Consolidation of motor memory

https://doi.org/10.1016/j.tins.2005.10.003Get rights and content

An issue of great recent interest is whether motor memory consolidates in a manner analogous to declarative memory – that is, with the formation of a memory that progresses over time from a fragile state, which is susceptible to interference by a lesion or a conflicting motor task, to a stabilized state, which is resistant to such interference. Here, we first review studies that examine the anatomical basis for motor consolidation. Evidence implicates cerebellar circuitry in two types of associative motor learning – eyelid conditioning and vestibulo-ocular reflex adaptation – and implicates primary motor cortex in skilled finger movements. We also review evidence for and against a consolidation process for adaptation of arm movements. We propose that contradictions have arisen because consolidation can be masked by inhibition of memory retrieval.

Introduction

It is clear from experience that the nervous system can form multiple long-term (>24 h) motor memories; for example, we apparently never forget how to swim, to ride a bicycle or to drive a car. However, despite the ubiquity of long-term motor memory in everyday life, experimental demonstration of how such memories are formed and retained has proven controversial. This review will focus on the specific issue of consolidation of motor memory, with consolidation defined as a set of processes whereby a long-term memory becomes more stable with the passage of time [1]. This definition implies that consolidation is proven if the memory is susceptible to disruption by a competing memory or a focal lesion during a limited time-window.

Motor memory differs from declarative memory in that it is demonstrated through savings in performance over several trials, rather than through recall of a single item (single-trial memory). ‘Savings’ refers to a more rapid rate of relearning compared with the rate of original learning. Thus, a motor memory has consolidated when there is a limited time-window within which savings can be disrupted. Here, we first describe studies of simple associative motor learning for two well-characterized reflexes, where there is good evidence for consolidation and insight into its underlying neural circuitry. We then address consolidation of skilled sequential finger movements. Finally, we examine adaptation of arm movements to novel dynamics and to new visuospatial mappings, two types of motor learning for which evidence of consolidation is more elusive.

Section snippets

Consolidation of associative motor learning

Experimental investigation of Pavlovian eyelid conditioning (EC) adaptation and vestibulo-ocular reflex (VOR) adaptation in several species has provided valuable insights into the neural circuitry, specifically in the cerebellum, involved in savings [2] and consolidation of motor memory 3, 4, 5. EC and VOR adaptation are similar in that they both involve associative learning in a reflex circuit [6], in which a conditioned stimulus (CS; e.g. tone or head motion) is paired with an unconditioned

Consolidation of skilled finger movements

Repetitive 1 Hz transcranial magnetic stimulation (rTMS) has been used to investigate the role of primary motor cortex (M1) in retention of a simple finger opposition task [36]. Subjects performed a metronome-paced (0.5 Hz) ballistic pinch between the index finger and thumb of the non-dominant left hand. The performance measure was acceleration of the pinching movement, which was assessed across two practice sessions. Control subjects showed increases in peak pinch acceleration within a first

Consolidation of internal models for reaching

In the past 20 years, a computational framework has been developed to characterize the behavioral and neural basis for planning and execution of reaching (reviewed extensively in [41]). It appears that the CNS plans reaching movements in extrinsic space 42, 43, 44, with target and hand location initially coded as vectors with respect to fixation that are then subtracted to produce an intended movement vector in a hand-centered coordinate system. The transformation of this vector into motor

Consolidation of internal models in bimanual skills

In bimanual movements, one hand often serves a supportive role by holding an object that is manipulated by the other hand. For example, if one hand holds an electronic notepad and the other hand writes on the device, the supporting hand shows compensatory adjustments to counteract the anticipated forces arising from the writing hand. A similar situation occurs when one hand holds a book while the other hand lifts it: the postural hand reduces the upward forces precisely at the moment when the

Concluding remarks

There is evidence for motor consolidation in several experimental systems – that is, the behavioral correlates of the memory suggest that under some conditions the neural substrate becomes resistant to disruption within hours or days. In specific tasks, the cerebellar cortex appears to be crucial in the initial storage of the memory but, with time, the memory can be represented elsewhere. Because motor learning comprises several distinct processes (planning of sequences of action, adaptation of

Acknowledgements

This work was supported by National Institute of Neurological Disorders and Stroke Grants K23-NS02138 (to J.W.K.), and R01-NS037422 (to R.S.). We thank Javier Medina and Michael Mauk for insightful discussions, and Toni Pearson for critical comments on the manuscript.

