Abstract
Practice is vital to the acquisition of new skills, but the brain does not stop processing information when practice stops. After practice, changes take place that strengthen and modify the new skill. These changes, described under the umbrella term 'consolidation', take two distinct forms: the enhancement of skills and the stabilization of memories. Here we describe and evaluate the evidence for these types of consolidation.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Lechner, H., Squire, L. & Byrne, J. 100 years of consolidation â remembering Muller and Pilzecker. Learn. Mem. 6, 77â87 (1999).
McGaugh, J. L. Memory â a century of consolidation. Science 287, 248â251 (2000).
Eysenk, H. & Frith, C. Reminiscence, Motivation, and Personality (Plenum, New York & London, 1977).
Karni, A., Tanne, D., Rubenstein, B. S., Askenasy, J. J. & Sagi, D. Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265, 679â682 (1994).
Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. Sleep, learning, and dreams: off-line memory reprocessing. Science 294, 1052â1057 (2001).
Fischer, S., Hallschmid, M., Elsner, A. L. & Born, J. Sleep forms memory for finger skills. Proc. Natl Acad. Sci. USA 99, 11987â11991 (2002).
Walker, M. P., Brakefield, T., Morgan, A., Hobson, J. A. & Stickgold, R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35, 205â211 (2002).
Korman, M., Raz, N., Flash, T. & Karni, A. Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance. Proc. Natl Acad. Sci. USA 100, 12492â12497 (2003).
Walker, M. P., Brakefield, T., Hobson, J. A. & Stickgold, R. Dissociable stages of human memory consolidation and reconsolidation. Nature 425, 616â620 (2003).
Giuditta, A. et al. The sequential hypothesis of the function of sleep. Behav. Brain Res. 69, 157â166 (1995).
Gais, S., Plihal, W., Wagner, U. & Born, J. Early sleep triggers memory for early visual discrimination skills. Nature Neurosci. 3, 1335â1339 (2000).
Stickgold, R., Whidbee, D., Schirmer, B., Patel, V. & Hobson, J. A. Visual discrimination task improvement: a multi-step process occurring during sleep. J. Cogn. Neurosci. 12, 246â254 (2000).
Smith, C. & MacNeill, C. Impaired motor memory for a pursuit rotor task following Stage 2 sleep loss in college students. J. Sleep Res. 3, 206â213 (1994).
Stickgold, R., James, L. & Hobson, J. A. Visual discrimination learning requires sleep after training. Nature Neurosci. 3, 1237â1238 (2000).
Maquet, P., Schwartz, S., Passingham, R. & Frith, C. Sleep-related consolidation of a visuomotor skill: brain mechanisms as assessed by functional magnetic resonance imaging. J. Neurosci. 23, 1432â1440 (2003).
Robertson, E. M., Pascual-Leone, A. & Press, D. Z. Awareness modifies the skill-learning benefits of sleep. Curr. Biol. 14, 208â212 (2004).
Hobson, J. & Pace-Schott, E. The cognitive neuroscience of sleep: neuronal systems, consciousness and learning. Nature Rev. Neurosci. 3, 679â693 (2002).
Wilson, M. A. & McNaughton, B. L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676â679 (1994).
Lee, A. K. & Wilson, M. A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36, 1183â1194 (2002).
Steriade, M. & Timofeev, I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37, 563â576 (2003).
Graves, L., Pack, A. & Abel, T. Sleep and memory: a molecular perspective. Trends Neurosci. 24, 237â243 (2001).
Gu, Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111, 815â835 (2002).
Gu, Q. Contribution of acetylcholine to visual cortex plasticity. Neurobiol. Learn. Mem. 80, 291â301 (2003).
Wagner, U., Gais, S., Haider, H. & Born, J. Sleep inspires insight. Nature 427, 352â355 (2004).
Stickgold, R. & Walker, M. To sleep, perchance to gain creative insight? Trends Cogn. Sci. 8, 191â192 (2004).
Pascual-Leone, A., Grafman, J. & Hallett, M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263, 1287â1289 (1994).
Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155â158 (1995).
Pascual-Leone, A. et al. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J. Neurophysiol. 74, 1037â1045 (1995).
Press, D. Z., Robertson, E. M., Casement, M. & Pascual-Leone, A. Increasing skill without awareness or practice. Soc. Neurosci. Abstr. 29, 443.5 (2003).
Eysenk, H. A three-factor theory of reminiscence. Br. J. Psychol. 56, 163â181 (1965).
Rachman, S. & Grassi, J. Reminiscence, inhibition and consolidation. Br. J. Psychol. 56, 157â162 (1965).
Brashers-Krug, T., Shadmehr, R. & Bizzi, E. Consolidation in human motor memory. Nature 382, 252 (1996).
Miall, R., Jenkinson, N. & Kulkarni, K. Adaptation to rotated visual feedback: a re-examination of motor interference. Exp. Brain Res. 154, 201â210 (2004).
Krakauer, J., Ghilardi, M. & Ghez, C. Independent learning or internal models of kinematic and dynamic control of reaching. Nature Neurosci. 2, 1026â1031 (1999).
Donchin, O., Sawaki, L., Madupu, G., Cohen, L. G. & Shadmehr, R. Mechanisms influencing acquisition and recall of motor memories. J. Neurophysiol. 88, 2114â2123 (2002).
Hopp, J. & Fuchs, A. The characteristics and neuronal substrate of saccadic eye movement plasticity. Prog. Neurobiol. 72, 27â53 (2004).
