Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Strengthening of horizontal cortical connections following skill learning

Abstract

Learning a new motor skill requires an alteration in the spatiotemporal pattern of muscle activation. Motor areas of cerebral neocortex are thought to be involved in this type of learning, possibly by functional reorganization of cortical connections. Here we show that skill learning is accompanied by changes in the strength of connections within adult rat primary motor cortex (M1). Rats were trained for three or five days in a skilled reaching task with one forelimb, after which slices of motor cortex were examined to determine the effect of training on the strength of horizontal intracortical connections in layer II/III. The amplitude of field potentials in the forelimb region contralateral to the trained limb was significantly increased relative to the opposite 'untrained' hemisphere. No differences were seen in the hindlimb region. Moreover, the amount of long-term potentiation (LTP) that could be induced in trained M1 was less than in controls, suggesting that the effect of training was at least partly due to LTP-like mechanisms. These data represent the first direct evidence that plasticity of intracortical connections is associated with learning a new motor skill.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Consequences of motor skill learning on field-potential responses evoked in layer II/III horizontal connections of M1.
Figure 2: Response differences in trained and control rats.

Similar content being viewed by others

References

  1. Cohen, L.G., Brasil, N.J., Pascual-Leone, L.A. & Hallett, M. Plasticity of cortical motor output organization following deafferentation, cerebral lesions, and skill acquisition. Adv. Neurol. 63, 187–200 (1993).

    CAS  PubMed  Google Scholar 

  2. Donoghue, J.P. Plasticity of sensorimotor representations. Curr. Opin. Neurobiol. 5, 749–754 (1995).

    Article  CAS  Google Scholar 

  3. Donoghue, J.P., Hess, G. & Sanes, J.N. in Acquisition of Motor Behavior (eds. Bloedel, J., Ebner, T. & Wise, S.P.) 363–386 (MIT Press, Cambridge, 1996).

    Google Scholar 

  4. Nudo, R.J., Milliken, G.W., Jenkins, W.M. & Merzenich, M.M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys . J. Neurosci. 16, 785– 807 (1996).

    Article  CAS  Google Scholar 

  5. Greenough, W.T., Larson, J.R. & Withers, G.S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav. Neural Biol. 44, 301 –314 (1985).

    Article  CAS  Google Scholar 

  6. Hess, G. & Donoghue, J.P. Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J. Neurophysiol. 71, 2543–2547 (1994).

    Article  CAS  Google Scholar 

  7. Hess, G., Aizenman, C.D. & Donoghue, J.P. Conditions for the induction of long-term potentiation in layer II/III horizontal connecitons of the rat motor cortex. J. Neurophysiol. 75, 1765–1778 (1996).

    Article  CAS  Google Scholar 

  8. Hess, G. & Donoghue, J.P. Long-term depression of horizontal connections in rat motor cortex. Eur. J. Neurosci. 8, 658–665 (1996).

    Article  CAS  Google Scholar 

  9. Aroniadou, V.A. & Keller, A. Mechanisms of LTP induction in rat motor cortex in vitro. Cereb. Cortex 5, 353–362 (1995).

    Article  CAS  Google Scholar 

  10. Castro-Alamancos, M.A., Donoghue, J.P. & Connors, B.W. Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J. Neurosci. 15, 5324–5333 (1995).

    Article  CAS  Google Scholar 

  11. Asanuma, H. & Pavlides, C. Neurological basis of motor learning in mammals. Neuroreport 8, i– vi (1997).

  12. Kaas, J.H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci . 14, 137–167 ( 1991).

    Article  CAS  Google Scholar 

  13. Merzenich, M.M., Recanzone, G., Jenkins, W.M., Allard, T.T. & Nudo, R.J. in Neurobiology of Neocortex (eds Rakic, P. & Singer, W.) 41–67 ( Wiley, New York, 1988).

