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The Journal of Neuroscience, July 16, 2008, 28(29):7426-7434; doi:10.1523/JNEUROSCI.1078-08.2008

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Behavioral/Systems/Cognitive
Pyramidal Tract Stimulation Restores Normal Corticospinal Tract Connections and Visuomotor Skill after Early Postnatal Motor Cortex Activity Blockade

Iran Salimi,^1,2 Kathleen M. Friel,¹ and John H. Martin^1,3,4,5

¹Department of Neuroscience, Columbia University, New York, New York 10032, ²Department of Neurosurgery, Mount Sinai Medical School, New York, New York 10029, and Departments of ³Psychiatry and ⁴Neurological Surgery, and ⁵The New York State Psychiatric Institute, Columbia University, New York, New York 10032

Correspondence should be addressed to Dr. John H. Martin, Department of Neuroscience, Columbia University, 1051 Riverside Drive, New York, NY 10032. Email: jm17{at}columbia.edu

Motor development depends on forming specific connections between the corticospinal tract (CST) and the spinal cord. Blocking CST activity in kittens during the critical period for establishing connections with spinal motor circuits results in permanent impairments in connectivity and function. The changes in connections are consistent with the hypothesis that the inactive tract is less competitive in developing spinal connections than the active tract. In this study, we tested the competition hypothesis by determining whether activating CST axons, after previous silencing during the critical period, abrogated development of aberrant corticospinal connections and motor impairments. In kittens, we inactivated motor cortex by muscimol infusion between postnatal weeks 5 and 7. Next, we electrically stimulated CST axons in the medullary pyramid 2.5 h daily, between weeks 7 and 10. In controls (n = 3), CST terminations were densest within the contralateral deeper, premotor, spinal layers. After previous inactivation (n = 3), CST terminations were densest within the dorsal, somatic sensory, layers. There were more ipsilateral terminations from the active tract. During visually guided locomotion, there was a movement endpoint impairment. Stimulation after inactivation (n = 6) resulted in significantly fewer terminations in the sensory layers and more in the premotor layers, and fewer ipsilateral connections from active cortex. Chronic stimulation reduced the current threshold for evoking contralateral movements by pyramidal stimulation, suggesting strengthening of connections. Importantly, stimulation significantly improved stepping accuracy. These findings show the importance of activity-dependent processes in specifying CST connections. They also provide a strategy for harnessing activity to rescue CST axons at risk of developing aberrant connections after CNS injury.

Key words: corticospinal tract; development; locomotion; motor cortex; movement; motion; motor activity; spinal cord

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Received March 12, 2008; revised May 23, 2008; accepted June 10, 2008.

Correspondence should be addressed to Dr. John H. Martin, Department of Neuroscience, Columbia University, 1051 Riverside Drive, New York, NY 10032. Email: jm17{at}columbia.edu

This article has been cited by other articles:

				S. Chakrabarty, B. Shulman, and J. H. Martin Activity-Dependent Codevelopment of the Corticospinal System and Target Interneurons in the Cervical Spinal Cord J. Neurosci., July 8, 2009; 29(27): 8816 - 8827. [Abstract] [Full Text] [PDF]

				M. Brus-Ramer, J. B. Carmel, and J. H. Martin Motor Cortex Bilateral Motor Representation Depends on Subcortical and Interhemispheric Interactions J. Neurosci., May 13, 2009; 29(19): 6196 - 6206. [Abstract] [Full Text] [PDF]

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