Goedert, K. & Willingham, D. Patterns of interference in sequence learning and prism adaptation inconsistent with the consolidation hypothesis. Learn. Mem. 9, 279â292 (2002).
Shadmehr, R. & Holcomb, H. Neural correlates of motor memory consolidation. Science 277, 821â825 (1997).
Shadmehr, R. & Brashers-Krug, T. Functional stages in the formation of human long-term motor memory. J. Neurosci. 17, 409â419 (1997).
Abeele, S. & Bock, O. Mechanisms for sensorimotor adaptation to rotated visual input. Exp. Brain Res. 139, 248â253 (2001).
Muellbacher, W. et al. Early consolidation in human primary motor cortex. Nature 415, 640â644 (2002).
Robertson, E. M., Theoret, H. & Pascual-Leone, A. Studies in cognition: the problems solved and created by transcranial magnetic stimulation. J. Cogn. Neurosci. 15, 948â960 (2003).
Baraduc, P., Lang, N., Rothwell, J. & Wolpert, D. Consolidation of dynamic motor learning is not disrupted by rTMS of primary motor cortex. Curr. Biol. 14, 252â256 (2004).
Tong, C., Wolpert, D. M. & Flanagan, J. R. Kinematics and dynamics are not represented independently in motor working memory: evidence from an interference study. J. Neurosci. 22, 1108â1113 (2002).
Tong, C. & Flanagan, J. R. Task-specific internal models for kinematic transformations. J. Neurophysiol. 90, 578â585 (2003).
Cunningham, H. & Welch, R. Multiple concurrent visual-motor mappings: implications for models of adaptation. J. Exp. Psychol. Hum. Percep. Perform. 20, 987â999 (1994).
Seidler, R. Multiple motor learning experiences enhance motor adaptability. J. Cogn. Neurosci. 16, 65â73 (2004).
Willingham, D. B., Salidis, J. & Gabrieli, J. D. Direct comparison of neural systems mediating conscious and unconscious skill learning. J. Neurophysiol. 88, 1451â1460 (2002).
Mayr, U. Spatial attention and implicit sequence learning: evidence from independent learning of spatial and nonspatial sequences. J. Exp. Psychol. Learn. Mem. Cogn. 22, 350â364 (1996).
Schmidtke, V. & Heuer, H. Task integration as a factor in secondary-task effects on sequence learning. Psychol. Res. 60, 53â71 (1997).
Shin, J. & Ivry, R. Concurrent learning of temporal and spatial sequences. J. Exp. Psychol. Learn. Mem. Cogn. 28, 445â457 (2002).
Aizenstein, H. J. et al. Regional brain activation during concurrent implicit and explicit sequence learning. Cereb. Cortex 14, 199â208 (2004).
Sakai, K., Kitaguchi, K. & Hikosaka, O. Chunking during visuomotor sequence learning. Exp. Brain Res. 152, 229â242 (2003).
Wright, D. L., Black, C. B., Immink, M. A., Brueckner, S. & Magnuson, C. Long-term motor programming improvements occur via concatenation of movement sequences during random but not during blocked practice. J. Mot. Behav. 36, 39â50 (2004).
Shea, J. & Morgan, R. Contextual interference effects on the acquisition, retention, and transfer of a motor skill. J. Exp. Psychol. Hum. Learn. Mem. 5, 179â187 (1978).
Simon, D. & Bjork, R. Metacognition in motor learning. J. Exp. Psychol. Learn. Mem. Cogn. 27, 907â912 (2001).
Osu, R., Hirai, S., Yoshioka, T. & Kawato, M. Random presentation enables subjects to adapt to two opposing forces on the hand. Nature Neurosci. 7, 111â112 (2004).
Misanin, J. R., Miller, R. R. & Lewis, D. J. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 160, 554â555 (1968).
Nader, K., Schafe, G. & LeDoux, J. The labile nature of consolidation theory. Nature Rev. Neurosci. 1, 216â219 (2000).
Sara, S. Strengthening the shaky trace through retrieval. Nature Rev. Neurosci. 1, 212â213 (2000).
Karni, A. The acquisition of perceptual and motor skills: a memory system in the adult human cortex. Brain Res. Cogn. Brain Res. 5, 39â48 (1996).
Acknowledgements
We are grateful to M. Glickstein and D. Press for helpful discussions, and to M. Casement and D. Cohen for their thoughtful comments on this manuscript. The National Alliance for Research in Schizophrenia and Depression (E.M.R.), the National Institutes of Health (A.P.L.) the Goldberg Foundation (A.P.L.) and the Wellcome Trust (R.C.M.) financially supported this work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Related links
Rights and permissions
About this article
Cite this article
Robertson, E., Pascual-Leone, A. & Miall, R. Current concepts in procedural consolidation. Nat Rev Neurosci 5, 576â582 (2004). https://doi.org/10.1038/nrn1426
Issue Date:
DOI: https://doi.org/10.1038/nrn1426
This article is cited by
-
Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight
Nature Communications (2024)
-
Error-based and reinforcement learning in basketball free throw shooting
Scientific Reports (2023)
-
Time of day and sleep effects on motor acquisition and consolidation
npj Science of Learning (2023)
-
The decay and consolidation of effector-independent motor memories
Scientific Reports (2022)
-
The online and offline effects of changing movement timing variability during training on a finger-opposition task
Scientific Reports (2022)