Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats

Murray, Marion; Me, Goldberger

doi:10.1523/jneurosci.06-11-03205.1986

Cited by 103 publications

(32 citation statements)

References 47 publications

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“…Although there is evidence that deafferentation results in compensatory sprouting of surviving sensory neurons (Murray and Goldberger, 1986;Goldberger and Murray, 1988), several studies using WGA-HRP have found little indication of sprouting of C-fiber primary sensory afferents out of their normal termination zone into neighbouring denervated areas of spinal cord, unless the denervation is accompanied by a conditioning peripheral nerve lesion (Molander et al, 1988;LaMotte et al, 1989;McMahon and Kett-White, 1991;Florence et al, 1993). There are reports, however, that after deafferentation produced by pronase injection into the sciatic nerve, true collateral sprouting of apparently uninjured saphenous central terminals occurs into the neighbouring sciatic nerve terminal territory (LaMotte et al, 1989;LaMotte and Kapadia, 1993).…”

Section: Discussionmentioning

confidence: 99%

Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve

Doubell

Woolf

1997

J. Comp. Neurol.

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Peripheral nerve section induces sprouting of the central terminals of axotomized myelinated primary afferents outside their normal dorsoventral termination zones in lamina I, III, and IV of the dorsal horn into lamina II, an area that normally only receives unmyelinated C-fiber input. This axotomy-induced regenerative sprouting is confined to the somatotopic boundaries of the injured nerve in the spinal cord. We examined whether intact myelinated sciatic afferents are able to sprout novel terminals into neighbouring areas of the dorsal horn in the adult rat following axotomy of two test nerves, either the posterior cutaneous nerve of the thigh or the saphenous nerve. These peripheral nerves have somatotopically organized terminal areas in the dorsal horn that overlap in some areas and are contiguous in others, with that of the sciatic central terminal field. Two weeks after cutting either the posterior cutaneous or the saphenous nerve, intact sciatic myelinated fibers labelled with the B fragment of cholera toxin conjugated to horseradish peroxidase (B-HRP) sprouted into an area of lamina II normally only innervated by the adjacent injured test nerve. This collateral sprouting was strictly limited, however, to those particular areas of the dorsal horn where the A-fiber terminal field of the control sciatic and the C-fiber terminal field of the injured test nerve overlapped in the dorsoventral plane. No mediolateral sprouting was seen into those areas of neuropil solely innervated by the test nerve. We conclude that intact myelinated primary afferents do have the capacity to collaterally sprout, but that any resultant somatotopic reorganization of central projections is limited to the dorsoventral plane. These changes may contribute to sensory hypersensitivity at the edges of denervated skin.

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Section: Discussionmentioning

confidence: 99%

Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve

Doubell

Woolf

1997

J. Comp. Neurol.

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“…These neurons are able to regenerate after peripheral axotomy. The central projections of dorsal root afferents sprout after removal of adjacent dorsal roots (for review, see Murray, 1993) or after central denervation that partially denervates the dorsal horn (Murray and Goldberger, 1986). Dorsal root axons are also capable of regenerating into transplants of fetal tissue placed into the spinal cord after axotomy (Tessler et al, 1988) or after removal of their normal targets by excitotoxins (Nothias and Peschanski.…”

Section: Phosphorylated Maplb and Morphological Plasticity In The Adumentioning

confidence: 99%

Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity

et al. 1996

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Microtubule-associated protein IB (MAP1B) is the first MAP to be detected in the developing nervous system, and it becomes markedly down-regulated postnatally. Its expression, particularly that of its phosphorylated isoform, is associated with axonal growth. To determine whether adult central nervous system (CNS) areas that retain immunoreactivity for MAP1B are associated with morphological plasticity, we compared the distribution of a phosphorylated MAP1B isoform (MAP1B-P) to the distribution of total MAP1B protein and MAP1B-mRNA. Although they were present only at very low levels, both protein and message were found ubiquitously in almost all adult CNS neurons. The intensity of staining, however, varied markedly among different regions, with only a few nuclei retaining relatively high levels. MAP1B-P was restricted to axons, whereas total MAP1B was present in cell bodies and processes. Relatively to total MAP1B protein and its mRNA, MAP1B-P levels decreased more dramatically with maturation, and they were detectable in only a few specific areas that underwent structural modifications. These included primary afferents and motor neurons, olfactory tubercles, habenular and raphe projections to interpeduncular nuclei, septum, and the hypothalamus. The distribution pattern of MAP1B-P was compared to that of the embryonic N-CAM rich in polysialic acid (PSA-NCAM). We found that the PSA-NCAM immunostaining was largely overlapped with that of MAP1B-P in the adult CNS. These results suggest that, like PSA-NCAM, MAP1B may be one of the molecules expressed during brain development that also plays a role in structural remodeling in the adult.

