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The Journal of Neuroscience, April 18, 2007, 27(16):4460-4471; doi:10.1523/JNEUROSCI.2302-06.2007

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Development/Plasticity/Repair
Changes in Motoneuron Properties and Synaptic Inputs Related to Step Training after Spinal Cord Transection in Rats

Jeffrey C. Petruska,¹ Ronaldo M. Ichiyama,² Devin L. Jindrich,² Eric D. Crown,² Keith E. Tansey,² Roland R. Roy,² V. Reggie Edgerton,² and Lorne M. Mendell¹

¹Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, New York 11794-5230, and ²Department of Physiological Sciences, University of California, Los Angeles, Los Angeles, California 90095-1527

Correspondence should be addressed to Dr. Lorne M. Mendell, Department of Neurobiology and Behavior, State University of New York at Stony Brook, 550 Life Sciences Building, Stony Brook, NY 11794-5230. Email: Lorne.Mendell{at}sunysb.edu

Although recovery from spinal cord injury is generally meager, evidence suggests that step training can improve stepping performance, particularly after neonatal spinal injury. The location and nature of the changes in neural substrates underlying the behavioral improvements are not well understood. We examined the kinematics of stepping performance and cellular and synaptic electrophysiological parameters in ankle extensor motoneurons in nontrained and treadmill-trained rats, all receiving a complete spinal transection as neonates. For comparison, electrophysiological experiments included animals injured as young adults, which are far less responsive to training. Recovery of treadmill stepping was associated with significant changes in the cellular properties of motoneurons and their synaptic input from spinal white matter [ipsilateral ventrolateral funiculus (VLF)] and muscle spindle afferents. A strong correlation was found between the effectiveness of step training and the amplitude of both the action potential afterhyperpolarization and synaptic inputs to motoneurons (from peripheral nerve and VLF). These changes were absent if step training was unsuccessful, but other spinal projections, apparently inhibitory to step training, became evident. Greater plasticity of axonal projections after neonatal than after adult injury was suggested by anatomical demonstration of denser VLF projections to hindlimb motoneurons after neonatal injury. This finding confirmed electrophysiological measurements and provides a possible mechanism underlying the greater training susceptibility of animals injured as neonates. Thus, we have demonstrated an "age-at-injury"-related difference that may influence training effectiveness, that successful treadmill step training can alter electrophysiological parameters in the transected spinal cord, and that activation of different pathways may prevent functional improvement.

Key words: spinal cord injury; locomotion; training; activity-dependent plasticity; proprioception; propriospinal; electrophysiology

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Received May 31, 2006; revised Feb. 21, 2007; accepted Feb. 26, 2007.

Correspondence should be addressed to Dr. Lorne M. Mendell, Department of Neurobiology and Behavior, State University of New York at Stony Brook, 550 Life Sciences Building, Stony Brook, NY 11794-5230. Email: Lorne.Mendell{at}sunysb.edu

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