Motor skill consolidation

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Motor skill consolidation represents the process by which motor skills are transformed from an initial fragile state, in which they are especially prone to being disrupted or lost, to a more solid or permanent state.[1] Any newly formed motor skill, such as learning to play a musical instrument or adjusting one's running stride, is subject to a consolidation period. The time course of this period during which new motor skills are susceptible to disruption appears to be on the order of a few hours.[1][2]

Distinctions between procedural and declarative memories[edit]

Motor skills, also known as procedural memories, are distinct from declarative memories, which involve memories of events, people, places, etc. Both types of memories are, however, subject to a consolidation period, though the neural mechanisms appear to differ. Some of the earliest evidence pointing to a distinction between procedural and declarative memories came from the famous neurology patient HM. As a treatment for severe epilepsy, portions of HM's temporal lobes, including both hippocampi, were removed. This left him unable to form new declarative memories (anterograde amnesia), while his ability to learn novel motor tasks remained intact.[3]

Motor skills and the internal model[edit]

It is believed that motor skill acquisition requires learning a new internal model of limb dynamics.[4][5] For instance, in order to reach for a cup of coffee, a person must have an implicit understanding of the mass of their own arm, and how specific patterns of muscle activation will change the position of that limb. A common model for studying motor learning and consolidation involves perturbations to reaching tasks using robotic arms to impart forces on the limb during reaches, forcing the subject to learn new internal representations of the limb to take these new external forces into account.[4][6]

Role of sleep in motor memory consolidation[edit]

A number of recent studies have begun to demonstrate the importance of sleep in the process of consolidation of both procedural and declarative memories.[7][8][9] For instance, it was recently shown that even a short 90 minute nap after training in a skilled finger task prevented interference two hours after the task when compared to subjects that did not nap.[10] During night sleep, REM sleep and slow-wave sleep both contribute to the motor memory consolidation process through an increase in neuromodulatory activity, as well as regular field potential oscillations such as sleep spindles (reviewed by Diekelmann and Born, 2010[11]).

Pathologies and processes affecting motor memory consolidation[edit]

While the precise neural basis for motor skill consolidation is not fully understood, many of the structures necessary for the process have been identified. As the process of learning a motor skill requires both initial execution of the skill, as well as long storage of the consolidated memory, a complex network of brain areas are involved, including the primary motor cortex, the cerebellum, the prefrontal cortex, and the basal ganglia.[5][12][13][14] Given that motor skill consolidation is a distributed process, the ability to form new procedural memories is susceptible to the effects of a number of processes and pathologies.

Cerebellar diseases[edit]

The cerebellum, and especially the cerebellar cortex, is critical for coordinating motor outputs during skilled tasks, as well as the process of stabilizing newly formed motor skills.[15] Damage to the cerebellum can occur through a number of causes including trauma, alcoholism, chronic degenerative diseases such as olivopontocerebellar atrophy, and genetic developmental disorders.[16][17]

Parkinson's disease[edit]

Parkinson's disease, which affects the basal ganglia, has been shown to cause an impairment in the ability to consolidate new motor skills.[18] For instance, when Parkinsonian patients were tested in force field reaching tasks, they showed significantly less retention of the motor skill than controls during later testing.[19] This points to the importance of the basal ganglia, the primary target of Parkinson's disease, in creating the new sensory/motor mappings that are necessary for the long term retention of a motor skill.

Stroke[edit]

A stroke is the damage of a volume of brain tissue resulting from restricted blood supply, which is often a result of occluded blood vessels leading to the brain. Given the large number of brain areas involved in the motor skill acquisition, strokes affecting any of these areas can lead to deficits in motor skill consolidation. Therapies for stroke have focused on modified practice techniques to allow the reacquisition of important skills after the damage has occurred.[20]

Aging[edit]

Aging has been shown to have an effect on declarative memory consolidation, which appears to be related to disruptions of sleep patterns,[21] as well as hippocampal degeneration.[22] However, aging does not appear to have a direct effect on motor skill consolidation, with subjects up to 95 years of age showing the ability to retain newly formed motor skills up to two years after acquisition.[23]

References[edit]

