Organization of hindlimb nerve projections to the rat spinal cord: A choleragenoid horseradish peroxidase study

Journal of Comparative Neurology

Volumn 364, Issue 4, 1996, Pages 651-663

  Rivero Melian C ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

cholera toxin; motor neurons; nerve fibers; neural pathways; peripheral nerves

Indexed keywords

CHOLERA TOXIN; HORSERADISH PEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; FEMORAL NERVE; HAMSTRING; LEG MUSCLE; MOTONEURON; NONHUMAN; OBTURATOR NERVE; PERIPHERAL NERVE; PERONEUS NERVE; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SENSORY NERVE; SPINAL CORD VENTRAL HORN; TIBIAL NERVE;

ANIMALS; FEMALE; FEMORAL NERVE; HINDLIMB; HISTOCYTOCHEMISTRY; HORSERADISH PEROXIDASE; NEURAL PATHWAYS; OBTURATOR NERVE; PERONEAL NERVE; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TIBIAL NERVE;

EID: 0030052329     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960122)364:4<651::AID-CNE4>3.0.CO;2-2     Document Type: Article

References (96)

1. Abrahams, V.C., F.J. Richmond, and J. Keane (1984) Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: A study using transganglionic transport of horseradish peroxidase. J. Comp. Neurol. 230:142-154.
2. Abrahams, V.C., and J.E. Swett (1986) The pattern of spinal and medullary projections from a cutaneous nerve and a muscle nerve of the forelimb of the cat: A study using the transganglionic transport of HRP. J. Comp. Neurol. 246:70-84.
3. Albright, B.C., and D.E. Haines (1973) The morphology of Clarke's column in the lesser bushbaby (Galago senegalensis). Brain Behav. Evol. 8:165-190.
4. Bakker, D.A., F.J. Richmond, and V.C. Abrahams (1984) Central projections from cat suboccipital muscles: A study using transganglionic transport of horseradish peroxidase. J. Comp. Neurol. 228:409-421.
5. Bodian, D. (1975) Origin of specific synaptic types in the motoneuron neuropil of the monkey. J. Comp. Neurol. 259:225-244.
6. Brown, A.G. (1981) Organization of the Spinal Cord. Berlin, Heidelberg: Springer-Verlag.
7. Brown, A.G., and R.E.W. Fyffe (1981) Direct observations on the contacts made between la afferent fibers and α-motoneurones in the cat's lumbosacral spinal cord. J. Physiol. 313:121-140.
8. Browne, K.M. (1950) The spatial distribution of segmental nerves to striate musculature of the hindlimb of the rat. J. Comp. Neurol. 93:441-455.
9. Brushart, T.M., and M.-M. Mesulam (1980) Transganglionic demonstration of central sensory projections from skin and muscle with HRP-lectin conjugates. Neurosci. Lett. 17:1-6.
10. Cajal, S.R. (1909) Histologie de Système Nerveus de l'Homme et des Vertébrés. Paris: Maloine.
11. Conradi, S. (1969) Ultrastructure of dorsal root boutons on lumbosacral motoneurons of the adult cat, as revealed by dorsal root section. Acts Physiol. Scand. Suppl. 332:85-115.
12. Conradi, S., and S. Skoglund (1969) Observations on the ultrastructure of the initial motor axon segment and dorsal root boutons on the motoneurons in the lumbosacral spinal cord of the cat during postnatal development. Acta Physiol. Scand. Suppl. 333:53-76.
13. Corbin, K.B., and J.C. Hinsey (1935) Intramedullary course of the dorsal root fibers of each of the first four cervical nerves. J. Comp. Neurol. 63:119-126.
14. Craig, A.D., and S. Mense (1983) The distribution of afferent fibers from the gastrocnemius-soleus muscle in the dorsal horn of the cat, as revealed by the transport of horseradish peroxidase. Neurosci. Lett. 41:233-238.
15. Crockett, D.P., S.L. Harris, and M.D. Egger (1987) Plantar motoneuron columns in the rat. J. Comp. Neurol. 265:109-118.
