Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula)

Journal of Comparative Neurology

Volumn 420, Issue 2, 2000, Pages 139-170

  Anadón, Ramón ^a   Molist, Pilar ^b   Rodríguez Moldes, Isabel ^a   López, Jesús María ^c   Quintela, Inés ^a   Cerviño, María Carmen ^a   Barja, Primitivo ^a   González, Agustín ^c  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b UNIVERSITY OF VIGO   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Acetylcholine; Brain; Dogfish; Elasmobranchs; Immunoblotting; Immunohistochemistry

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; DOGFISH; ENZYME LOCALIZATION; EVOLUTION; IMMUNOBLOTTING; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; VERTEBRATE;

ACETYLCHOLINE; ANIMALS; BLOTTING, WESTERN; BRAIN; CEREBELLAR NUCLEI; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; DIENCEPHALON; DOGFISH; GANGLIA, SENSORY; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; MESENCEPHALON; NEURONS; PREOPTIC AREA; RHOMBENCEPHALON; SPINAL CORD; TELENCEPHALON;

EID: 0034192850     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000501)420:2<139::AID-CNE1>3.0.CO;2-T     Document Type: Article

References (180)

1. Alvarez-Otero R, Anadón R. 1992. Golgi cells of the cerebellum of the dogfish, Scyliorhinus canicula (Elasmobranchs): a Golgi and ultrastructural study. J Hirnforsch 33:321-327.
2. Alvarez-Otero R, Pérez S, Rodríguez MA, Adrio F, Anadón R. 1995. GABAergic neuronal circuits in the cerebellum of the dogfish Scyliorhinus canicula (Elasmobranchs): an immunocytochemical study. Neurosci Lett 187:87-90.
3. Alvarez-Otero R, Pérez S, Rodríguez MA, Anadón R. 1996. Organization of the cerebellar nucleus of the dogfish, Scyliorhinus canicula L.: a light microscopic, immunocytochemical, and ultrastructural study. J Comp Neurol 368:487-502.
4. Anadón R. 1978. Núcleos y conexiones primarias de los nervios branquiales de Torpedo marmorata (Risso) y otros selacios. Trab Inst Cajal 69:55-66.
5. Anadón R, Rodicio MC, Corujo A. 1980. Ultraestructura del núcleo del nervio oculomotor común de la pintarroja (Scylliorhinus canicula L.). Trab Inst Cajal 71:255-270.
6. Anadón R, Molist P, Pombal MA, Rodríguez-Moldes I, Rodicio MC. 1995a. Marginal cells in the spinal cord of four elasmobranchs (Torpedo marmorata, T. torpedo, Raja undulata and Scyliorhinus canicula): evidence for homology with lamprey intraspinal stretch receptor neurons. Eur J Neurosci 7:934-943.
7. Anadón R, Pérez SE, Adrio F, Rodriguez MA, Rodríguez-Moldes I. 1995b. The electric lobes of the electric ray (Torpedo marmorata) are innervated by GABAergic fibres: immunocytochemical evidence for dual innervation of electromotoneurons. Neurosci Lett 201:171-174.
8. Armstrong DM, Saper CB, Levey AI, Wainer BH, Terry RD. 1983. Distribution of cholinergic neurons in rat brain: demonstrated by the immunocytochemical localization of choline acetyltransferase. J Comp Neurol 216:53-68.
9. Aston-Jones G, Shipley MT, Grzanna R. 1995. The locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G, editor. The rat nervous system, 2nd ed. San Diego: Academic Press, p 183-213.
10. Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329-346.
11. Barmack NH, Baughman RW, Eckenstein FP. 1992. Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunocytochemistry. J Comp Neurol 317:233-249.
12. Barrett DL, Taylor EW. 1985. The location of cardiac vagal preganglionic neurones in the brain stem of the dogfish Scyliorhinus canicula. J Exp Biol 117:449-458.
13. Batten TF, Lo VK, Maqbool A, McWilliam PN. 1989. Distribution of calcitonin gene-related peptide-like immunoreactivity in the medulla oblongata of the cat, in relation to choline acetyltransferase-immunoreactive neurons and substance P-immunoreactive fibres. J Chem Neuroanat 2:163-176.
14. Blaker SN, Armstrong DM, Gage FH. 1988. Cholinergic neurons within the rat hippocampus: response to fimbria-fornix transection. J Comp Neurol 275:87-105.
15. Bodznick D, Northcutt RG. 1980. Segregation of electro-and mechanoreceptive inputs to the elasmobranch medulla. Brain Res 195:313-321.
16. Boord RL, Montgomery JC. 1989. Central mechanosensory lateral line centers and pathways among the elasmobranchs. In: Coombs S, Görner P, Münz H, editors. The mechanosensory lateral line: neurobiology and evolution. New York: Springer, p 323-339.
