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The Journal of Neuroscience, April 29, 2009, 29(17):5681-5689; doi:10.1523/JNEUROSCI.6058-08.2009

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Development/Plasticity/Repair
Propriospinal Bypass of the Serotonergic System That Can Facilitate Stepping

Yury Gerasimenko,^1,2 Pavel Musienko,¹ Irina Bogacheva,¹ Tatiana Moshonkina,¹ Alexandr Savochin,¹ Igor Lavrov,² Roland R. Roy,^2,3 and V. Reggie Edgerton^2,3,4

¹Pavlov Institute of Physiology, St. Petersburg 199034, Russia, and Departments of ²Physiological Science and ³Neurobiology and ⁴Brain Research Institute, University of California, Los Angeles, Los Angeles, California 90095

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 neurotransmitter systems mediating spinal locomotion in response to epidural spinal cord stimulation (ES) have not been identified. Here, we examine the role of the serotonergic system in regulating locomotor behavior of decerebrated cats during ES at L4–L5. ES elicited coordinated, weight-bearing, hindlimb stepping with plantar foot placement on a moving treadmill belt. Ketanserin [a 5-hydroxytryptamine (serotonin) (5-HT)_2/7 receptor antagonist] depressed this locomotor activity: only weak rhythmic movements without plantar foot placement and depressed EMG activity were observed. Cyproheptadine, a nonselective 5-HT blocker, prevented facilitation of stepping by epidural stimulation. These data demonstrate an important role of the serotonergic system in facilitating locomotion in the presence of epidural stimulation. In the presence of ketanserin, passive movements of one forelimb in a step-like manner immediately induced stepping of both hindlimbs with EMG patterns similar to those observed with ES without ketanserin. Thus, a non-5-HT-dependent spinal circuitry projecting from the cervical to the lumbar region of the spinal cord can facilitate stepping. The specific neurotransmitters responsible for this forelimb-facilitated stepping of the hindlimbs are unknown. These data suggest that a 5-HT_2/7 receptor-dependent pathway that processes hindlimb locomotor-like proprioception to facilitate hindlimb stepping can be complemented with proprioceptive afferents from the forelimbs via a non-5-HT_2/7 receptor neurotransmitter system. Thus, different neurotransmitter receptor systems can be used to mediate the same type of sensory event, i.e., locomotor-like proprioception to facilitate the same motor task, i.e., hindlimb stepping.

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Received Dec. 19, 2008; revised Feb. 11, 2009; accepted March 31, 2009.

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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