16. Culberson, J.L., D.E. Haines, D.L. Kimmel, and P.E. Brown (1979) Contralateral projection of primary afferent fibers to mammalian spinal cord. Exp. Neurol. 64:83-97.
17. Culberson, J.L., and D.L. Kimmel (1975) Primary afferent fiber distribution at brachial and lumbosacral spinal cord levels in the opossum (Didelphis marsupialis virginiana). Brain Behav. Evol. 12:229-246.
18. Cullheim, S., and J.O. Kellerth (1976) Combined light and electron microscopic tracing of neurons including axons and synaptic terminals after intracellular injection of horseradish peroxidase. Neurosci. Lett. 2:307-313.
19. Cullheim, S., J.O. Kellerth, and S. Conradi (1977) Evidence for direct synaptic interconnections between cat spinal α-motoneurons via the recurrent axon collaterals: A morphological study using intracellular injection of horseradish peroxidase. Brain Res. 132:1-10.
20. DeGroat, W.C., I. Nadelhaft, C. Morgan, and T. Schauble (1978) Horseradish peroxidase tracing of visceral efferent and primary afferent pathways in the cat's sacral spinal cord using benzidine processing. Neurosci. Lett. 10:103-108.
21. Eccles, J.C., R.M. Eccles, and A. Lundberg (1957) The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones. J. Physiol. 137:22-50.
22. Fu, T.C., M. Santini, and E.D. Schomburg (1974) Characteristics and distribution of spinal focal synaptic potentials generated by group II muscle afferents. Acta Physiol. Scand. 91:298-313.
23. Fu, T.C., and E.D. Schomburg (1974) Electrophysiological investigation of the projection of secondary muscle spindle afferents in the cat spinal cord. Acta Physiol. Scand. 91:314-29.
24. Fyffe, R.E.W. (1979) The morphology of Group II muscle afferent fibre collaterals. J. Physiol. 296:39-40.
25. Ganser, A.L., D.A. Kirschner, and M. Willinger (1983) Ganglioside localization on myelinated nerve fibres by cholera toxin binding. J. Neurocytol. 12:921-938.
26. Goering, J.H. (1928) An experimental analysis of the motor-cell columns in the cervical enlargement of the spinal cord in the albino rat. J. Comp. Neurol. 46:125-151.
27. Gonatas, N.K., C. Harper, T. Mizutani, and J.O. Gonatas (1979) Superior sensitivity of conjugates of horseradish peroxidase with wheat germ agglutinin for studies of retrograde axonal transport. J. Histochem. Cytochem. 27:728-734.
28. Grant, G., J. Arvidsson, B. Robertson, and J. Ygge (1979) Transganglionic transport of horseradish peroxidase in primary sensory neurons. Neurosci. Lett. 12:23-28.
29. Greene, E.C. (1963) Anatomy of the Rat. New York and London: Hafner Publishing Company.
30. Hand, P.J. (1966) Lumbosacral dorsal root terminations in the nucleus gracilis of the cat: Some observations on terminal degeneration in other medullary sensory nuclei. J. Comp. Neurol. 126:137-156.
31. Hirakawa, M., J.T. McCabe, and M. Kawata (1992) Time-related changes in the labeling pattern of motor and sensory neurons innervating the gastrocnemius muscle as revealed by the retrograde transport of the cholera toxin B subunit. Cell Tiss. Res. 267:419-427.
32. Hongo, T., N. Kudo, S. Sasaki, M. Yamashita, K. Yoshida, N. Ishizuka, and M. Mannen (1987) Trajectory of group Ia and Ib fibers from the hind-limb muscles at the L3 and L4 segments of the spinal cord of the cat. J. Comp. Neurol. 262:159-194.
33. Hongo, T., N. Kudo, M. Yamashita, K. Yoshida, N. Ishizuka, and H. Mannen (1981) Transneuronal passage of intra-axonally injected horseradish peroxidase (HRP) from group Ib and II fibers into the secondary neurons in the dorsal horn of the cat spinal cord. Biomed. Res. Tokyo 2:722-727.
