Abstract
The time course of recovery of locomotor function was examined with kinematic analysis and muscle recordings in larval lampreys 2–32 weeks after rostral spinal cord transection at the level of the third gill (∼10% of body length, BL). Animals began to recover locomotor movements within 2–4 weeks of spinal cord transection, but the amplitude of locomotor movements in the tail region was less than in normal animals. At 2 weeks post-transection, locomotor activity was limited to 20% BL, and at 3 weeks after spinal transection activity could be recorded at least as far as 40% BL. At 4 weeks after spinal transection, well-coordinated locomotor muscle activity was often present as far as 60% BL. At 8 weeks of recovery and longer, well-coordinated locomotor activity was present consistently at least as far as 60% BL, and the amplitudes of locomotor movements were restored to normal values. At each recovery time examined the ranges of locomotor parameters (cycle time, burst proportion, and intersegmental phase lag) overlapped with those in normal animals. Thus, the gradual recovery of the amplitude of locomotor movements in the caudal body is associated with the gradual return of coordinated muscle activity at progressively more caudal levels along the body. The mechanisms responsible for this gradual recovery of locomotor function are discussed in relation to our recent anatomical and in vitro studies.
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References
Ayers J (1989) Recovery of oscillator function following spinal regeneration in the sea lamprey. In: Jacklet J (ed) Neuronal and cellular oscillators. Dekker, New York, pp 371–405
Bainbridge R (1958) The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. J Exp Biol 35:109–133
Beattie MS, Bresnahan JC, Lopate G (1990) Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs. J Neurobiol 21:1108–1122
Bernstein JJ, Gelderd JB (1970) Regeneration of the long spinal tracts in the goldfish. Brain Res 20:33–38
Clarke JDW, Alexander R, Holder N (1988) Regeneration of descending axons in the spinal cord of the axolotl. Neurosci Lett 89:1–6
Coggeshall RE, Youngblood CS (1983) Recovery from spinal transection in fish: regrowth of axons past the transection. Neurosci Lett 38:227–231
Cohen AH, Mackler SA, Selzer ME (1986) Functional regeneration following spinal transection demonstrated in the isolated spinal cord of the larval sea lamprey. Proc Nat Acad Sci 83:2763–2766
Davis BM, Duffy MT, Simpson SB (1989) Bulbospinal and intraspinal connections in normal and regenerated salamander spinal cord. Exp Neurol 103:41–51
Davis BM, Ayers JL, Koran L, Carlson J, Andersen MC, Simpson SB (1990) Time course of salamander spinal cord regeneration and recovery of swimming: HRP retrograde pathway tracing and kinematic analysis. Exp Neurol 108:198–213
Davis GR, McClellan AD (1993) Time course of anatomical regeneration of descending brainstem neurons and behavioral recovery in spinal-transected lamprey. Brain Res 602:131–137
Eidelberg E (1981) Consequences of spinal cord lesions upon motor function, with special reference to locomotor activity. Prog Neurobiol 17:185–202
Forehand CJ, Farel PB (1982) Anatomical and behavioral recovery from the effects of spinal cord transection: dependence on metamorphosis in anuran larvae. J Neurosci 2:654–662
Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Brooks V (ed) Handbook of physiology, motor control. American Physiological Society, Washington DC, pp 1179–1236
Grillner S, Kashin S (1976) On the generation and performance of swimming in fish. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion, vol 18. Plenum, New York, pp 181–202
Hanson LH, King EL, Howell JH, Smith AJ (1974) A culture method for sea lamprey larvae. Progressive Fish-Culturist 36:122–128
Hasan SJ, Nelson BH, Valenzuela JI, Keirstead HS, Shull SE, Ethell DW, Steeves JD (1991) Functional repair of transected spinal cord in embryonic chick. Restor Neurol Neurosci 2:137–154
Hooker D (1925) Studies on regeneration in the spinal cord. III. Re-establishment of anatomical and physiological continuity after transection in frog tadpoles. J Comp Neurol 38:315–347
Kiernan JA (1979) Hypotheses concerned with axonal regeneration in the mammalian nervous system. Biol Rev 54:155–197
Kopell N, Ermentrout GB (1990) Phase transitions and other phenomena in chains of coupled oscillators. SIAM J Appl Math 50:1014–1052
