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
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 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
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).
Donoghue, J.P. Plasticity of sensorimotor representations. Curr. Opin. Neurobiol. 5, 749–754 (1995).
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).
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).
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).
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).
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).
Hess, G. & Donoghue, J.P. Long-term depression of horizontal connections in rat motor cortex. Eur. J. Neurosci. 8, 658–665 (1996).
Aroniadou, V.A. & Keller, A. Mechanisms of LTP induction in rat motor cortex in vitro. Cereb. Cortex 5, 353–362 (1995).
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).
Asanuma, H. & Pavlides, C. Neurological basis of motor learning in mammals. Neuroreport 8, i– vi (1997).
Kaas, J.H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci . 14, 137–167 ( 1991).
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).
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).
Donoghue, J.P. Limits of reorganization in cortical circuits. Cereb. Cortex 7, 97–99 (1997).
Jacobs, K. & Donoghue, J. Reshaping the cortical map by unmasking latent intracortical connections. Science 251 , 944–947 (1991).
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).
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).
Garraghty, P.E. & Kaas, J.H. Dynamic features of sensory and motor maps. Curr. Opin. Neurobiol. 2, 522 –527 (1992).
Sanes, J.N. & Donoghue, J.P. Motor areas of the cerebral cortex . J. Clin. Neurophysiol. 11, 382– 396, (1994).
Rogan, M.T., Staeubli, U.V. & LeDoux, J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390, 604– 607 (1997).
McKernan, M.G. & Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607–611 ( 1997).
Ahissar, E. et al. Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science 257, 1412– 1415 (1992).
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).
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).
Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155– 158 (1995).
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).
Woody, C.D., Gruen, E. & Birt, D. Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res. 539, 76– 84 (1991).
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).
Darian, S.C. & Gilbert, C.D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737–740 (1994).
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).
Gilbert, C.D. Rapid dynamic changes in adult cerebral cortex. Curr. Opin. Neurobiol. 3, 100–103 (1993).
Donoghue, J.P. & Wise, S.P. The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J. Comp. Neurol. 212, 76–88 (1982).
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
Corresponding author
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/678
This article is cited by
-
De novo motor learning creates structure in neural activity that shapes adaptation
Nature Communications (2024)
-
Intracortical brain-computer interfaces in primates: a review and outlook
Biomedical Engineering Letters (2023)
-
NR1 Splicing Variant NR1a in Cerebellar Granule Neurons Constitutes a Better Motor Learning in the Mouse
The Cerebellum (2023)
-
Small, correlated changes in synaptic connectivity may facilitate rapid motor learning
Nature Communications (2022)
-
Epidural cerebellar stimulation drives widespread neural synchrony in the intact and stroke perilesional cortex
Journal of NeuroEngineering and Rehabilitation (2021)