  1. ^ a b Brashers-Krug T, Shadmehr R, Bizzi E., Consolidation in human motor memory. Nature. 1996 Jul 18;382(6588):252-5.
  2. ^ Press DZ, Casement MD, Pascual-Leone A, Robertson EM. The time course of off-line motor sequence learning. Brain Res Cogn Brain Res. 2005 Sep;25(1):375-8.
  3. ^ Corkin S. What's new with the amnesic patient H.M.? Nat Rev Neurosci. 2002 Feb;3(2):153-60.
  4. ^ a b Wolpert, D. M.; Ghahramani, Z; Jordan, M. I. (1995). "An internal model for sensorimotor integration". Science. 269 (5232). New York: 1880–2. Bibcode:1995Sci...269.1880W. doi:10.1126/science.7569931. PMID 7569931. S2CID 2321011.
  5. ^ a b Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science. 1997 Aug 8;277(5327):821-5.
  6. ^ Ahmed AA, Wolpert DM, Flanagan JR. Flexible representations of dynamics are used in object manipulation. Curr Biol. 2008 May 20;18(10):763-8.
  7. ^ Fischer S, Hallschmid M, Elsner AL, Born J. Sleep forms memory for finger skills. Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11987-91. Epub 2002 Aug 22.
  8. ^ Walker MP, Stickgold R. Sleep-dependent learning and memory consolidation. Neuron. 2004 Sep 30;44(1):121-33.
  9. ^ Stickgold R. Sleep-dependent memory consolidation. Nature. 2005 Oct 27;437(7063):1272-8.
  10. ^ Korman M, Doyon J, Doljansky J, Carrier J, Dagan Y, Karni A. Daytime sleep condenses the time course of motor memory consolidation. Nat Neurosci. 2007 Sep;10(9):1206-13. Epub 2007 Aug 12.
  11. ^ Diekelmann S, Born J., The memory function of sleep. Nat Rev Neurosci. 2010 Feb;11(2):114-26. Epub 2010 Jan 4.
  12. ^ Krakauer JW, Shadmehr R. Consolidation of motor memory. Trends Neurosci. 2006 Jan;29(1):58-64. Epub 2005 Nov 14.
  13. ^ Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167-202.
  14. ^ Packard MG, Knowlton BJ. Learning and memory functions of the Basal Ganglia. Annu Rev Neurosci. 2002;25:563-93. Epub 2002 Mar 27.
  15. ^ Diedrichsen J, Verstynen T, Lehman SL, Ivry RB. Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements. J Neurophysiol. 2005 Feb;93(2):801-12. Epub 2004 Sep 8.
  16. ^ Kandel, E., Schwartz, J., & Jessell, T. Principles of neural science. 2000: McGraw-Hill, New York.
  17. ^ Millen KJ, Gleeson JG. Cerebellar development and disease. Curr Opin Neurobiol. 2008 Feb;18(1):12-9. Epub 2008 May 29.
  18. ^ Doyon J. Motor sequence learning and movement disorders. Curr Opin Neurol. 2008 Aug;21(4):478-83.
  19. ^ Krebs HI, Hogan N, Hening W, Adamovich SV, Poizner H. Procedural motor learning in Parkinson's disease. Exp Brain Res. 2001 Dec;141(4):425-37. Epub 2001 Oct 18.
  20. ^ Krakauer JW. Motor learning: its relevance to stroke recovery and neurorehabilitation. Curr Opin Neurol. 2006 Feb;19(1):84-90.
  21. ^ Buckley TM, Schatzberg AF. Aging and the role of the HPA axis and rhythm in sleep and memory-consolidation. Am J Geriatr Psychiatry. 2005 May;13(5):344-52.
  22. ^ Ward MT, Oler JA, Markus EJ. Hippocampal dysfunction during aging I: deficits in memory consolidation. Neurobiol Aging. 1999 Jul-Aug;20(4):363-72.
  23. ^ Smith CD, Walton A, Loveland AD, Umberger GH, Kryscio RJ, Gash DM Memories that last in old age: motor skill learning and memory preservation. Neurobiol Aging. 2005 Jun;26(6):883-90.
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