34. Hubbard, J.I., and O. Oscarsson (1962) Localization of the cell bodies of the ventral spinocerebellar tract in lumbar segments of the cat. J. Comp. Neurol. 118:199-204.
35. Hultborn, H. (1972) Convergence on interneurones in the reciprocal Ia inhibitory pathway to motoneurones. Acta Physiol. Scand. 375:1-42.
36. Hultborn, H., E. Jankowska, and S. Lindström (1971) Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents. J. Physiol. 215:613-636.
37. Iansek, R., and S.J. Redman (1973) The amplitude time course and charge of unitary excitatory post-synaptic potentials evoked in spinal motoneurone dendrites. J. Physiol. 234:665-688.
38. Ishizuka, N., H. Mannen, T. Hongo, and S. Sasaki (1979) Trajectory of group Ia afferent fibers stained with horseradish peroxidase in the lumbosacral spinal cord of the cat: Three dimensional reconstructions from serial sections. J. Comp. Neurol. 186:189-211.
39. Jack, J.J.B., S. Miller, R. Porter, and S.J. Redman (1971) The time course of minimal excitatory post-synaptic potentials evoked in spinal motoneurones by group Ia afferent fibres. J. Physiol. 215:353-380.
40. Jankowska, E. (1992) Interneuronal relay in spinal pathways from proprioceptors. Prog. Neurobiol. 38:335-378.
41. Jankowska, E., and S. Lindström (1972) Morphology of interneurones mediating Ia reciprocal inhibition of motoneurones in the spinal cord of the cat. J. Physiol. 226:805-823.
42. Johnson, J.I., W.I. Walker, and B.H. Pubols (1968) Somatotopic organization of raccoon dorsal column nuclei. J. Comp. Neurol. 132:1-44.
43. Kaizawa, J., and I. Takahashi (1970) Motor cell columns in rat lumbar spinal cord. Tohoku J. Exp. Med. 101:25-34.
44. Kirkwood, P.A., and T.A. Sears (1974) Monosynaptic excitation of motoneurones from secondary endings of muscle spindles. Nature 252:243-244.
45. Kuno, M., E.J. Muńoz-Martinez, and M. Randić (1973) Sensory inputs to neurones in Clarke's column from muscle, cutaneous and joint receptors. J. Physiol. 228:327-342.
46. LaMotte, C.C., S.E. Kapadia. and C.M. Shapiro (1991) Central projections of the sciatic, saphenous, median, and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin-HRP (WGA-HRP). J. Comp. Neurol. 311:546-562.
47. Laporte, Y., and D.P.C. Lloyd (1952) Nature and significance of the reflex connections established by large afferent fibers of muscular origin. Am. J. Physiol. 169:609-621.
48. Liddell, E.G.T., and C.S. Sherrington (1924) Reflexes in response to stretch. Proc. R. Soc. 95b:212-242.
49. Light, A.R., and E.R. Perl (1979a) Reexamination of the dorsal root projection to the spinal dorsal horn including observation on the differential termination of coarse and fine fibers. J. Comp. Neurol. 186:117-132.
50. Light, A.R., and E.R. Perl (1979b) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J. Comp. Neurol. 186:133-150.
51. Lloyd, D.P.C. (1943) Neuron patterns controlling transmission of ipsilateral hind limb reflexes in cat. J. Neurophysiol. 6:293-315.
52. Lundberg, A., K. Malmgren, and E.D. Schomburg (1975) Characteristics of the excitatory pathway from group II muscle afferents to alpha motoneurones. Brain Res. 88:538-542.
53. Maslany, S., D.P. Crockett, and M.D. Egger (1992) Organization of cutaneous primary afferent fibers projecting to the dorsal horn in the rat: WGA-HRP versus B-HRP. Brain Res. 569:123-135.
54. Matsushita, M., and Y. Hosoya (1979) Cells of origin of the spinoeerebellar tract in the rat, studied with the method of retrograde transport of horseradish peroxidase. Brain Res. 173:185-200.
55. McLaughlin, B.J. (1972) Dorsal root projections to the motor nuclei in the cat spinal cord. J. Comp. Neurol. 144:461-474.
