Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin

Yongbo Li, Sung-Tsang Hsieh, Hsiung-Fei Chien, Xiaorong Zhang, Justin C. McArthur, John Wesley Griffin

Research output: Contribution to journalArticle

53 Citations (Scopus)

Abstract

Denervation in man often results in shiny, dry, thin skin. A previous study has shown that the epidermis of glabrous skin in the rat becomes approximately 40% thinner within 1 week following sciatic nerve transection, but which nerve fiber type or types influence epidermal thickness is unknown. In this study, we compared the effects on the epidermis of selective sensory, motor, and sympathetic denervation. Protein gene product 9.5 and calcitonin gene-related peptide immunocytochemical staining were used to determine the extent of denervation of epidermis, dermis, and sweat glands in the footpads. Epidermal thickness of the glabrous plantar skin of the foot was measured to verify the specificity and reliability of each animal model, the relevant regions of the peripheral nervous system were examined by light or electron microscopy or both. Epidermal thickness decreased significantly following sciatic nerve transection (58% of control, P <0.05) and dorsal root ganglionectomy (59%; P <0.05). The thickness also decreased following lumbar ventral rhizotomy (61%; P <0.01), destruction of lumbar spinal motor neurons (66%; P <0.05), and botulinum toxin-induced paralysis of the tibialis anterior and gastrocnemius muscles (70%; P <0.05). A slight decrease followed dorsal rhizotomy (84%; P <0.01). In contrast, no significant alterations in epidermal thickness were detected following sham operation and sympathectomy. Epidermal thinning was paralleled by reductions in the amounts of transcripts for glyceraldehyde-3-phosphate dehydrogenase and β-actin. These results suggest that selective loss of both sensory and motor fibers to the hind limb can contribute to reducing epidermal thickness in rat foot glabrous skin.
Original languageEnglish
Pages (from-to)452-462
Number of pages11
JournalExperimental Neurology
Volume147
Issue number2
DOIs
Publication statusPublished - 1997
Externally publishedYes

Fingerprint

Denervation
Foot
Epidermis
Rhizotomy
Skin
Sympathectomy
Sciatic Nerve
Ganglionectomy
Sweat Glands
Glyceraldehyde-3-Phosphate Dehydrogenases
Botulinum Toxins
Calcitonin Gene-Related Peptide
Spinal Nerve Roots
Peripheral Nervous System
Motor Neurons
Dermis
Nerve Fibers
Paralysis
Actins
Electron Microscopy

Keywords

  • animal tissue
  • article
  • denervation
  • epidermis cell
  • ganglionectomy
  • glabrous skin
  • muscle innervation
  • nonhuman
  • priority journal
  • rat
  • rhizotomy
  • sciatic nerve
  • skin nerve
  • sympathectomy
  • Actins
  • Animals
  • Botulinum Toxins
  • Denervation
  • Epidermis
  • Ganglia, Spinal
  • Ganglionectomy
  • Gene Expression Regulation
  • Glyceraldehyde-3-Phosphate Dehydrogenases
  • Hydrogen Peroxide
  • Hypertrophy
  • Hypesthesia
  • Keratinocytes
  • Laminectomy
  • Male
  • Motor Neurons
  • Muscle Denervation
  • Muscle, Skeletal
  • Neurons, Afferent
  • Paralysis
  • Peptide Fragments
  • Polymerase Chain Reaction
  • Rats
  • Rats, Sprague-Dawley
  • Rhizotomy
  • Sciatic Nerve
  • Spinal Cord Injuries
  • Sympathectomy

Cite this

Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin. / Li, Yongbo; Hsieh, Sung-Tsang; Chien, Hsiung-Fei; Zhang, Xiaorong; McArthur, Justin C.; Griffin, John Wesley.

In: Experimental Neurology, Vol. 147, No. 2, 1997, p. 452-462.

