Elsevier

Neuroscience

Volume 125, Issue 2, 2004, Pages 329-336
Neuroscience

Skilled-learning-induced potentiation in rat sensorimotor cortex: a transient form of behavioural long-term potentiation

https://doi.org/10.1016/j.neuroscience.2004.01.048Get rights and content

Abstract

The relation between the acquisition of a skilled motor task and synaptic plasticity in the sensorimotor cortex of the awake, freely behaving rat was examined. Skilled-motor training was previously found to induce a functional reorganization of the caudal forelimb area, and to induce an increase in synaptic efficacy, measured in vitro, on the side contralateral to the reaching forelimb. Here, we repeatedly measured neocortical evoked potential recordings in awake, freely behaving rats to examine whether skilled training would induce changes in polysynaptic efficacy on the side contralateral to the reaching forelimb. We found that the increase in task proficiency, but not the acquisition of task requirements or the maintenance of task proficiency, induced an increase in synaptic efficacy on the side contralateral to the reaching forelimb. We also tested the hypothesis that skilled learning induced potentiation shares similar mechanisms to long-term potentiation (LTP) and long-term depression by artificially manipulating polysynaptic efficacy in skilled rats with high- and low-frequency stimulation. We observed that, compared with the ipsilateral side, less potentiation but more depression could be induced on the side contralateral to the reaching forelimb. We conclude that a transient, network-based LTP-like mechanism operates during the learning of a skilled motor task.

Section snippets

Subjects

Twenty-six male Long-Evans rats, weighing between 350 and 425 g at the time of surgery, were used. The rats were obtained from the University of Calgary (Calgary, Alberta, Canada) breeding colonies. All animals were housed individually in clear plastic cages in a colony room that was maintained on a 12-h light/dark cycle. All experimentation was conducted during the light phase. Rats were maintained on Laboratory Diet no. 5001 (PMI feeds Inc., St. Louis, MO, USA) and water ad libitum, and were

Effects of skilled-training on reaching acquisition and evoked potential late component

The profile of number of reach attempts differed between the skilled- and unskilled-trained rats (Fig. 1A). The percent reaching success, expressed over 15 days of training, is represented in Fig. 1B and shows that, on average, the skilled-trained rats took 4 days to acquire the task requirements. Over days 5–8, the rats improved their motor skill, as evidenced by the slope (12.78) of the line during increase in skill proficiency. The slope (1.69) during the acquisition of task requirements and

Discussion

In the present study, two complementary experiments were performed to examine the synaptic plasticity and memory hypothesis in the caudal forelimb area of the awake, freely behaving rat. To our knowledge, this represents the first report of the effects of the acquisition of a skilled motor task on synaptic plasticity in the rat motor cortex in vivo. Two major findings arise from this work, and each will be revisited in turn.

Our first finding revealed that the increase in proficiency of a

Acknowledgements

Research supported by NSERC and CSN grants to G.C.T., and an NSERC scholarship to M.H.M. The authors wish to thank D. Pontin for technical assistance.

References (45)

  • I.Q. Whishaw

    Loss of the innate cortical engram for action patterns used in skilled reaching and the development of behavioral compensation following motor cortex lesions in the rat

    Neuropharmacology

    (2000)
  • I.Q. Whishaw et al.

    The impairments in reaching and the movements of compensation in rats with motor cortex lesionsAn endpoint, videorecording, and movement notation analysis

    Behav Brain Res

    (1991)
  • G.S. Withers et al.

    Reach training selectively alters dendritic branching in subpopulations of layer II–III pyramids in rat motor-somatosensory forelimb cortex

    Neuropsychologia

    (1989)
  • G.Q. Bi et al.

    Synaptic modifications in cultured hippocampal neuronsDependence on spike timing, synaptic strength, and postsynaptic cell type

    J Neurosci

    (1998)
  • D.V. Buonomano et al.

    Cortical plasticityFrom synapses to maps

    Annu Rev Neurosci

    (1998)
  • S.D. Bury et al.

    Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the “Unaffected” forelimb and training-induced dendritic structural plasticity in the motor cortex

    J Neurosci

    (2002)
  • C.A. Chapman et al.

    Changes in field potentials and membrane currents in rat sensorimotor cortex following repeated tetanization of the corpus callosum in vivo

    Cereb Cortex

    (1998)
  • D.J. Froc et al.

    Long-term depression and depotentiation in the sensorimotor cortex of the freely moving rat

    J Neurosci

    (2000)
  • S.T. Grafton et al.

    Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET

    J Neurosci

    (1992)
  • G. Hess et al.

    Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps

    J Neurophysiol

    (1994)
  • J.A. Kleim et al.

    Functional reorganization of the rat motor cortex following motor skill learning

    J Neurophysiol

    (1998)
  • J.A. Kleim et al.

    Synaptogenesis and FOS expression in the motor cortex of the adult rat after motor skill learning

    J Neurosci

    (1996)
  • Cited by (0)

    1

    Present address: Canadian Centre for Behavioural Neuroscience, University of Lethbridge, Lethbridge, Alberta, Canada, T1K 3M4.

    View full text