Anatomical and behavioral recovery from the effects of spinal cord transection: dependence on metamorphosis in anuran larvae

Abstract

This study of spinal cord injury in bullfrog (Rana catesbeiana) tadpoles using the neuroanatomical tracer horseradish peroxidase (HRP) was undertaken to determine (1) whether the same anatomical regions that normally give rise to ascending or descending spinal tracts do so following complete spinal cord transection and (2) whether the course of behavioral recovery could be related to the anatomical results. The results of this study show that (1) spinal cord continuity is readily restored in tadpoles subjected to spinal cord transection, but nerve fibers crossing the site of injury end within 1 to 2 mm of the lesion site; (2) tadpoles with spinal cord transections held through metamorphosis show, as juvenile frogs, restoration of lumbar projections from all brainstem regions that normally project to the lumbar spinal cord; (3) neither long ascending projections from dorsal root ganglion cells nor those from spinal neurons caudal to the transection traverse the transection site, even after metamorphosis; and (4) consistent with the anatomical results, tadpoles show only minimal behavioral recovery, but these same animals as juvenile frogs show recovery of behaviors that are dependent upon connections to supraspinal regions. In other experiments, [3H]thymidine or [3H]apo-HRP was combined with HRP histochemistry to determine if new brainstem neurons projecting to the spinal cord are born in the metamorphic period and if, in normal animals, brainstem projections to the lumbar spinal cord persist through metamorphosis. We found no evidence that neurons with lumbar spinal cord projections are born during metamorphosis; however, evidence was found that most brainstem neurons that project to the lumbar spinal cord before metamorphosis retain this projection in the juvenile frog.

Axonal regeneration of descending brain neurons in larval lamprey demonstrated by retrograde double labeling

“…In the bullfrog, autoradiography experiments indicate that very few descending brain neurons are ''born'' during metamorphosis, and double-label experiments demonstrate that many brainstem neurons that project to the lumbar spinal cord in tadpoles retain this projection as adults (Forehand and Farel, 1982). In the salamander, after transection of the thoracic spinal cord, the percentages of double labeling of descending brain neurons resulting from focal injection of tracers to the spinal cord are 6-27% compared with 3-27% double labeling when both tracers are applied simultaneously (Davis et al, 1989b;Garner et al, 1990).…”

Metamorphosis alters the response to spinal cord transection in Xenopus laevis frogs

“…Studies of spinalized urodele amphibians showed almost complete recovery of function and cord integrity, even in adult stages ( Hibbard, 1963;Piatt, 1955). Anuran tadpoles also have been shown to reconstitute the cord and descending axons after spinal cord transection (Forehand and Farel, 1982;Michel and Reier, 1979). However, adult anurans seem incapable of spinal cord regeneration (Forehand and Farel, 1982;Piatt, 1955), although partial regeneration of the dorsal roots has been documented (Katzenstein and Bohn, 1984; Liuzzi and Lasek, 1985; Liuzzi and Lasek, 1986; Sah and Frank, 1984).…”

Adaptive plasticity ofXenopus glial cells in vitro and after CNS fiber tract lesions in vivo

“…They are thus able to adapt to the state of the retinal axons. These changes were not observed in the case of oligodendrocytes in the spinal cord, where axon regeneration does not occur (Beattie et al, 1990;Forehand and Farel, 1982;Lang et al, 1995).…”

“…This occurred at 4 weeks and was unchanged 8 weeks after lesion, except that the gap between the cut ends gradually filled up with GFAP-and fibronectin-positive cells. Thus, in the Xenopus spinal cord where lesioned axons fail to regenerate (Beattie et al, 1990;Forehand and Farel, 1982;Lang et al, 1995), myelin markers in the vicinity of the cut axons persist. 04-expressing glia precursors and radial processes, both of which are present in the optic nerve, are not seen a t the lesion or elsewhere in the cord.…”