Research output: Contribution to journalArticle

Li, Yongbo ; Hsieh, Sung-Tsang ; Chien, Hsiung-Fei ; Zhang, Xiaorong ; McArthur, Justin C. ; Griffin, John Wesley. / Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin. In: Experimental Neurology. 1997 ; Vol. 147, No. 2. pp. 452-462.
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title = "Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin",
abstract = "Denervation in man often results in shiny, dry, thin skin. A previous study has shown that the epidermis of glabrous skin in the rat becomes approximately 40{\%} thinner within 1 week following sciatic nerve transection, but which nerve fiber type or types influence epidermal thickness is unknown. In this study, we compared the effects on the epidermis of selective sensory, motor, and sympathetic denervation. Protein gene product 9.5 and calcitonin gene-related peptide immunocytochemical staining were used to determine the extent of denervation of epidermis, dermis, and sweat glands in the footpads. Epidermal thickness of the glabrous plantar skin of the foot was measured to verify the specificity and reliability of each animal model, the relevant regions of the peripheral nervous system were examined by light or electron microscopy or both. Epidermal thickness decreased significantly following sciatic nerve transection (58{\%} of control, P <0.05) and dorsal root ganglionectomy (59{\%}; P <0.05). The thickness also decreased following lumbar ventral rhizotomy (61{\%}; P <0.01), destruction of lumbar spinal motor neurons (66{\%}; P <0.05), and botulinum toxin-induced paralysis of the tibialis anterior and gastrocnemius muscles (70{\%}; P <0.05). A slight decrease followed dorsal rhizotomy (84{\%}; P <0.01). In contrast, no significant alterations in epidermal thickness were detected following sham operation and sympathectomy. Epidermal thinning was paralleled by reductions in the amounts of transcripts for glyceraldehyde-3-phosphate dehydrogenase and β-actin. These results suggest that selective loss of both sensory and motor fibers to the hind limb can contribute to reducing epidermal thickness in rat foot glabrous skin.",
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author = "Yongbo Li and Sung-Tsang Hsieh and Hsiung-Fei Chien and Xiaorong Zhang and McArthur, {Justin C.} and Griffin, {John Wesley}",
note = "被引用次數:49 Export Date: 16 March 2016 CODEN: EXNEA 通訊地址: Li, Y.; Department of Neurology, Department of Epidemiology, Department of Neuroscience, Baltimore, MD 21287, United States 化學物質/CAS: Actins; Botulinum Toxins; glyceraldehyde 3-phosphate dehydrogenase (304-313), 130349-12-1; Glyceraldehyde-3-Phosphate Dehydrogenases, EC 1.2.1.-; Hydrogen Peroxide, 7722-84-1; Peptide Fragments 參考文獻: Abelli, L., Geppetti, P., Maggi, C.A., Relative contribution of sympathetic and sensory nerves to thermal nociception and tissue trophism in rats (1993) Neuroscience, 57, pp. 739-745; Baker, K.W., Habowsky, J.E., EDTA separation and ATPase Langerhans cell staining in the mouse epidermis (1983) J. Invest. Dermatol., 80, pp. 104-107; Baron, R., Janig, W., Kollmann, W., Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat (1988) J. Comp. Neurol., 275, pp. 460-468; Beuerman, R., Schimmelpfennig, B., Sensory denervation of the cornea affects epithelial proportion (1980) Exp. Neurol., 69, pp. 196-201; Brain J.E., Jr., Heisted, D.D., Faraci, F.M., Mechanisms of endotoxin-induced dilatation of cerebral arterioles (1995) Am. J. Physiol., 269, pp. 783-H788; Dalsgaard, C.