17. Borges LF, Iversen SD. 1986. Topography of choline acetyltransferase immunoreactive neurons and fibers in the rat spinal cord. Brain Res 362:140-148.
18. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
19. Brantley RK, Bass AH. 1988. Cholinergic neurons in the brain of a teleost fish (Porichthys notatus) located with a monoclonal antibody to choline acetyltransferase. J Comp Neurol 275:87-105
20. Brauth SE, Kitt CA, Price DL, Wainer BH. 1985. Cholinergic neurons in the telencephalon of the reptile Caiman crocodilus. Neurosci Lett 58: 235-240.
21. Bruce G, Wainer BH, Hersh LB. 1985. Immunoaffinity purification of human choline acetyltransferase: comparison of the brain and placental enzymes. J Neurochem 445:611-620.
22. Butcher LL, Woolf NJ. 1984. Histochemical distribution of acetylcholinesterase in the central nervous system: clues to the localization of cholinergic neurons. In: Björklund A, Hökfelt T, Kuhar MJ, editors. Handbook of chemical neuroanatomy, vol 3: classical transmitters and transmitter receptors in the CNS, part II. Amsterdam: Elsevier, p 1-50.
23. Carpenter MB, Chang L, Pereira AB, Hersh LB. 1987. Comparisons of the immunocytochemical localization of choline acetyltransferase in the vestibular nuclei of the monkey and cat. Brain Res 418:403-408.
24. Carpenter MB, Huang Y, Pereira AB, Hersh LB. 1990. Immunocytochemical features of the vestibular nuclei in the monkey and cat. J Hirnforsch 31:585-599.
25. Catois E. 1901. Recherches sur l'Histologie et l'Anatomie Microscopique de l'Encèphale chez les Poissons. Lille: L. Danel.
26. Contestabile A, Villani L, Fasolo A, Franzoni MF, Gribaudo L, Oktedalen O, Fonnum F. 1987. Topography of Cholinergic and substance P pathways in the habenulo-interpeduncular system of the rat. An immunocytochemical and microchemical approach. Neuroscience 21:253-270.
27. Cruce WLR, Stuesse SL, Northcutt RG. 1999. Brainstem neurons with descending projections to the spinal cord of two elasmobranch fishes: thornback guitarfish, Platyrhinoidis triseriata, and horn shark, Heterodontus francisci. J Comp Neurol 403:534-560.
28. Davidoff MS, Schulze W. 1988. Coexistence of GABA-and choline acetyltransferase (ChAT)-like immunoreactivity in the hypoglossal nucleus of the rat. Histochemistry 89:25-33.
29. Desan PH, Gruberg ER, Grewell KM, Eckenstein F. 1987. Cholinergic innervation of the optic tectum in the frog Rana pipiens. Brain Res 413:344-349.
30. Díaz C, Puelles L. 1992. In vitro HRP-labeling of the fasciculus retroflexus in the lizard Gallotia galloti. Brain Behav Evol 39:305-311.
31. Díaz-Regueira SM, Alvarez-Otero R, Anadón R. 1990. Organization of the lateral line lobes of the dogfish, Scyliorhinus canicula L. Eur J Neurosci 3(Suppl): 151.
32. Eckenstein F, Sofroniew MV. 1983. Identification of central cholinergic neurons containing both choline acetyltransferase and acetylcholinesterase and of central neurons containing only acetylcholinesterase. J Neurosci 3:2286-2291.
33. Eckenstein F. Thoenen H. 1982. Production of specific antisera and monoclonal antibodies to choline acetyltransferase: characterization and use for identification of cholinergic neurons. EMBO J 1:363-368.
34. Eckenstein F, Thoenen H. 1983. Cholinergic neurons in the rat cerebral cortex demonstrated by immunohistochemical localization of choline acetyltransferase. Neurosci Lett 36:211-215.
35. Ekström P. 1987. Distribution of choline acetyltransferase-immunoreactive neurons in the brain of a cyprinid teleost (Phoxinus phoxinus L.). J Comp Neurol 256:494-515.
36. Epstein ML, Davis JP, Gellman LE, Lamb JR, Dahl JL. 1988. Cholinergic neurons of the chicken ciliary ganglion contain somatostatin. Neuroscience 25:1053-1060.
37. Fiebig E. 1988. Connections of the corpus cerebelli in the thornback guitarfish Platyrhinoidis triseriata (Elasmobranchii): a study with WGA-HRP and extracellular granule recording. J Comp Neurol 268:567-583.
38. Gilland E, Baker R. 1992. Longitudinal and tangential migration of cranial nerve efferent neurons in the developing hindbrain of Squalus acanthias. Biol Bull 183:356-358.