Lee MT (1982) Regeneration and functional reconnection of an identified vertebrate central neuron. J Neurosci 2:1793–1811
Mackler SA, Selzer ME (1987) Specificity of synaptic regeneration in the spinal cord of the larval sea lamprey. J Physiol (Lond) 388:183–198
Manion PJ, Stauffer TM (1970) Metamorphosis of the landlocked sea lamprey, Petromyzon marinus. J Fish Res Board Can 27:1735–1746
Matsushima T, Grillner S (1992) Neural mechanisms of intersegmental coordination in lamprey: local excitability changes modify the phase coupling along the spinal cord. J Neurophysiol 67:373–388
McClellan AD (1984) Descending control and sensory gating of “fictive” swimming and turning responses elicited in an in vitro brainstem/spinal cord preparation of the lamprey. Brain Res 302:151–162
McClellan AD (1986) Command systems for initiating locomotor responses in fish and amphibians parallels to initiation of locomotion in mammals. In: Grillner S, Herman R, Stein P, Stuart D (eds) Neurobiology of vertebrate locomotion. Wennergren Symposium Series, MacMillan, Basingstoke, pp 1–20
McClellan AD (1987) In vitro CNS preparations: unique approaches to the study of command and pattern generation systems in motor systems, J Neurosci Meth 21:251–264
McClellan AD (1988) Functional regeneration of descending brainstem command pathways for locomotion demonstrated in the in vitro lamprey CNS. Brain Res 448:339–345
McClellan AD (1989) Control of locomotion in a lower vertebrate, the lamprey: brainstem command systems and spinal cord regeneration. Am Zool 29:37–51
McClellan AD (1990a) Locomotor recovery in spinal-transected lamprey: role of functional regeneration of descending axons from brainstem locomotor command neurons. Neuroscience 37:781–798
McClellan AD (1990b) Locomotor recovery in spinal-transected lamprey: regenerated spinal coordinating neurons and mechanosensory inputs couple locomotor activity across a spinal transection. Neuroscience 35:675–685
McClellan AD (1992) Functional regeneration and recovery of locomotor activity in spinally transected lamprey. J Exp Zool 260:274–287
McClellan AD, Sigvardt KA (1988) Features of entrainment of spinal pattern generators for locomotor activity in the lamprey. J Neurosci 8:133–145
Pettigrew RK, Windle WF (1976) Factors in recovery from spinal cord injury. Exp Neurol 53:815–829
Piatt J (1955) Regeneration of the spinal cord in the salamander. J Exp Zool 29:177–208
Puchala E, Windle WF (1977) The possibility of structural and functional restitution after spinal cord injury. A review. Exp Neurol 55:1–42
Rovainen CM (1976) Regeneration of Muller and Mauthner axons after spinal transection in larval lampreys. J Comp Neurol 168:545–554
Rovainen CM (1979) Neurobiology of lampreys. Physiol Rev 59:1007–1077
Rovainen CM (1985) Effects of groups of propriospinal interneurons on fictive swimming in the isolated spinal cord of the lamprey. J Neurophysiol 54:299–317
Schwab ME (1990) Myelin-associated inhibitors of neurite growth and regeneration in the CNS. Trends Neurosci 13:452–456
Selzer M (1978) Mechanisms of functional recovery and regeneration after spinal cord transection in larval lampreys. J Physiol (Lond) 277:395–408
Shimizu I, Oppenheim R, O'Brien M, Schneiderman A (1990) Anatomical and functional recovery following spinal cord transection in the chick embryo. J Neurobiol 21:918–937
Sigvardt K, Kopell N, Ermentrout GB, Remler MP (1991) Effects of local oscillator frequency on intersegmental coordination in the lamprey locomotory CPG: theory and experiment. Soc Neurosci Abstr 17:122
Stein PSG (1978) Motor systems, with special reference to locomotion. Annu Rev Neurosci 1:61–81
Swain GP 1989 CNS regeneration and behavioral recovery following spinal cord transection in the sea lamprey Petromyzon marinus. Doctoral dissertation. Northeastern University
Tunstall MJ, Roberts A (1991) Longitudinal coordination of motor output during swimming in Xenopus embryos. Proc R Soc Lond B 244:27–32
Wallen P, 1982 Spinal mechanisms controlling locomotion in dog fish and lamprey. Acta Physiol Scand [Suppl 503]: 1–45
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Davis, G.R., Troxel, M.T., Kohler, V.J. et al. Time course of locomotor recovery and functional regeneration in spinal-transected lamprey: kinematics and electromyography. Exp Brain Res 97, 83–95 (1993). https://doi.org/10.1007/BF00228819
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DOI: https://doi.org/10.1007/BF00228819