-J., Rydh, M., Haegerstrand, A., Cutaneous innervation in man visualized with protein gene product 9.5 (PGP 9.5) antibodies (1989) Histochemistry, 92, pp. 385-389; Delforno, C., Holt, P.J.A., Marks, R., Corticosteroid effect on epidermal cell size (1978) Br. J. Dermatol., 98, pp. 619-623; Donnerer, J., Amann, R., Lembeck, F., Neurogenic and non-neurogenic inflammation in the rat paw following chemical sympathectomy (1991) Neuroscience, 45, pp. 761-765; Dykes, P.J., Marks, R., The effect of serum calcium levels on the rate of epidermal renewal in the rat (1984) Br. J. Dermatol., 111, pp. 191-196; English, K.B., The ultrastructure of cutaneous type I mechanoreceptors (Haarscheiben) in cats following denervation (1977) J. Comp. Neurol., 172, pp. 137-164; Farmer, S.R., Wan, K.M., Ben-Ze'ev, A., Penman, S., Regulation of actin mRNA levels and translation responds to changes in cell configuration (1983) Mol. Cell. Biol., 3, pp. 182-189; Fisher, L.B., Miabach, H.I., The effect of corticosteroids on human epidermal mitotic activity (1971) Arch. Dermatol., 103, pp. 39-44; Griffin, J.W., Drachman, D.B., Price, D.L., Fast axonal transport in motor nerve regeneration (1976) J. Neurobiol., 7, pp. 355-370; Guth, L., The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat (1957) Anat. Rec., 128, pp. 715-731; Haegerstrand, A., Jonzon, B., Dalsgaard, C.-J., Nilsson, J., Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 5993-5996; Head, H., Sherren, J., The consequences of injury to the peripheral nerves in man (1905) Brain, 28, pp. 116-338; Hsieh, S.-T., Choi, S., Lin, W.-M., McArthur, J.C., Griffin, J.W., Epidermal denervation and its effects on keratinocytes and Langerhans cells (1996) J. Neurocytol., 25, pp. 513-524; Kennedy, W.R., Wendelschafer-Crabb, G., Brelje, T.C., Innervation and vasculature of human sweat glands: An immunohistochemistry-laser scanning confocal fluorescence microscopy study (1994) J. Neurosci., 14, pp. 6825-6833; Lasek, R.J., Axoplasmic transport of labeled proteins in rat ventral motoneurons (1968) Exp. Neurol., 21, pp. 41-51; Latov, N., Antibodies to glycoconjugates in neuropathy and motor neuron disease (1994) Prog. Brain Res., 101, pp. 295-303; Lim, C.H., Innervation of the cornea of monkeys and the effects of denervation (1976) Br. J. Physiol. Opt., 31, pp. 38-42; McCarthy, B.G., Hsieh, S.-T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaluation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; McLean, I., Nakane, P., Periodate-lysine-paraformaldehyde fixative: A new fixative for immunoelectron microscopy (1974) J. Histochem. Cytochem., 22, pp. 1077-1083; Meyer-Siegler, K., Rahman-Mansur, N., Wurzer, J.C., Sirover, M.A., Proliferative dependent regulation of the glyceraldehyde-3-phosphate dehydrogenase/uracil DNA glycosylase gene in human cells (1992) Carcinogenesis, 13, pp. 2127-2132; Mitchell, W., (1872) Injuries of Nerves and Their Consequences, , Philadelphia: Lippincott; Nagahara, S., Matsuda, T., Cell-substrate and cell-cell interactions differently regulate cytoskeletal and extracellular matrix protein gene expression (1996) Journal of Biomedical Materials Research, 32, pp. 677-686; Nielsch, U., Keen, P., Effects of neonatal 6-hydroxydopamine administration on different substance P-containing sensory neurones (1987) Eur. J. Pharmacol., 138, pp. 193-197; Rahman-Mansur, N., Meyer-Siegler, K., Wurzer, J.C., Sirover, M.A., Cell cycle regulation of the glyceraldehyde-3-phosphate dehydrogenase/uracil DNA glycosylase gene in normal human cells (1993) Nucleic Acids Res., 21, pp. 993-998; Takahashi, K., Nakanishi, S., Imamura, S., Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: Stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors (1993) J. Invest. Dermatol., 101, pp. 646-651; Tanaka, T., Danno, K., Ikai, K., Imamura, S., Effects of substance P and substance K on the growth of cultured keratinocytes (1988) J. Invest. Dermatol., 90, pp. 399-401; Tervo, T., Sulonen, J., Valtones, S., Vannas, A., Vitranen, I., Distribution of fibronectin in human and rabbit corneas (1986) Exp. Eye Res., 42, pp. 399-406; Wesselingh, S.L., Power, C., Glass, J.D., Tyor, W.R., McArthur, J.C., Farber, J.M., Griffin, J.W., Griffin, D.E., Intracerebral cytokine mRNA expression in acquired immunodeficiency syndrome dementia (1993) Ann. Neurol., 33, pp. 576-582",
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doi = "10.1006/exnr.1997.6624",
language = "English",
volume = "147",
pages = "452--462",
journal = "Experimental Neurology",
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}