39. Gilland E, Baker R. 1993. Conservation of neuroepithelial and mesodermal segments in the embryonic vertebrate head. Acta Anat 148:110-123.
40. Gómez-Segade P, Segade LAG, Anadón R. 1991. Ultrastructure of the organum vasculosum laminae terminalis in the advanced teleost Chelon labrosus (Risso, 1826). J Hirnforsch 32:69-77.
41. Gould E, Butcher LL. 1986. Cholinergic neurons in the rat substantia nigra. Neurosci Lett 63:315-319.
42. Gould E, Butcher LL. 1987. Transient expression of choline acetyltransferase-like immunoreactivity in Purkinje cells of the developing rat cerebellum. Brain Res 431:303-306.
43. Gould E, Woolf NJ, Butcher LI. 1991. Postnatal development of cholinergic neurons in the rat: I. Forebrain. Brain Res Bull 27:767-789.
44. Grillner S, Williams T, Lagerback PA. 1984. The edge cell, a possible intraspinal mechanoreceptor. Science 223:500-503.
45. Grosman DD, Lorenzi MV, Trinidad AC, Strauss WL. 1995. The human choline acetyltransferase gene encodes two proteins. J Neurochem 65:484-491.
46. Grover BG, Sharma SC. 1981. Organization of extrinsic tectal connections in goldfish, Carassius auratus. J Comp Neurol 196:471-488.
47. Hamill GS, Jacobowitz DM. 1984. A study of afferent projections to the rat interpeduncular nucleus. Brain Res Bull 13:527-539.
48. Hedreen JC, Bacon SJ, Cork LC, Kitt CA, Crawford GD, Salvaterra PM, Price DL. 1983. Immunocytochemical identification of cholinergic neurons in the monkey central nervous system using monoclonal antibodies against choline acetyltransferase. Neurosci Lett 43:173-177.
49. Helselmans JM, Wouterlood FG. 1994. Light and electron microscopic characterization of cholinergic and dopaminergic structures in the striatal complex and the dorsal ventricular ridge of the lizard Gekko gecko. J Comp Neurol 345:69-83.
50. Herreros J, Blasi J, Arribas M, Marsal J. 1995. Tetanus toxin mechanism of action in Torpedo electromotor system: a study on different steps in the intoxication process. Neuroscience 65:305-311.
51. Hersh LB, Wainer BM, Andrews L. 1984. Multiple isoelectric and molecular weight variants of choline acetyltransferase: artifact or real? J Biol Chem 259:1253-1258.
52. Hietanen M, Pelto-Huikko M, Rechardt L. 1990. Immunocytochemical study of the relations of acetylcholinesterase, enkephalin-, substance P-, choline acetyltransferase-and calcitonin gene-related peptide-immunoreactive structures in the ventral horn of rat spinal cord. Histochemistry 93:473-477.
53. Holmes CJ, Mainville LS, Jones BE. 1994. Distribution of cholinergic, GABAergic and serotonergic neurons in the medial medullary reticular formation and their projections studied by cytotoxic lesions in the cat. Neuroscience 62:1155-1178.
54. Holmqvist BI, Ekström P. 1995. Hypophysiotrophic systems in the brain of the Atlantic salmon. Neuronal innervation of the pituitary and the origin of pituitary dopamine and nonapeptides identified by means of combined carbocyanine tract tracing and immunocytochemistry. J Chem Neuroanat 8:125-145.
55. Hoogland PV, Vermeulen-VanderZee E. 1990. Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko. Brain Behav Evol 36:378-390.
56. Hoover DB, Muth EA, Jacobowitz DA. 1978. A mapping of the distribution of acetylcholine, choline acetyltransferase and acetylcholinesterase in discrete areas of rat brain. Brain Res 153:295-306.
57. Houser CR, Crawford GD, Barber RP. Salvaterra PM, Vaughn JE. 1983. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 266:97-119.
58. Ichikawa T, Hirata Y. 1990. Organization of choline acetyltransferase-containing structures in the cranial nerve motor nuclei and lamina IX of the cervical spinal cord of the rat. J Hirnforsch 31:251-257.
59. Ichikawa T, Ajiki K, Matsuura J, Misawa H. 1997. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J Chem Neuroanat 13:23-39.
60. Ikeda M, Houtani T, Ueyama T, Sugimoto T. 1991. Choline acetyltransferase immunoreactivity in the cat cerebellum. Neuroscience 45:671-690.
61. Ishida I, Ichikawa T, Deguchi T. 1983. Immunochemical and immunohistochemical studies on the specificity of a monoclonal antibody to choline acetyltransferase. Neurosci Lett 42:267-271.
62. Jones BE, Beaudet A. 1987. Distribution of acetylcholine and catecholamine neurons in the cat brainstem: a choline acetyltransferase and tyrosine hydroxylase immunohistochemical study. J Comp Neurol 261: 15-32.