References (75)

  • C. Schmitz et al.

    Developmental sequence in the acquisition of anticipation during a new co-ordination in a bimanual load-lifting task in children

    Neurosci. Lett.

    (2002)
  • L. Nadel et al.

    Memory consolidation, retrograde amnesia and the hippocampal complex

    Curr. Opin. Neurobiol.

    (1997)
  • M. Nissen et al.

    Attentional requirements of learning: evidence from performance measures

    Cognit. Psychol.

    (1987)
  • O. Hikosaka

    Parallel neural networks for learning sequential procedures

    Trends Neurosci.

    (1999)
  • M.P. Walker

    Practice with sleep makes perfect: sleep-dependent motor skill learning

    Neuron

    (2002)
  • I. Toni

    The time course of changes during motor sequence learning: a whole-brain fMRI study

    Neuroimage

    (1998)
  • Y. Dudai

    The neurobiology of consolidations, or, how stable is the engram?

    Annu. Rev. Psychol.

    (2004)
  • J.F. Medina

    A mechanism for savings in the cerebellum

    J. Neurosci.

    (2001)
  • T. Ohyama et al.

    Latent acquisition of timed responses in cerebellar cortex

    J. Neurosci.

    (2001)
  • S.F. Cooke

    Temporal properties of cerebellar-dependent memory consolidation

    J. Neurosci.

    (2004)
  • K.M. Christian et al.

    Neural substrates of eyeblink conditioning: acquisition and retention

    Learn. Mem.

    (2003)
  • N. Schneiderman

    Acquisition and extinction of the classically conditioned eyelid response in the albino rabbit

    Science

    (1962)
  • K. Robleto

    Brain mechanisms of extinction of the classically conditioned eyeblink response

    Learn. Mem.

    (2004)
  • R.M. Napier

    Rapid reaquisition in conditioning of the rabbit's nictitating membrane response

    J. Exp. Psychol. Anim. Behav. Process.

    (1992)
  • J.F. Medina

    Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses

    Nature

    (2002)
  • J.F. Medina

    Parallels between cerebellum- and amygdala-dependent conditioning

    Nat. Rev. Neurosci.

    (2002)
  • S. Nagao

    Effects of vestibulocerebellar lesions upon dynamic characteristics and adaptation of vestibulo-ocular and optokinetic responses in pigmented rabbits

    Exp. Brain Res.

    (1983)
  • J.G. McElligott

    Effect of cerebellar inactivation by lidocaine microdialysis on the vestibuloocular reflex in goldfish

    J. Neurophysiol.

    (1998)
  • C.D. Kassardjian

    The site of a motor memory shifts with consolidation

    J. Neurosci.

    (2005)
  • A.E. Luebke et al.

    Gain changes of the cat's vestibulo-ocular reflex after flocculus deactivation

    Exp. Brain Res.

    (1994)
  • A.M. Partsalis

    Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals

    J. Neurophysiol.

    (1995)
  • D.M. Broussard et al.

    Learning in a simple motor system

    Learn. Mem.

    (2004)
  • B. Sacchetti

    Cerebellar role in fear-conditioning consolidation

    Proc. Natl. Acad. Sci. U. S. A.

    (2002)
  • J. Diedrichsen

    Cerebellar involvement in anticipating the consequences of self-produced actions during bimanual movements

    J. Neurophysiol.

    (2005)
  • M.J. Weiner

    Adaptation to lateral displacement of vision in patients with lesions of the central nervous system

    Neurology

    (1983)
  • T.A. Martin

    Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation

    Brain

    (1996)
  • M. Maschke

    Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements

    J. Neurophysiol.

    (2004)
  • Cited by (0)

    View full text