TY - JOUR

T1 - Sensory and motor denervation influence epidermal thickness in rat foot glabrous skin

AU - Li, Yongbo

AU - Hsieh, Sung-Tsang

AU - Chien, Hsiung-Fei

AU - Zhang, Xiaorong

AU - McArthur, Justin C.

AU - Griffin, John Wesley

N1 - 被引用次數:49 Export Date: 16 March 2016 CODEN: EXNEA 通訊地址: Li, Y.; Department of Neurology, Department of Epidemiology, Department of Neuroscience, Baltimore, MD 21287, United States 化學物質/CAS: Actins; Botulinum Toxins; glyceraldehyde 3-phosphate dehydrogenase (304-313), 130349-12-1; Glyceraldehyde-3-Phosphate Dehydrogenases, EC 1.2.1.-; Hydrogen Peroxide, 7722-84-1; Peptide Fragments 參考文獻: Abelli, L., Geppetti, P., Maggi, C.A., Relative contribution of sympathetic and sensory nerves to thermal nociception and tissue trophism in rats (1993) Neuroscience, 57, pp. 739-745; Baker, K.W., Habowsky, J.E., EDTA separation and ATPase Langerhans cell staining in the mouse epidermis (1983) J. Invest. Dermatol., 80, pp. 104-107; Baron, R., Janig, W., Kollmann, W., Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat (1988) J. Comp. Neurol., 275, pp. 460-468; Beuerman, R., Schimmelpfennig, B., Sensory denervation of the cornea affects epithelial proportion (1980) Exp. Neurol., 69, pp. 196-201; Brain J.E., Jr., Heisted, D.D., Faraci, F.M., Mechanisms of endotoxin-induced dilatation of cerebral arterioles (1995) Am. J. Physiol., 269, pp. 783-H788; Dalsgaard, C.-J., Rydh, M., Haegerstrand, A., Cutaneous innervation in man visualized with protein gene product 9.5 (PGP 9.5) antibodies (1989) Histochemistry, 92, pp. 385-389; Delforno, C., Holt, P.J.A., Marks, R., Corticosteroid effect on epidermal cell size (1978) Br. J. Dermatol., 98, pp. 619-623; Donnerer, J., Amann, R., Lembeck, F., Neurogenic and non-neurogenic inflammation in the rat paw following chemical sympathectomy (1991) Neuroscience, 45, pp. 761-765; Dykes, P.J., Marks, R., The effect of serum calcium levels on the rate of epidermal renewal in the rat (1984) Br. J. Dermatol., 111, pp. 191-196; English, K.B., The ultrastructure of cutaneous type I mechanoreceptors (Haarscheiben) in cats following denervation (1977) J. Comp. Neurol., 172, pp. 137-164; Farmer, S.R., Wan, K.M., Ben-Ze'ev, A., Penman, S., Regulation of actin mRNA levels and translation responds to changes in cell configuration (1983) Mol. Cell. Biol., 3, pp. 182-189; Fisher, L.B., Miabach, H.I., The effect of corticosteroids on human epidermal mitotic activity (1971) Arch. Dermatol., 103, pp. 39-44; Griffin, J.W., Drachman, D.B., Price, D.L., Fast axonal transport in motor nerve regeneration (1976) J. Neurobiol., 7, pp. 355-370; Guth, L., The effects of glossopharyngeal nerve transection on the circumvallate papilla of the rat (1957) Anat. Rec., 128, pp. 715-731; Haegerstrand, A., Jonzon, B., Dalsgaard, C.