63. Kappers CUA, Huber GC, Crosby EC. 1936. The comparative anatomy of the nervous system of vertebrates, including man [reprinted in 1967]. New York: Hafner.
64. Kása P. 1986. The cholinergic neurons in brain and spinal cord. Progr Neurobiol 26:211-272.
65. Kanwal JS, Finger TE. 1997. Parallel medullary gustatospinal pathways in a catfish: possible neural substrates for taste-mediated food search. J Neurosci 17:4873-4885
66. Kimura H, McGeer PL, Peng J-H, McGeer EG. 1980. Choline acetyltransferase-containing neurons in rodent brain demonstrated by immunohistochemistry. Science 208:1057-1059.
67. Kimura H, McGeer PL, Peng J-H, McGeer EG. 1981. The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200:151-201.
68. Kimura H, McGeer PL, Peng J-H, McGeer EG. 1984. Choline acetyltransferase-containing neurons in the rat brain. In: Björklund A, Hökfelt T, Kuhar MJ, editors. Handbook of chemical neuroanatomy, vol 3: classical transmitters and transmitter receptors in the CNS, part II. Amsterdam: Elsevier. p 51-67.
69. Koester DM. 1983. Central projections of the octavolateralis nerves of the clearnose skate, Raja eglanteria. J Comp Neurol 221:199-215.
70. Kosaka T, M Tauchi, Dahl JL. 1988. Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 70:605-617.
71. Kunzle H, Snyder H. 1984. The isthmus-tegmentum complex in the turtle and rat: a comparative analysis of its interconnections with the optic tectum. Exp Brain Res 56:509-522.
72. Kusunoki T, Tsuda Y, Takashima F. 1973. The chemoarchitectonics of the shark brain. J Hirnforsch 14:13-26.
73. Landis SC, Jackson PC, Fredieu JR, Thibault J. 1987. Catecholaminergic properties of cholinergic neurons and synapses in adult rat ciliary ganglion. J Neurosci 7:3574-3587.
74. Lavoie B, Parent A. 1994a. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190-209.
75. Lavoie B, Parent A. 1994b. Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344:232-241.
76. Lenhossék von M. 1894. Zur Kentniss des Ruckenmarkes der Rochen. Beiträge zur Histologie des Nervensystems und der Sinnesorgane. Wiesbaden: Bergman
77. Levey AI, Wainer BH. 1982. Cross-species and intraspecies reactivities of monoclonal antibodies against choline acetyltransferase. Brain Res 234:469-473.
78. Levey AI, Armstrong DM, Atweh SF, Terry RD, Wainer BH. 1983. Monoclonal antibodies to choline acetyltransferase: production, specificity, and immunocytochemistry. J Neurosci 3:1-9.
79. Levey AI, Wainer BH, Rye DB, Mufson EJ. Mesulam MM. 1984. Choline acetyltransferase-immunoreactive neurons in rodent cortex and distinction from acetylcholinesterase positive neurons. Neuroscience 13: 341-353.
80. Li R, Sakaguchi H. 1997. Cholinergic innervation of the song control nuclei by the ventral paleostriatum in the zebra finch: a double-labeling study with retrograde fluorescent tracers and choline acetyltranaferase immunohistochemistry. Brain Res 763:239-246.
81. Lumsden A, Keynes R. 1989. Segmental patterns of neuronal development in the chick hindbrain. Nature 337:424-428.
82. Maley BE, Frick ML, Levey AI, Wainer BH, Eide RP. 1988. Immunohistochemistry of choline acetyltransferase in the guinea pig brain. Neurosci Lett 84:137-142.
83. Manso MJ, Anadón R. 1993. A Golgi study of the telencephalon of the small-spotted dogfish Scyiorhinus canicula L. J Comp Neurol 333:485-502.
84. Marín O, González A. 1997. Origin of tectal cholinergic projections in amphibians. A combined study of choline acetyltransferase immunohistochemistry and retrograde transport of dextran amines. Vis Neurosci 16:271-283.
85. Marín O, Smeets WJ, González A. 1997. Distribution of choline acetyltransferase immunoreactivity in the brain of anuran (Rana perezi, Xenopus laevis) and urodele (Pleurodeles waltl) amphibians. J Comp Neurol 382:499-534.
86. Mason WT, Ho YW, Eckenstein F, Hatton GI. 1983. Mapping of cholinergic neurons associated with rat supraoptic nucleus: combined immunocytochemical and histochemical identification. Brain Res Bull 11:617-626.
87. Mazzi V. 1952. I fenomeni neurosecretori nel nucleo magnocellulare preottico dei Selachii e dei Ciclostomi. Riv Biol 44:429-449.
88. McCormick CA. 1983. Organization and evolution of the octavolateralis area of fishes. In: Northcutt RG, Davis RE, editors. Fish neurobiology, vol. I. Brain stem and sense organs. Ann Arbor, MI: University of Michigan Press. p 179-213.
89. Medina L, Reiner A. 1994. Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol 342:497-537.
90. Medina L, Smeets WJ, Hoogland PV, Puelles L. 1993. Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. J Comp Neurol 331:2611-285.
91. Mellinger JCA. 1963. Les Relations Neuro-Vasculo-Glandulaires dans l'Appareil Hypophysaire de la Rousette Scyliorhinus canicula L [thesis]: Faculty of Sciences, series E, no. 238. Strasbourg: Université Strasbourgh.
92. Meredith GE, Roberts BL. 1986. Central organization of the efferent supply to the labyrinthine and lateral line receptors of the dogfish. Neuroscience 17:225-233.
93. Meredith GE, Smeets WJAJ. 1987. Immunocytochemical analysis of the dopamine system in the forebrain and midbrain of Raja radiata: evidence for a substantia nigra and ventral tegmental area in cartilaginous fish. J Comp Neurol 265:530-548.
94. Mesulam MM, Mufson EJ, Levey AI, Wainer BH. 1984. Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry. Neuroscience 12:669-686.
95. Meurling P, Rodríguez EM. 1990. The paraventricular and posterior recess organs of elasmobranchs: a system of cerebrospinal fluid-contacting neurons containing immunoreactive serotonin and somatostatin. Cell Tissue Res 259:463-473.
96. Meurling P, Rodríguez EM, Pena P, Grondona JM, Pérez J. 1996. Hypophysial and extrahypophysial projections of the neurosecretory system of cartilaginous fishes: an immunocytochemical study using a polyclonal antibody against dogfish neurophysin. J Comp Neurol 373:400-421.
97. Molist P. 1990. Estudio Immunohistoquímico de Algunos Sistemas del Encéfalo de Algunos Seláceos [doctoral thesis]. Santiago de Compostela: University of Santiago de Compostela.
98. Molist P, Maslam S, Velzing E, Roberts BL. 1993a. The organization of cholinergic neurons in the mesencephalon of the eel, Anguilla anguilla, as determined by choline acetyltransferase immunohistochemistry and acetylcholinesterase enzyme histochemistry. Cell Tissue Res 271:555-566.
99. Molist P, Rodríguez-Moldes I, Anadón R. 1993b. Organization of catecholaminergic systems in the hypothalamus of two elasmobranch species, Raja undulata and Scyliorhinus canicula. A histofluorescence and immunohistochemical study. Brain Behav Evol 41:290-302.
100. Molist P. Rodríguez-Moldes I, Batten T, Anadón R. 1995. Distribution of calcitonin gene-related peptide (CGRP)-like immunoreactivity in the brain of the dogfish, Scyliorhinus canicula. J Comp Neurol 352:335-350.
101. Montgomery JC, Housley GD. 1983. The abducens nucleus in the carpet shark Cephaloscyllium isabella. J Comp Neurol 221:163-168.
102. Mufson EF, Cunningham MG. 1988. Observations of choline acetyltransferase containing structures in the CD-1 mouse brain. Neurosci Lett 84:7-12.
103. Mufson EJ, Desan PH, Mesulam MM, Wainer BH, Levey AI. 1984. Choline acetyltransferase-like immunoreactivity in the forebrain of the redeared pond turtle (Pseudemys scripta elegans). Brain Res 323:103-108.
104. Muñoz A, Muñoz M, Navarro B, Terres A, Marín O, González A. 1992. Cytoarchitecture and ultrastructural characteristics of the area octavolateralis of the urodele amphibian Pleurodeles waltlii. J Hirnforsch 33:499-507.
105. Muñoz-Maines VJ, Slemmon JR, Panicker MM, Neighbor N, Salvaterra PM. 1988. Production of polyclonal antisera to choline acetyltransferase using fusion protein produced by a cDNA clone. J Neurochem 50:167-175
106. Murakami T, Morita Y. 1987. Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebasticus marmoratus. J Comp Neurol 256:607-623.
107. Necker R. 1997. Projections of the marginal nuclei in the spinal cord of the pigeon. J Comp Neurol 377:95-104.
108. Nicholls GE. 1915. An occurrence of an intracranial ganglion upon the oculomotor nerve in Scyllium canicula, with a suggestion as to its bearing upon the question of the segmental value of certain of the cranial nerves. Proc R Soc London B 88:553-568.
109. Nicholson H. 1924. On the presence of ganglion cells in the third and sixth nerves of man. J Comp Neurol 37:31-36.
110. Nicholson LFB, Montgomery JC, Faull RLM. 1994. GABA, muscarinic Cholinergic, excitatory amino acid, neurotensin and opiate binding sites in the octavolateralis column and cerebellum of the skate Raja nasuta (Pisces: Rajidae). Brain Res 652:40-48.
111. Northcutt RG, Reiner A, Karten HJ. 1988. Immunohistochemical study of the telencephalon of the spiny dogfish, Squalus acanthias. J Comp Neurol 277:250-267.
112. Palouzier B, Barrit-Chamoin MC, Portalier P, Ternaux JP. 1987. Cholinergic neurons in the rat nodose ganglia. Neurosci Lett 80:147-152.
113. Parnavelas JG, Kelly W, Franke E, Eckenstein F. 1986. Cholinergic neurons and fibres in the rat visual cortex. J Neurocytol 15:329-336.
114. Paul DH, Roberts BL. 1977a. Studies on a primitive cerebellar cortex. II: The projection of the posterior lateral-line nerve to the lateral-line lobes of the dogfish brain. Proc R Soc London B 195:467-478.
115. Paul DH, Roberts BL. 1977b. Studies on a primitive cerebellar cortex. III: The projection of the anterior lateral line nerve to the lateral-line lobes of the dogfish hindbrain. Proc R Soc London B 195:479-496.
116. Paul DH, Roberts BL. 1984. Projections of cerebellar Purkinje cells in the dogfish, Scyliorhinus. Neurosci Lett 44:43-46.
117. Pérez SE, Adrio F, Rodríguez MA, Anadón R, Rodríguez-Moldes I. 1995. Nitric oxide synthase-like immunoreactive extrahypophysial projections of the neurosecretory preoptic nucleus of the electric ray (Elasmobranchs) suggest it is involved in neuroregulation of the brain and spinal cord. Neurosci Lett 195:85-88.
118. Phelps PE, Vaughn JE. 1986. Immunocytochemical localization of choline acetyltransferase in rat ventral striatum: a light and electron microscopic study. J Neurocytol 15:595-617.
119. Phelps PE, Barber RP, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. Postnatal development of neurons containing choline acetyltransferase in rat spinal cord: an immunocytochemical study. J Comp Neurol 229:347-361.
120. Poethke R, Härtig W, Brückner G, Felgenhauer K, Mäder M. 1997. Characterization of monoclonal and polyclonal antibodies to human choline acetyltransferase and epitope analysis. Biol Chem 378:997-1004.
121. Pombal MA, Rodicio MC, Anadón R. 1994. Development and organization of the oculomotor nuclei in the larval sea lamprey, Petromyzon marinus L. An HRP study. J Comp Neurol 341:393-406.
122. Pombal MA, Marín O, González A. 1999a. Choline acetyltransferase immunoreactivity in the hypothalamoneurohypophysial system of the lamprey. Eur J Morphol 37:103-106.
123. Pombal MA, Yáñez J, Marín O, González A, Anadón R. 1999b. Cholinergic and GABAergic neuronal elements in the pineal organ of lampreys, and tract-tracing observations of differential connections of pinealofugal neurons. Cell Tissue Res 295:215-223.
124. Powers AS, Reiner A. 1993. The distribution of cholinergic neurons in the central nervous system of turtles. Brain Behav Evol 41:326-345.
125. Puelles L. 1995. A segmental morphological paradigm for understanding vertebrate forebrains. Brain Behav Evol 46:319-337.
126. Ramón y Cajal SR. 1911. Histologie du Système Nerveux de l'Homme et des Vertébrés, vol II. Paris: Maloine.
127. Reiner A. 1991. A comparison of neurotransmitter-specific and neuropeptide-specific neuronal cell types present in the dorsal cortex in turtles with those present in the isocortex in mammals: implications for the evolution of the isocortex. Brain Behav Evol 38:53-91.
128. Repérant J, Miceli D, Rio JP, Peyrichoux J, Pierre J, Kirpitchnikova E. 1986. The anatomical organization of retinal projections in the shark Scyliorhinus canicula with special reference to the evolution of the selachian primary visual system. Brain Res 396:227-248.
129. Rhodes KJ, Zottoli SJ, Mufson EJ. 1986. Choline acetyltransferase immunohistochemical staining in the goldfish (Carassius auratus) brain: evidence that the Mauthner cell does not contain choline acetyltransferase. Brain Res 381:215-224.
130. Ribeiro da Silva A, Cuello AC. 1990. Choline acetyltransferase-immunoreactive profiles are presynaptic to primary sensory fibers in the rat superficial dorsal horn. J Comp Neurol 295:370-384.
131. Rico B, Cavada C. 1998. A population of cholinergic neurons is present in the macaque monkey thalamus. Eur J Neurosci 10:2346-2352.
132. Roberts BL. 1992. Differences in the dopaminergic innervation of the electroreceptive and mechanoreceptive medullary lateral line nuclei of the ray, Raja radiata. Brain Res 593:339-342.
133. Roberts BL, Maslam S, Los I, Van der Jagt B. 1994. Coexistence of calcitonin gene-related peptide and choline acetyltransferase in eel efferent neurons. Hearing Res 74:231-237.
134. Rodríguez-Moldes I, Manso MJ, Becerra M, Molist P, Anadón R. 1993. Distribution of substance P-like immunoreactivity in the brain of the elasmobranch Scyliorhinus canicula. J Comp Neurol 335:228-244.
135. Rosiles JR, Leonard RB, 1980. The organization of the extraocular motor nuclei in the Atlantic stingray, Dasyatis sabina. J Comp Neurol 193: 677-687.
136. Saji M, Miura M. 1991. Coexistence of glutamate and choline acetyltransferase in a major subpopulation of laryngeal motoneurons of the rat. Neurosci Lett 123:175-178.
137. Sann H, McCarthy PW, Mader M, Schemann M. 1995. Choline acetyltransferase-like immunoreactivity in small diameter neurones of the dorsal root ganglion. Neurosci Lett 198:17-20.
138. Satoh K, Fibiger HC. 1985. Distribution of central cholinergic neurons in the baboon (Papio papio), I. General morphology. J Comp Neurol 236: 197-214.
139. Satoh K, Armstrong DM, Fibiger HC. 1983. A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res Bull 11:693-720.
140. Schäfer MK-H, Eiden LE, Weihe E. 1998. Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter. I. Central nervous system. Neuroscience 84:331-359.
141. Scharrer E. 1952. Das Hypophysen-Zwischenhirnsystem von Scyllium stellatum. Z Zellforsch 37:196-204.
142. Schmidt AW, Bodznick D. 1987. Afferent and efferent connections of the vestibulolateral cerebellum of the little skate, Raja erinacea. Brain Behav Evol 30:282-302.
143. Shiromani PJ, Armstrong DM, Bruce G. Hersh LB, Groves PM, Gillin JC. 1987. Relation of pontine choline acetyltransferase immunoreactive neurons with cells which increase discharge during REM sleep. Brain Res Bull 18:447-455.
144. Shu SY, Penny GR, Peterson GM. 1988. The "marginal division": a new subdivision of the neostriatum of the rat. J Chem Neuroanat 1:147-163.
145. Smeets WJAJ. 1981. Retinofugal pathways in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 195:1-11.
146. Smeets WJAJ. 1982. The afferent connections of the tectum mesencephali in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 205:139-152.
147. Smeets WJAJ, Timerick SJB. 1981. Cells of origin of pathways descending to the spinal cord in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. J Comp Neurol 202:473-491.
148. Smeets WJAJ, Nieuwenhuys R, Roberts BL. 1983. The central nervous system of cartilaginous fishes. Berlin: Springer-Verlag.
149. Sorenson EM, Parkinson D, Dahl JL. Chiapinelli VA. 1989. Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. J Comp Neurol 281:641-657.
150. St-Jacques R, Gorczyca W, Mohr G, Schipper H-M. 1996. Cholinergic system of the dog: a choline acetyltransferase immunocytochemical study. J Comp Neurol 366:717-725.
151. Sterzi G. 1909. Il Sistema Nervoso Centrale dei Vertebrate, vol 2. Pesci I. Selaci. Padova: Draghi.
152. Strassman A, Mason P, Eckenstein F, Baughman RW, Maciewicz R. 1987. Choline acetyltransferase immunocytochemistry of Edinger-Westphal and ciliary ganglion afferent neurons in the cat. Brain Res 423:293-304.
153. Stuesse SL, Cruce WLR. 1992. Distribution of tyrosine hydroxylase, serotonin, and leu-enkephalin immunoreactive cells in the brainstem of a shark, Squalus acanthias. Brain Behav Evol 39:77-92.
154. Stuesse SL, Cruce WLR, Northcutt RG. 1990. Distribution of tyrosine hydroxylase-and serotonin-immunoreactive cells in the central nervous system of the thornback guitarfish, Platyrhinoidis triseriata. J Chem Neuroanat 3:45-58.
155. Stuesse SL, Cruce WLR, Northcutt RG. 1991a. Localization of serotonin, tyrosine hydroxylase, and leu-enkephalin immunoreactive cells in the brainstem of the horn shark, Heterodontus francisci. J Comp Neurol 308:277-292.
156. Stuesse SL, Cruce WLR, Northcutt RG. 1991b. Serotoninergic and enkephahnergic cell groups in the reticular formation of the bat ray and two skates. Brain Behav Evol 38:39-52.
157. Stuesse SL, Stuesse DC, Cruce WLR. 1995. Raphe nuclei in three cartilaginous fishes, Hydrolagus colliei, Heterodontus francisci, and Squalus acanthias. J Comp Neurol 358:414-427.
158. Tago H, McGeer PL, Bruce G, Hersh LB. 1987. Distribution of choline acetyltransferase-containing neurons of the hypothalamus. Brain Res 415:49-62.
159. Tago H, McGeer PL, McGeer EG, Akiyama H, Hersh LB. 1989. Distribution of choline acetyltransferase immunopositive structures in the rat brainstem. Brain Res 495:271-297.
160. Takami K, Kawai Y, Shiosaka S, Lee Y, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Tohyama M. 1985. Immunohistochemical evidence for coexistence of calcitonin gene-related peptide and choline acetyltransferase-like immunoreactivity in neurons of the rat hypoglossal, facial and ambiguus nuclei. Brain Res 328:386-389.
161. Tata AM, Plateroti M, Cibati M, Biagioni S, Augusti-Tocco G. 1994. Cholinergic markers are expressed in developing and mature neurons of chick dorsal ganglia. J Neurosci Res 37:247-255.
162. Thiriet G, Kempf J, Ebel A. 1992. Distribution of cholinergic neurons in the chick spinal cord during embryonic development. Comparison of ChAT immunocytochemistry with AChE histochemistry. Int J Dev Neurosci 10:459-466.
163. Timerick SB, Roberts BL, Paul DH. 1992. Brainstem neurons projecting to different levels of the spinal cord of the dogfish Scyliorhinus canicula. Brain Behav Evol 39:93-100.
164. Vaage S. 1969. The segmentation of the primitive neural tube in chick embryos (Callus domesticus). A morphological, histochemical and autoradiographical investigation. Adv Anat Embryol Cell Biol 41:1-88.
165. Vetter DE, Adams JC, Mugnaini E. 1991, Chemically distinct rat olivocochlear neurons. Synapse 7:21-43.
166. Villani L, Guarnieri T, Zironi I. 1994. Choline acetyltransferase and NADPH-diaphorase localization in the goldfish habenulo-interpeduncular system. Neurosci Lett 173:67-70.
167. Vinay L, Bussières N, Shupliakov O, Dubuc R, Grillner S. 1998. Anatomical study of spinobulbar neurons in lampreys. J Comp Neurol 397: 475-492.
168. Vincent SR, Reiner A. 1987. The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 18:371-415.
169. Wessler I, Reichenheimer T, Bittinger F, Kirkpatrick CJ, Schenda J, Vollrath L. 1997. Day-night rhythm of acetylcholine in the rat pineal gland. Neurosci Lett 224:173-176.
170. Wetts R, Vaughn JE. 1994. Choline acetyltransferase and NADPH diaphorase are co-expressed in rat spinal cord neurons. Neuroscience 63: 1117-1124.
171. Withington-Wray DJ, Roberts BL, Taylor EW. 1986. The topographical organization of the vagal motor column in the elasmobranch fish, Scyliorhinus canicula L. J Comp Neurol. 248:95-104.
172. Witkovsky P, Roberts BL. 1975. The light microscopical structure of the mesencephalic nucleus of the fifth nerve in the selachian brain. Proc R Soc London B 190:457-471.
173. Woolf NJ, Butcher LL. 1989. Cholinergic systems in the rat brain: IV. Descending projection of the pontomesencephalic tegmentum. Brain Res Bull 23:519-540.
174. Woolf NJ. 1991. Cholinergic systems in mammalian brain and spinal cord. Progr Neurobiol 37:475-524.
175. Wullimann MF, Roth G. 1992. Is the nucleus corticalis of teleosts a new cholinergic central nervous system for vertebrates? Neuroreport 3:33-35.
176. Yáñez J, Anadón R. 1994. Afferent and efferent connections of the habenula in the larval sea lamprey (Petromyzon marinus L.). An experimental study. J Comp Neurol 345:148-160
177. Yáñez J, Anadón R. 1996. Afferent and efferent connections of the habenula in the rainbow trout (Oncorhynchus mykiss). An indocarbocyanine dye (DiI) study. J Comp Neurol 372:529-543.
178. Yáñez J, Pombal MA, Anadón R. 1999. Afferent and efferent connections of the parapineal organ in lamprey: a tract tracing and immunocytochemical study. J Comp Neurol 403:171-189.
179. Zottoli SJ, Rhodes KJ, Mufson EJ. 1987. Comparison of acetylcholinesterase and choline acetyltransferase staining patterns in the optic tectum of the goldfish Carassius auratus. A histochemical and immunocytochemical analysis. Brain Behav Evol 30:143-159.
180. Zottoli SJ, Rhodes KJ, Corrodi JG, Mufson EJ. 1988. Putative cholinergic projections from the nucleus isthmi and the nucleus reticularis mesencephali to the optic tectum in the goldfish (Carassius auratus). J Comp Neurol 273:385-398.