Journal of Neurophysiology, Vol 72, Issue 2 847-860, Copyright © 1994 by APS

ARTICLES

Time course of locomotor recovery and functional regeneration in spinal cord-transected lamprey: in vitro preparations

A. D. McClellan
Division of Biological Sciences, University of Missouri, Columbia 65211.

1. Previous studies indicate that after transection of the rostral spinal cord, larval lamprey begin to recover locomotor behavior 2 wk posttransection and recovery is complete at approximately 8 wk. To examine the mechanisms underlying behavioral recovery after spinal cord transection, in the present study the time course and extent of recovery of locomotor function was examined in in vitro brain/spinal cord preparations. With these preparations the contributions of functional regeneration of descending brain stem projections to recovery of spinal locomotor function can be examined in the absence of mechanosensory inputs and descending propriospinal relay systems. 2. In in vitro preparations from normal lamprey, stimulation in brain stem locomotor regions resulted in direct descending activation of locomotor networks in the rostral, middle, and caudal spinal cord. 3. At 4 wk posttransection, in vitro locomotor activity was usually confined to the rostral spinal cord a few millimeters below the transection site. At 8 wk posttransection locomotor activity was present in both the rostral and middle spinal cord, and spinal locomotor networks at these levels could be directly activated by restored descending projections from the brain stem. 4. At 16-32 wk posttransection locomotor activity similar to that seen in normal animals was present along the spinal cord. Additional manipulations suggest that at 32 wk posttransection descending axons from brain stem command/initiation neurons had grown for relatively long distances and could directly activate the locomotor networks in the caudal spinal cord. At each recovery time examined the ranges of locomotor parameters (cycle time, burst proportion, and intersegmental phase lag) overlapped with those in normal animals. 5. In vitro locomotor activity in spinal cord-transected animals could be recorded at progressively more caudal levels below the transection site during the course of recovery. However, locomotor activity in in vitro preparations occurred for shorter distances below the lesion than in whole animals at comparable recovery times. 6. Our recent double-labeling experiments suggest that behavioral recovery in spinal cord-transected lamprey is largely due to true regeneration of preexisting descending axons rather than development of new descending projections. Thus, these results in conjunction with our behavioral, in vitro, and anatomic data suggest that functional regeneration of descending axons from the brain, as well as other mechanisms such as descending propriospinal relay systems and mechanosensory inputs, account for the gradual restoration of locomotor function in spinal cord-transected lamprey.

This article has been cited by other articles:

				A. D. McClellan, M. O. Kovalenko, J. A. Benes, and D. J. Schulz Spinal Cord Injury Induces Changes in Electrophysiological Properties and Ion Channel Expression of Reticulospinal Neurons in Larval Lamprey J. Neurosci., January 16, 2008; 28(3): 650 - 659. [Abstract] [Full Text] [PDF]

				A. W. Jackson, F. A. Pino, E. D. Wiebe, and A. D. McClellan Movements and Muscle Activity Initiated by Brain Locomotor Areas in Semi-Intact Preparations From Larval Lamprey J Neurophysiol, May 1, 2007; 97(5): 3229 - 3241. [Abstract] [Full Text] [PDF]

				E. Zaporozhets, K. C. Cowley, and B. J. Schmidt Propriospinal neurons contribute to bulbospinal transmission of the locomotor command signal in the neonatal rat spinal cord J. Physiol., April 15, 2006; 572(2): 443 - 458. [Abstract] [Full Text] [PDF]

				A. W. Jackson, D. F. Horinek, M. R. Boyd, and A. D. McClellan Disruption of Left-Right Reciprocal Coupling in the Spinal Cord of Larval Lamprey Abolishes Brain-Initiated Locomotor Activity J Neurophysiol, September 1, 2005; 94(3): 2031 - 2044. [Abstract] [Full Text] [PDF]

				S. J. Zottoli and M. M. Freemer Recovery of C-starts, equilibrium and targeted feeding after whole spinal cord crush in the adult goldfish Carassius auratus J. Exp. Biol., September 1, 2003; 206(17): 3015 - 3029. [Abstract] [Full Text] [PDF]

				M. R. Boyd and A. D. McClellan Changes in locomotor activity parameters with variations in cycle time in larval lamprey J. Exp. Biol., December 1, 2002; 205(23): 3707 - 3716. [Abstract] [Full Text] [PDF]

				L. Guan, T. Kiemel, and A. H. Cohen Impact of movement and movement-related feedback on the lamprey central pattern generator for locomotion J. Exp. Biol., January 7, 2001; 204(13): 2361 - 2370. [Abstract] [Full Text] [PDF]

				W. L. Miller and K. A. Sigvardt Extent and Role of Multisegmental Coupling in the Lamprey Spinal Locomotor Pattern Generator J Neurophysiol, January 1, 2000; 83(1): 465 - 476. [Abstract] [Full Text] [PDF]

				A. D. McClellan and A. Hagevik Descending Control of Turning Locomotor Activity in Larval Lamprey: Neurophysiology and Computer Modeling J Neurophysiol, July 1, 1997; 78(1): 214 - 228. [Abstract] [Full Text] [PDF]