-J., Nilsson, J., Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 5993-5996; Head, H., Sherren, J., The consequences of injury to the peripheral nerves in man (1905) Brain, 28, pp. 116-338; Hsieh, S.-T., Choi, S., Lin, W.-M., McArthur, J.C., Griffin, J.W., Epidermal denervation and its effects on keratinocytes and Langerhans cells (1996) J. Neurocytol., 25, pp. 513-524; Kennedy, W.R., Wendelschafer-Crabb, G., Brelje, T.C., Innervation and vasculature of human sweat glands: An immunohistochemistry-laser scanning confocal fluorescence microscopy study (1994) J. Neurosci., 14, pp. 6825-6833; Lasek, R.J., Axoplasmic transport of labeled proteins in rat ventral motoneurons (1968) Exp. Neurol., 21, pp. 41-51; Latov, N., Antibodies to glycoconjugates in neuropathy and motor neuron disease (1994) Prog. Brain Res., 101, pp. 295-303; Lim, C.H., Innervation of the cornea of monkeys and the effects of denervation (1976) Br. J. Physiol. Opt., 31, pp. 38-42; McCarthy, B.G., Hsieh, S.-T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaluation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; McLean, I., Nakane, P., Periodate-lysine-paraformaldehyde fixative: A new fixative for immunoelectron microscopy (1974) J. Histochem. Cytochem., 22, pp. 1077-1083; Meyer-Siegler, K., Rahman-Mansur, N., Wurzer, J.C., Sirover, M.A., Proliferative dependent regulation of the glyceraldehyde-3-phosphate dehydrogenase/uracil DNA glycosylase gene in human cells (1992) Carcinogenesis, 13, pp. 2127-2132; Mitchell, W., (1872) Injuries of Nerves and Their Consequences, , Philadelphia: Lippincott; Nagahara, S., Matsuda, T., Cell-substrate and cell-cell interactions differently regulate cytoskeletal and extracellular matrix protein gene expression (1996) Journal of Biomedical Materials Research, 32, pp. 677-686; Nielsch, U., Keen, P., Effects of neonatal 6-hydroxydopamine administration on different substance P-containing sensory neurones (1987) Eur. J. Pharmacol., 138, pp. 193-197; Rahman-Mansur, N., Meyer-Siegler, K., Wurzer, J.C., Sirover, M.A., Cell cycle regulation of the glyceraldehyde-3-phosphate dehydrogenase/uracil DNA glycosylase gene in normal human cells (1993) Nucleic Acids Res., 21, pp. 993-998; Takahashi, K., Nakanishi, S., Imamura, S., Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: Stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors (1993) J. Invest. Dermatol., 101, pp. 646-651; Tanaka, T., Danno, K., Ikai, K., Imamura, S., Effects of substance P and substance K on the growth of cultured keratinocytes (1988) J. Invest. Dermatol., 90, pp. 399-401; Tervo, T., Sulonen, J., Valtones, S., Vannas, A., Vitranen, I., Distribution of fibronectin in human and rabbit corneas (1986) Exp. Eye Res., 42, pp. 399-406; Wesselingh, S.L., Power, C., Glass, J.D., Tyor, W.R., McArthur, J.C., Farber, J.M., Griffin, J.W., Griffin, D.E., Intracerebral cytokine mRNA expression in acquired immunodeficiency syndrome dementia (1993) Ann. Neurol., 33, pp. 576-582

