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The Journal of Neuroscience, December 14, 2005, 25(50):11738-11747; doi:10.1523/JNEUROSCI.1523-05.2005

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Development/Plasticity/Repair
Spinal Cord-Transected Mice Learn to Step in Response to Quipazine Treatment and Robotic Training

Andy J. Fong,^3,5 Lance L. Cai,⁵ Chad K. Otoshi,² David J. Reinkensmeyer,^7,8 Joel W. Burdick,^5,6 Roland R. Roy,⁴ and V. Reggie Edgerton^1,4

Departments of ¹Physiological Science and ²Neurobiology, ³Biomedical Engineering Interdepartmental Program, and ⁴Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095, Division of Engineering, ⁵Bioengineering and ⁶Mechanical Engineering Options, California Institute of Technology, Pasadena, California 91125, and Departments of ⁷Mechanical and Aerospace Engineering and ⁸Biomedical Engineering, University of California, Irvine, Irvine, California 92612

In the present study, concurrent treatment with robotic step training and a serotonin agonist, quipazine, generated significant recovery of locomotor function in complete spinal cord-transected mice (T7–T9) that otherwise could not step. The extent of recovery achieved when these treatments were combined exceeded that obtained when either treatment was applied independently. We quantitatively analyzed the stepping characteristics of spinal mice after alternatively administering no training, manual training, robotic training, quipazine treatment, or a combination of robotic training with quipazine treatment, to examine the mechanisms by which training and quipazine treatment promote functional recovery. Using fast Fourier transform and principal components analysis, significant improvements in the step rhythm, step shape consistency, and number of weight-bearing steps were observed in robotically trained compared with manually trained or nontrained mice. In contrast, manual training had no effect on stepping performance, yielding no improvement compared with nontrained mice. Daily bolus quipazine treatment acutely improved the step shape consistency and number of steps executed by both robotically trained and nontrained mice, but these improvements did not persist after quipazine was withdrawn. At the dosage used (0.5 mg/kg body weight), quipazine appeared to facilitate, rather than directly generate, stepping, by enabling the spinal cord neural circuitry to process specific patterns of sensory information associated with weight-bearing stepping. Via this mechanism, quipazine treatment enhanced kinematically appropriate robotic training. When administered intermittently during an extended period of robotic training, quipazine revealed training-induced stepping improvements that were masked in the absence of the pharmacological treatment.

Key words: locomotion; quipazine; serotonin; robotics; spinal cord injury; SCI; motor learning; training; plasticity

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Received Aug 6, 2004; revised October 27, 2005; accepted November 5, 2005.

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