56. Mense, S., and A.D. Craig (1988) Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat. Neuroscience 26:1023-1035.
57. Mense, S., and N.R. Prabhakar (1986) Spinal termination of nociceptive afferent fibers from deep tissues in the cat. Neurosci. Lett. 66:169-174.
58. Mesulam, M.-M. (1978) Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: A noncarcinogenic blue reaction product with superior sensitivity for visualizing neuronal afferents and efferents. J. Histochem. Cytochem. 26:106-117.
59. Mesulam, M.-M., and T.M. Brushart (1979) Transganglionic and anterograde transport of horseradish peroxidase across dorsal root ganglia: A tetramethylbenzidine method for tracing central sensory connections of muscles and peripheral nerves. Neuroscience 4:1107-1117.
60. Mesulam, M.-M., E. Hegarty, H. Barbas, K. Carson, E. Gower, A. Knapp, M. Moss, and E. Mufson (1980) Additional factors influencing sensitivity in the tetramethylbenzidine method for horseradish peroxidase neurohistochemistry. J. Histochem. Cytochem. 28:1255-1259.
61. Molander, C., and G. Grant (1985) Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA-HRP conjugate. J. Comp. Neurol. 237:476-484.
62. Molander. C., and G. Grant (1986) Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn: A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience 19:297-312.
63. Molander, C., and G. Grant (1987) Spinal cord projections from hindlimb muscle nerves in the rat studied by transganglionic transport of horseradish peroxidase wheat germ agglutinin conjugated horseradish peroxidase or horseradish peroxidase with dimethylsulfoxide. J. Comp. Neurol. 260:246-255.
64. Nicolopoulos-Stournaras, S., and J.F. lies (1983) Motor neuron columns in the lumbar spinal cord of the rat. J. Comp. Neurol. 217:75-85.
65. Oldfors, A. (1986) Cholera toxin B-subunit incorporation into synaptic vesicles of the neuromuscular junction of the rat. Experientia 42:415-417.
66. Petras, J.M. (1977) Spinocerebellar neurons in the rhesus monkey. Brain Res. 130:146-151.
67. Peyronnard, J.M., and L. Charron (1983) Decreased horseradish peroxidase labeling in deafferented motoneurons of the rat. Brain Res. 275:203-214.
68. Rasdolsky, J. (1928) Über die endigung der Hinterwurzelfasern im Rückenmark. Arch. Psychiat. Nervenkr. 85:795-809.
69. Reed, A.F. (1940) The nuclear masses in the cervical spinal cord of Macaca mulatta. J. Comp. Neurol. 72:187-206.
70. Réthelyi, M., D.L. Trevino, and E.R. Perl. (1979) Distribution of primary afferent fibers within the sacrococcygeal dorsal horn: An autoradiographic study. J. Comp. Neurol. 185:603-622.
71. Rivero-Melián, C., and J. Arvidsson (1992) Brain stem projections of rat lumbar dorsal root ganglia studied with choleragenoid conjugated horseradish peroxidase. Exp. Brain. Res. 91:12-20.
72. Rivero-Melián, C., and G. Grant (1988) Somatotopic organization of hindlimb muscle afferent projections to the column of Clarke of the rat studied with choleragenoid horseradish peroxidase conjugate. Neurosci. Abstr. 14:1:693.
73. Rivero-Melián, C., and G. Grant (1990a) Distribution of lumbar dorsal root fibers in the lower thoracic and lumbosacral spinal cord of the rat studied with choleragenoid horseradish peroxidase conjugate. J. Comp. Neurol. 299:470-481.
74. Rivero-Melián, C., and G. Grant (1990b) Lumbar dorsal root projections to spinocerebellar cell groups in the rat spinal cord: A double labeling study. Exp. Brain Res. 81:85-94.
75. Rivero-Melián. C., and G. Grant (1991) Choleragenoid horseradish peroxidase used for studying projections of some hindlimb cutaneous nerves and plantar foot afferents to the dorsal horn and Clarke's column in the rat. Exp. Brain Res. 84:125-132.