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“…Data from quantitative immunoelectron microscopy and receptor binding experiments showed that this change resulted from the degeneration of dorsal root afferents (17,18). In turtles, the dorsal root terminals were found in synaptic fields Ia, Ib, II and III, with some long fibers projecting to the contralateral dorsal horn (9).…”

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confidence: 99%

Substance P immunoreactivity in the lumbar spinal cord of the turtle Trachemys dorbigni following peripheral nerve injury

Partata

Krepsky

Xavier

et al. 2003

Braz J Med Biol Res

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Immunoreactive substance P was investigated in turtle lumbar spinal cord after sciatic nerve transection. In control animals immunoreactive fibers were densest in synaptic field Ia, where the longest axons invaded synaptic field III. Positive neuronal bodies were identified in the lateral column of the dorsal horn and substance P immunoreactive varicosities were observed in the ventral horn, in close relationship with presumed motoneurons. Other varicosities appeared in the lateral and anterior funiculi. After axotomy, substance P immunoreactive fibers were reduced slightly on the side of the lesion, which was located in long fibers that invaded synaptic field III and in the varicosities of the lateral and anterior funiculus. The changes were observed at 7 days after axonal injury and persisted at 15, 30, 60 and 90 days after the lesion. These findings show that turtles should be considered as a model to study the role of substance P in peripheral axonal injury, since the distribution and temporal changes of substance P were similar to those found in mammals. Key wordsPeripheral nerve injury may result in significant changes in neuropeptide production and the development of neuropathic pain behavior (1). In rats, peripheral nerve sectioning leads to a marked quantitative decrease in the nerve of substance P, a peptide of 11 amino acids that is present in small primary afferents and plays an important role in pain sensation (2,3).The chemical structure of substance P is highly conserved in non-mammalian species, and is also found in turtles, animals considered phylogenetically related to the extinct theropsids from which mammals arose (4). Previous studies demonstrated substance P immunoreactivity in the turtle central nervous system (5,6); however, the effects of peripheral axotomy on substance P distribution have not been studied. Therefore, the aim of this study was to determine the effects of sciatic nerve transection on substance P immunoreactive fibers in the lumbar spinal cord of the turtle Trachemys dorbigni.Under ether-induced anesthesia (7), the right sciatic nerve was exposed and transected approximately 5 mm distal to the sciatic notch. In this nerve transection, a 2-mm segment of the nerve was removed to ensure that the transection was complete. Groups of three turtles of both sexes, weighing 300-400 g, were sacrificed 7, 15, 30, 60 and 90 days later. On the final day of the experiment, both operated and control turtles were anesthetized (25 mg/kg Thionembutal, intraperitoneally) and perfused through the heart with cold saline solution followed by 4% paraformaldehyde in 0.1 M sodium phosphate buffer, pH 7.4. The lumbar spinal cord was quickly dissected out, immersed in the same fixative for 2 h and then cryoprotected in 15 and 30% sucrose solutions in phosphate buffer at 4ºC. Coronal serial sections (50 µm) were obtained with a cryostat (Leitz) and collected in cold phosphate-buffered saline (PBS). The sections were then treated with 3% hydrogen peroxide in 10% methanol for 30 min, washed wit...

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Replacement of synaptic terminals in lamina II and Clarke's nucleus after unilateral lumbosacral dorsal rhizotomy in adult cats

Cited by 103 publications

References 47 publications

Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve

Intact sciatic myelinated primary afferent terminals collaterally sprout in the adult rat dorsal horn following section of a neighbouring peripheral nerve

Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity

Substance P immunoreactivity in the lumbar spinal cord of the turtle Trachemys dorbigni following peripheral nerve injury

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