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J Neurophysiol (January 22, 2003). doi:10.1152/jn.00900.2002
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Submitted on October 8, 2002
Accepted on January 18, 2003

A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex

Alexander Wolters1, Friedhelm Sandbrink1, Antje Schlottmann1, Erwin Kunesch1, Katja Stefan1, Leonardo G. Cohen2, Reiner Benecke1, and Joseph Classen3*

1 Neurology, University of Rostock, Rostock, Germany
2 Human Cortical Physiology Section, NINDS, NIH, Bethesda, MD, USA
3 Neurology, University of Rostock, Rostock, Germany; Neurology, University of Wuerzburg, Wuerzburg, Germany

* To whom correspondence should be addressed. E-mail: joseph.classen{at}mail.uni-wuerzburg.de.

Synaptic plasticity is conspicuously dependent on the temporal order of the pre-and postsynaptic activity. Human motor cortical excitability can be increased by a paired associative stimulation (PAS) protocol. Here we show that it can also be decreased, by minimally changing the interval between the two associative stimuli. Corticomotor excitability of the abductor pollicis brevis (APB) representation was tested before and after repetitively pairing of single right median nerve simulation with single pulse transcranial magnetic stimulation (TMS) delivered over the optimal site for activation of the contralateral APB. Following PAS, depression of TMS-evoked motor evoked potentials (MEPs) was induced only when the median nerve stimulation preceded the TMS pulse by 10ms, while enhancement of cortical excitability was induced using an interstimulus interval of 25ms, suggesting an important role of the sequence of cortical events triggered by the two stimulation modalities. Experiments using F-wave studies and electrical brainstem-stimulation indicated that the site of the plastic changes underlying the decrease of MEP-amplitudes following PAS(10ms) was within the motor cortex. MEP-amplitudes remained depressed for approximately 90 min. The decrease of MEP amplitudes was blocked when PAS(10ms) was performed under the influence of dextromethorphan, an N-methyl-D-aspartate (NMDA)-receptor antagonist, or nimodipine, an L-type voltage gated calcium-channel antagonist. The physiological profile of the depression of human motor cortical excitability following PAS(10ms) suggests long-term depression of synaptic efficacy to be involved. Together with earlier findings this study suggests that strict temporal Hebbian rules govern the induction of LTP/LTD- like phenomena in vivo in the human primary motor cortex.




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