76. Robertson, B., and G. Grant (1985) A comparison between wheat germ agglutinin and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurons in the rat with some observations in the cat. Neuroscience 14:895-905.
77. Romanes, G.J. (1951) The motor cell columns of the lumbosacral spinal cord of the cat. J. Comp. Neurol. 94:313-363.
78. Rustioni, A., and G. Macchi (1968) Distribution of dorsal root fibers in the medulla oblongata of the cat. J. Comp. Neurol. 134:113-126.
79. Scheibel, M.E., and A.B. Scheibel (1966) Spinal motoneurons, interneurons and Renshaw cells: A Golgi study. Arch. Ital. Biol. 104:328-353.
80. Scheibel, M.E., and A.B. Scheibel (1969) Terminal patterns in cat spinal cord. III. Primary afferent collaterals. Brain Res. 13:417-443.
81. Scheibel, M.E., and A.B. Scheibel (1971) Inhibition and the Renshaw cell: A structural critique. Brain Behav. Evol. 4:53-93.
82. Schultze, F. (1882) Befund bei spinaler Kinderlähmung nach dreijährigem Bestehen derselben. Neurol. Centralbl. 1:433-437.
83. Sherrington, C.S. (1890) On outlying nerve cells in the mammalian spinal cord. Phil. Trans. R. Soc. Lond. 181:33-48.
84. Smith, C.L. (1983) The development and postnatal organization of primary afferent projections to the rat thoracic spinal cord. J. Comp. Neurol. 220:29-43.
85. Sprague, J.M. (1958) The distribution of dorsal root fibers on motor cells in the lumbosacral spinal cord of the cat, and the site of excitatory and inhibitory terminals in monosynaptic pathways. Proc. R. Soc. Lond. Ser. B. 140:534-556.
86. Sprague, J.M., and H. Ha (1964) The terminal fields of dorsal root fibers in the lumbosacral spinal cord of the cat, and the dendritic organization of the motor nuclei. In JC Eccles and JP Schade (eds): Organization of the Spinal Cord. Amsterdam: Elsevier. Prog. in Brain Res. 11:120-152.
87. Sterling, P., and H.G. Kuypers (1967) Anatomical organization of the brachial spinal cord of the cat. I. The distribution of dorsal root fibers. Brain Res. 4:1-15.
88. Swett, J.E., R.P. Wikholm, R.H.I. Blanks, A.L. Swett, and L.C. Conley (1986) Motoneurons of the rat sciatic nerve. Exp. Neurol. 93:227-252.
89. Swett, J.E., and C.J. Woolf (1985) The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord. J. Comp. Neurol. 231:66-77.
90. Trojanowski, J.Q., J.O. Gonatas, and N.K. Gonatas (1981) Conjugates of horseradish peroxidase (HRP) with cholera toxin and wheat germ agglutinin are superior to free HRP as orthogradely transported markers. Brain Res. 223:381-385.
91. Trojanowski, J.Q., J.O. Gonatas, and N.K. Gonatas (1982) Horseradish peroxidase (HRP) conjugates of cholera toxin and lectins are more sensitive retrogradely transported markers than free HRP. Brain Res. 231:33-50.
92. Ueyama, T., H. Arakawa, and N. Mizuno (1985) Contralateral termination of pudendal nerve fibers in the gracile nucleus of the rat. Neurosci. Lett. 62:113-117.
93. Ulfhake, B., and J.O. Kellerth (1981) A quantitative light microscopic study of the dendrites of cat spinal α-motoneurons after intracellular staining with horseradish peroxidase. J. Comp. Neurol. 202:571-583.
94. Wan, X.-C.S., J.Q. Trojanowski, and J.O. Gonatas (1982) Cholera toxin and wheat germ agglutinin conjugates as neuroanatomical probes: Their uptake and clearance, transganglionic and retrograde transport and sensitivity. Brain Res. 243:215-224.
95. Woolf, C.J., and M. Fitzgerald (1986) Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord. J. Comp. Neurol. 251:517-531.
96. Ygge, J., and G. Grant (1983) The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of Horseradish peroxidase. J. Comp. Neurol. 216:1-9.