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The Journal of Neuroscience, June 4, 2008, 28(23):6022-6029; doi:10.1523/JNEUROSCI.0080-08.2008

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Development/Plasticity/Repair
Epidural Stimulation Induced Modulation of Spinal Locomotor Networks in Adult Spinal Rats

Igor Lavrov,¹ Christine J. Dy,¹ Andy J. Fong,⁴ Yury Gerasimenko,^1,5 Grégoire Courtine,⁶ Hui Zhong,¹ Roland R. Roy,^1,3 and V. Reggie Edgerton^1,2,3

¹Departments of Physiological Science and ²Neurobiology, and ³Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095, ⁴Bioengineering Option, California Institute of Technology, Pasadena, California 91125, ⁵Pavlov Institute of Physiology, St. Petersburg 199034, Russia, and ⁶University of Zurich, CH-8006 Zurich, Switzerland

Correspondence should be addressed to Dr. V. Reggie Edgerton, Department of Physiological Science, University of California, Los Angeles, 621 Charles E. Young Drive LS 1804, Los Angeles, CA 90095-1527. Email: vre{at}ucla.edu

The importance of the in vivo dynamic nature of the circuitries within the spinal cord that generate locomotion is becoming increasingly evident. We examined the characteristics of hindlimb EMG activity evoked in response to epidural stimulation at the S1 spinal cord segment in complete midthoracic spinal cord-transected rats at different stages of postlesion recovery. A progressive and phase-dependent modulation of monosynaptic (middle) and long-latency (late) stimulation-evoked EMG responses was observed throughout the step cycle. During the first 3 weeks after injury, the amplitude of the middle response was potentiated during the EMG bursts, whereas after 4 weeks, both the middle and late responses were phase-dependently modulated. The middle- and late-response magnitudes were closely linked to the amplitude and duration of the EMG bursts during locomotion facilitated by epidural stimulation. The optimum stimulation frequency that maintained consistent activity of the long-latency responses ranged from 40 to 60 Hz, whereas the short-latency responses were consistent from 5 to 130 Hz. These data demonstrate that both middle and late evoked potentials within a motor pool are strictly gated during in vivo bipedal stepping as a function of the general excitability of the motor pool and, thus, as a function of the phase of the step cycle. These data demonstrate that spinal cord epidural stimulation can facilitate locomotion in a time-dependent manner after lesion. The long-latency responses to epidural stimulation are correlated with the recovery of weight-bearing bipedal locomotion and may reflect activation of interneuronal central pattern-generating circuits.

Key words: CPG; spinal cord stimulation; locomotion; spinal cord; spinal cord injury; synaptic plasticity

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Received Jan. 8, 2008; revised April 28, 2008; accepted May 2, 2008.

Correspondence should be addressed to Dr. V. Reggie Edgerton, Department of Physiological Science, University of California, Los Angeles, 621 Charles E. Young Drive LS 1804, Los Angeles, CA 90095-1527. Email: vre{at}ucla.edu

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