PY - 1997

Y1 - 1997

N2 - Denervation in man often results in shiny, dry, thin skin. A previous study has shown that the epidermis of glabrous skin in the rat becomes approximately 40% thinner within 1 week following sciatic nerve transection, but which nerve fiber type or types influence epidermal thickness is unknown. In this study, we compared the effects on the epidermis of selective sensory, motor, and sympathetic denervation. Protein gene product 9.5 and calcitonin gene-related peptide immunocytochemical staining were used to determine the extent of denervation of epidermis, dermis, and sweat glands in the footpads. Epidermal thickness of the glabrous plantar skin of the foot was measured to verify the specificity and reliability of each animal model, the relevant regions of the peripheral nervous system were examined by light or electron microscopy or both. Epidermal thickness decreased significantly following sciatic nerve transection (58% of control, P <0.05) and dorsal root ganglionectomy (59%; P <0.05). The thickness also decreased following lumbar ventral rhizotomy (61%; P <0.01), destruction of lumbar spinal motor neurons (66%; P <0.05), and botulinum toxin-induced paralysis of the tibialis anterior and gastrocnemius muscles (70%; P <0.05). A slight decrease followed dorsal rhizotomy (84%; P <0.01). In contrast, no significant alterations in epidermal thickness were detected following sham operation and sympathectomy. Epidermal thinning was paralleled by reductions in the amounts of transcripts for glyceraldehyde-3-phosphate dehydrogenase and β-actin. These results suggest that selective loss of both sensory and motor fibers to the hind limb can contribute to reducing epidermal thickness in rat foot glabrous skin.

AB - Denervation in man often results in shiny, dry, thin skin. A previous study has shown that the epidermis of glabrous skin in the rat becomes approximately 40% thinner within 1 week following sciatic nerve transection, but which nerve fiber type or types influence epidermal thickness is unknown. In this study, we compared the effects on the epidermis of selective sensory, motor, and sympathetic denervation. Protein gene product 9.5 and calcitonin gene-related peptide immunocytochemical staining were used to determine the extent of denervation of epidermis, dermis, and sweat glands in the footpads. Epidermal thickness of the glabrous plantar skin of the foot was measured to verify the specificity and reliability of each animal model, the relevant regions of the peripheral nervous system were examined by light or electron microscopy or both. Epidermal thickness decreased significantly following sciatic nerve transection (58% of control, P <0.05) and dorsal root ganglionectomy (59%; P <0.05). The thickness also decreased following lumbar ventral rhizotomy (61%; P <0.01), destruction of lumbar spinal motor neurons (66%; P <0.05), and botulinum toxin-induced paralysis of the tibialis anterior and gastrocnemius muscles (70%; P <0.05). A slight decrease followed dorsal rhizotomy (84%; P <0.01). In contrast, no significant alterations in epidermal thickness were detected following sham operation and sympathectomy. Epidermal thinning was paralleled by reductions in the amounts of transcripts for glyceraldehyde-3-phosphate dehydrogenase and β-actin. These results suggest that selective loss of both sensory and motor fibers to the hind limb can contribute to reducing epidermal thickness in rat foot glabrous skin.

KW - animal tissue

KW - article

KW - denervation

KW - epidermis cell

KW - ganglionectomy

KW - glabrous skin

KW - muscle innervation

KW - nonhuman

KW - priority journal

KW - rat

KW - rhizotomy

KW - sciatic nerve

KW - skin nerve

KW - sympathectomy

KW - Actins

KW - Animals

KW - Botulinum Toxins

KW - Denervation

KW - Epidermis

KW - Ganglia, Spinal

KW - Ganglionectomy

KW - Gene Expression Regulation

KW - Glyceraldehyde-3-Phosphate Dehydrogenases

KW - Hydrogen Peroxide

KW - Hypertrophy

KW - Hypesthesia

KW - Keratinocytes

KW - Laminectomy

KW - Male

KW - Motor Neurons

KW - Muscle Denervation

KW - Muscle, Skeletal

KW - Neurons, Afferent

KW - Paralysis

KW - Peptide Fragments

KW - Polymerase Chain Reaction

KW - Rats

KW - Rats, Sprague-Dawley

KW - Rhizotomy

KW - Sciatic Nerve

KW - Spinal Cord Injuries

KW - Sympathectomy

U2 - 10.1006/exnr.1997.6624

DO - 10.1006/exnr.1997.6624

M3 - Article

VL - 147

SP - 452

EP - 462

JO - Experimental Neurology

JF - Experimental Neurology

SN - 0014-4886

IS - 2

ER -