberenne F, Benali H, Maquet P, Doyon J (2010) The multifaceted nature of the relationship between performance and brain activity in motor sequence learning. Neuroimage 49:694–702

    Article  PubMed  Google Scholar 

  • Portney L, Watkins M (2000) Foundations of clinical research: applications to practice. Appleton & Lange, Norwalk, CN

    Google Scholar 

  • Robertson EM, Pascual-Leone A, Press DZ (2004) Awareness modifies the skill-learning benefits of sleep. Curr Biol 14:208–212

    PubMed  CAS  Google Scholar 

  • Robertson EM, Press DZ, Pascual-Leone A (2005) Off-line learning and the primary motor cortex [see comment]. J Neurosci 25:6372–6378

    Article  PubMed  CAS  Google Scholar 

  • Rosler KM, Petrow E, Mathis J, Arányi Z, Hess CW, Magistris MR (2002) Effect of discharge desynchronization on the size of motor evoked potentials: an analysis. Clin Neurophysiol 113:1680–1687

    Google Scholar 

  • Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2009) Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120:2008–2039

    Article  PubMed  Google Scholar 

  • Rossini PM, Berardelli A, Deuschl G, Hallett M, Maertens de Noordhout AM, Paulus W, Pauri F (1999) Applications of magnetic cortical stimulation. The international federation of clinical neurophysiology. Electroencephalogr Clin Neurophysiol-Suppl 52:171–185

    PubMed  CAS  Google Scholar 

  • Sadeh A, Sharkey KM, Carskadon MA (1994) Activity-based sleep-wake identification: an empirical test of methodological issues. Sleep 17:201–207

    PubMed  CAS  Google Scholar 

  • Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I, Sakai K, Ugawa Y, Terao Y, Hanajima R, Furubayashi T, Kanazawa I (1997) Preferential activation of different I waves by transcranial magnetic stimulation with a figure-of-eight-shaped coil. Exp Brain Res 113:24–32

    Article  PubMed  CAS  Google Scholar 

  • Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530:307–317

    Article  PubMed  CAS  Google Scholar 

  • Schmidt RA (2005) Motor control and learning: a behavioral emphasis. Human Kinetics, Champaign

    Google Scholar 

  • Shadmehr R, Brashers-Krug T (1997) Functional stages in the formation of human long-term motor memory. J Neurosci 17:409–419

    PubMed  CAS  Google Scholar 

  • Siengsukon CF, Boyd LA (2008) Sleep enhances implicit motor skill learning in individuals poststroke. Top Stroke Rehabil 15:1–12

    Article  PubMed  Google Scholar 

  • Stickgold R, James L, Hobson JA (2000a) Visual discrimination learning requires sleep after training [see comment]. Nature Neurosci 3:1237–1238

    Article  PubMed  CAS  Google Scholar 

  • Stickgold R, Whidbee D, Schirmer B, Patel V, Hobson JA (2000b) Visual discrimination task improvement: a multi-step process occurring during sleep. J Cogn Neurosci 12:246–254

    Article  PubMed  CAS  Google Scholar 

  • Tucker MA, Hirota Y, Wamsley EJ, Lau H, Chaklader A, Fishbein W, Tucker MA, Hirota Y, Wamsley EJ, Lau H, Chaklader A, Fishbein W (2006) A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiol Learn Mem 86:241–247

    Article  PubMed  Google Scholar 

  • Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R (2002) Practice with sleep makes perfect: sleep-dependent motor skill learning [see comment]. Neuron 35:205–211

    Article  PubMed  CAS  Google Scholar 

  • Walker MP, Brakefield T, Hobson JA, Stickgold R (2003a) Dissociable stages of human memory consolidation and reconsolidation [see comment]. Nature 425:616–620

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Walker MP, Stickgold R, Alsop D, Gaab N, Schlaug G (2005) Sleep-dependent motor memory plasticity in the human brain. Neuroscience 133:911–917

    Article  PubMed  CAS  Google Scholar 

  • Wassermann EM (2008) The Oxford handbook of transcranial stimulation. Oxford University Press, Oxford

    Google Scholar 

  • Willingham DB, Peterson EW, Manning C, Brashear HR, Willingham DB, Peterson EW, Manning C, Brashear HR (1997) Patients with Alzheimer’s disease who cannot perform some motor skills show normal learning of other motor skills. Neuropsychology 11:261–271

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996a) The effect of lorazepam on the motor cortical excitability in man. Exp Brain Res 109:127–135

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996b) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Rothwell JC, Ridding MC (1996c) Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol 496:873–881

    PubMed  CAS  Google Scholar 

  • Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124:1171–1181

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D, Ziemann U, Ilic TV, Pauli C, Meintzschel F, Ruge D (2004) Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex [erratum appears in J Neurosci 2004 Nov 17;24(46):1 p following 10552 Note: Iliac, Tihomir V [corrected to Ilic, Tihomir V]]. J Neurosci 24:1666–1672

    Google Scholar 

Download references

Acknowledgments

This publication was made possible by support from the National Center for Research Resources’ (NCRR) grant M01 RR00400, a component of the National Institutes of Health. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NIH or NCRR. This study was also supported by a Doctoral Dissertation Fellowship from the University of Minnesota Graduate School (M.B.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael R. Borich.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borich, M.R., Kimberley, T.J. Both sleep and wakefulness support consolidation of continuous, goal-directed, visuomotor skill. Exp Brain Res 214, 619–630 (2011). https://doi.org/10.1007/s00221-011-2863-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-011-2863-0

Keywords

Navigation