Central nervous system lesion triggers inappropriate pathway choice in adult vertebrate system

Bentley, Adrienne P.; Zottoli, Steven J.

doi:10.1016/0006-8993(93)90673-b

Cited by 19 publications

(9 citation statements)

References 17 publications

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“…(3) They may have regrown past the transection site but exited the spinal cord via a ventral root. It has been shown in goldfish that, following a crush lesion of the medulla, spinal projection axons, including the MAC, can grow erroneously and even preferentially into the peripheral nervous system via the first ventral root (Titmus et al, 1986;Bentley and Zottoli, 1993;Zottoli et al, 1994). We cannot conclusively rule out this possibility.…”

Section: Ascending and Descending Projections After Spinal Cord Transmentioning

confidence: 86%

Axonal regrowth after spinal cord transection in adult zebrafish

et al. 1997

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Using axonal tracers, we characterized the neurons projecting from the brain to the spinal cord as well as the terminal fields of ascending spinal projections in the brain of adult zebrafish with unlesioned or transected spinal cords. Twenty distinct brain nuclei were found to project to the spinal cord. These nuclei were similar to those found in the closely related goldfish, except that additionally the parvocellular preoptic nucleus, the medial octavolateralis nucleus, and the nucleus tangentialis, but not the facial lobe, projected to the spinal cord in zebrafish. Terminal fields of axons, visualized by anterograde tracing, were seen in the telencephalon, the diencephalon, the torus semicircularis, the optic tectum, the eminentia granularis, and throughout the ventral brainstem in unlesioned animals. Following spinal cord transection at a level approximately 3.5 mm caudal to the brainstem/spinal cord transition zone, neurons in most brain nuclei grew axons beyond the transection site into the distal spinal cord to the level of retrograde tracer application within 6 weeks. However, the individually identifiable Mauthner cells were never seen to do so up to 15 weeks after spinal cord transection. Nearly all neurons survived axotomy, and the vast majority of axons that had grown beyond the transection site belonged to previously axotomized neurons as shown by double tracing. Terminal fields were not re-established in the torus semicircularis and the eminentia granularis following spinal cord transection.

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Section: Ascending and Descending Projections After Spinal Cord Transmentioning

confidence: 86%

Axonal regrowth after spinal cord transection in adult zebrafish

et al. 1997

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“…Individual differences in postoperative bleeding or cellular reactions at the lesion site are also factors that could have affected axon regeneration. Alternatively, regrowing axons may have exited the spinal cord through the ventral roots, as has been observed in goldfish (Bentley and Zottoli, 1993).…”

Section: Supraspinal Descending Axons Regrow In the Spinal Gray Mattermentioning

confidence: 90%

Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish

Becker

2001

J of Comparative Neurology

109

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We analyzed pathway choices of regenerating, mostly supraspinal, descending axons in the spinal cord of adult zebrafish and the cellular changes in the spinal cord caudal to a lesion site after complete spinal transection. Anterograde tracing (by application of the tracer rostral to the spinal lesion site) showed that significantly more descending axons (74%) regenerated in the spinal gray matter of the caudal spinal cord than would be expected from random growth. Retrograde tracing (by application of the tracer caudal to the spinal lesion site) showed that, rostral to the lesion, most of these axons (80%) extended into the major white matter tracts. Thus, ventral descending tracts often were devoid of labeled axons caudal to a spinal lesion but contained many axons rostral to the lesion in the same animals, indicating a pathway switch of descending axons from the white matter to the gray matter. Ascending axons of spinal neurons were not observed regrowing to the rostral tracer application site; therefore, they most likely did not contribute to the axonal populations analyzed. A macrophage/microglia response within 2 days of spinal cord transection, along with phagocytosis of myelin, was observed caudal to the transection by immunohistochemistry and electron microscopy. Nevertheless, caudal to the lesion, descending tracts in the white matter were filled with myelin debris during the time of axonal regrowth, at least up to 6 weeks postlesion. We suggest that the spontaneous regeneration of axons of supraspinal origin after spinal cord transection in adult zebrafish may be due in part to the axons' ability to negotiate novel pathways in the spinal cord gray matter.

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“…The age of the fish, subtle differences in the crush wound or the wound level may limit the return of behavior. In addition, regenerating central nervous system (CNS) neurons are known to make inappropriate pathway choices into the peripheral nervous system just caudal to an SML crush (Bentley and Zottoli, 1993;Zottoli et al, 1994). This inappropriate pathway choice may limit, delay or prevent the return of behavior caudal to the wound.…”

Section: Recovery Of Behavior Was Due To Morphological Regenerationmentioning

confidence: 99%

“…However, the majority of M-axons sprout extensively both rostrally and caudally for distances up to 5·mm within the CNS at 22°C (Zottoli et al, 1988). Few of the caudally projecting axons cross the wound site and those that do tend to be within or directed towards the first ventral root (Bentley and Zottoli, 1993;Zottoli et al, 1994).…”

Section: Recovery Of Behavior Was Due To Morphological Regenerationmentioning

confidence: 99%

Recovery of C-starts, equilibrium and targeted feeding after whole spinal cord crush in the adult goldfishCarassius auratus

Zottoli

Freemer

2003

Journal of Experimental Biology

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SUMMARYCentral nervous system neurons of many adult teleost fish are capable of regrowth across spinal cord lesions, which may result in behavioral recovery of swimming. Since there have been few, if any, studies that examine the return of behaviors other than swimming, we provide a quantitative analysis of the recovery of C-starts that occur in adult goldfish after spinal cord injury. In addition, we include a qualitative analysis of the return of targeted feeding and equilibrium. Whole spinal cord crushes near the junction of the brain and spinal cord [spinomedullary level (SML)] were made in 45 experimental fish. Eight sham-operated goldfish served as controls for the effects of the surgery procedures alone. After spinal cord crush and recovery from the anesthetic, experimental fish lay on their sides with no movement caudal to the wound. The fish were monitored for the return of behaviors for up to 190 days postoperatively. Twenty-five fish survived the course of this study. Of these fish, 12 regained equilibrium and C-starts, two regained equilibrium but not C-starts, and 11 did not regain equilibrium (one of these did display a C-start). Twenty-two of the 25 experimental fish that survived the 190 days were able to target food from the water surface. Quantitative analysis of recovered C-starts in this study revealed that the probability of eliciting the response is reduced, that latencies from stimulus to response are longer and that movement parameters (i.e. angles, distance and velocity)are reduced compared with those of sham-operated control animals for up to 190 days postoperatively. The recovery of C-starts, equilibrium and targeted feeding was due to re-growth across the wound site, since re-crushing the spinal cord at the SML resulted in the loss of these behaviors. Mauthner cells are known to initiate C-starts in goldfish. Since the majority of M-axons that regrow across a crush wound associate with an inappropriate pathway (i.e. the first ventral root), it is unlikely that these cells play a major role in the return of C-starts. We propose that regeneration of Mauthner cell homologues across the wound site is responsible for the recovery of most C-starts. The identifiability of the M-cell and its homologues provides a unique opportunity to analyze the mechanisms underlying behavioral recovery at the cellular level.

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Central nervous system lesion triggers inappropriate pathway choice in adult vertebrate system

Cited by 19 publications

References 17 publications

Axonal regrowth after spinal cord transection in adult zebrafish

Axonal regrowth after spinal cord transection in adult zebrafish

Regenerating descending axons preferentially reroute to the gray matter in the presence of a general macrophage/microglial reaction caudal to a spinal transection in adult zebrafish

Recovery of C-starts, equilibrium and targeted feeding after whole spinal cord crush in the adult goldfishCarassius auratus

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