  14. Huntley, G.W. Correlation between patterns of horizontal connectivity and the extent of short term representational plasticity in rat motor cortex. Cereb. Cortex 7, 143–156 (1997).

    Article  CAS  Google Scholar 

  15. Donoghue, J.P. Limits of reorganization in cortical circuits. Cereb. Cortex 7, 97–99 (1997).

    Article  CAS  Google Scholar 

  16. Jacobs, K. & Donoghue, J. Reshaping the cortical map by unmasking latent intracortical connections. Science 251 , 944–947 (1991).

    Article  CAS  Google Scholar 

  17. Hirsch, J. & Gilbert, C. Long-term changes in synaptic strength along specific intrinsic pathways in the cat's visual cortex. J. Physiol. (Lond) 461, 247–262 (1993).

    Article  CAS  Google Scholar 

  18. Price, A.W. & Fowler, S.C. Deficits in contralateral and ipsilateral forepaw motor control following unilateral motor cortical ablation in rats . Brain Res. 205, 81– 90 (1981).

    Article  CAS  Google Scholar 

  19. Garraghty, P.E. & Kaas, J.H. Dynamic features of sensory and motor maps. Curr. Opin. Neurobiol. 2, 522 –527 (1992).

    Article  CAS  Google Scholar 

  20. Sanes, J.N. & Donoghue, J.P. Motor areas of the cerebral cortex . J. Clin. Neurophysiol. 11, 382– 396, (1994).

    PubMed  Google Scholar 

  21. Rogan, M.T., Staeubli, U.V. & LeDoux, J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604– 607 (1997).

    Article  CAS  Google Scholar 

  22. McKernan, M.G. & Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607–611 ( 1997).

    Article  CAS  Google Scholar 

  23. Ahissar, E. et al. Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science 257, 1412– 1415 (1992).

    Article  CAS  Google Scholar 

  24. Grafton, S.T et al. Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J. Neurosci. 12, 2542–2548 (1992).

    Article  CAS  Google Scholar 

  25. Pascual-Leone, A., Grafman, J. & Hallett, M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263, 1287–1289 (1994).

    Article  CAS  Google Scholar 

  26. Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155– 158 (1995).

    Article  CAS  Google Scholar 

  27. Morris, R.G.M., Davis, S. & Butcher, P. in Long Term Potentiation: A Debate of Current Issues (eds Baudry, M. & Davis, J.L.) 267–300 (MIT Press, Cambridge, 1991).

    Google Scholar 

  28. Woody, C.D., Gruen, E. & Birt, D. Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res. 539, 76– 84 (1991).

    Article  CAS  Google Scholar 

  29. Yoshimura, Y. & Tsumoto, T. Dependence of LTP induction on postsynaptic depolarization: a perforated patch-clamp study in visual cortical slices of young rats. J. Neurophysiol. 71, 1638–1645 (1994).

    Article  CAS  Google Scholar 

  30. Darian, S.C. & Gilbert, C.D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737–740 (1994).

    Article  Google Scholar 

  31. Kleim, J.A., Lussnig, E., Schwarz, E.R., Comery, T.A. & Greenough, W.T. Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. J. Neurosci. 16, 4529–4535 (1996).

    Article  CAS  Google Scholar 

  32. Gilbert, C.D. Rapid dynamic changes in adult cerebral cortex. Curr. Opin. Neurobiol. 3, 100–103 (1993).

    Article  CAS  Google Scholar 

  33. Donoghue, J.P. & Wise, S.P. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 212, 76–88 (1982).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Drs. Barry Connors, Mark Bear, and Marc G. Rioult for critical comments. This work was supported by NIH grant NS22517. G. H. is an international scholar of the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mengia -S. Rioult-Pedotti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rioult-Pedotti, MS., Friedman, D., Hess, G. et al. Strengthening of horizontal cortical connections following skill learning . Nat Neurosci 1, 230–234 (1998). https://doi.org/10.1038/678

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/678

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing