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Neurotransmitter organization of the nucleus of Edinger–Westphal and its projection to the avian ciliary ganglion

Published online by Cambridge University Press:  02 June 2009

Anton Reiner ,
Jonathan T. Erichsen ,
John B. Cabot ,
Craig Evinger ,
Malinda E. C. Fitzerald  and
Harvey J. Karten
Anton Reiner
Affiliation:
Department of Anatomy and Neurobiology, University of Tennesse, Memphis
Jonathan T. Erichsen
Affiliation:
Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook
John B. Cabot
Affiliation:
Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook
Craig Evinger
Affiliation:
Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook
Malinda E. C. Fitzerald
Affiliation:
Department of Anatomy and Neurobiology, University of Tennesse, Memphis
Harvey J. Karten
Affiliation:
Department of Neurosciences, University of California at San Diego, La Jolla
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Abstract

Two morphologically distinct types of preganglionic endings are observed in the avian ciliary ganglion: boutonal and cap-like. Boutonal endings synapse on ciliary ganglion neurons (called choroidal neurons) innervating choroidal blood vessels, while cap-like endings synapse on ciliary ganglion neurons (called ciliary neurons) controlling the lens and pupil. Some of both types of preganglionic endings contain the neuropeptides substance P (SP) and/or leucine-enkephalin (LENK). Although both types of preganglionic terminals are also known to be cholinergic, there has been no direct evidence that SP and LENK are found in cholinergic endings in the ciliary ganglion. The present studies in pigeons, which involved the use of single- and double-label immunohistochemical techniques, were undertaken to examine this issue, as well as to (1) determine the relative percentages of the boutonal and cap-like endings that contain SP, LENK, or both SP and LENK; and (2) determine if the two different types of terminals in the ciliary ganglion arise from different subdivisions of the nucleus of Edinger-Westphal (EW).

Single- and double-label immunohistochemical studies revealed that all neurons of EW, regardless of whether they contained immunohistochemically detectible amounts of SP or LENK, are cholinergic. In the medial subdivision of EW (EWM), which was found to contain approximately 700 neurons, 20.2% of these neurons were observed to contain both SP and LENK, while 11.6% were observed to contain SP only and 10.7% were observed to contain LENK only. In contrast, in lateral EW (EWL), which was found to contain approximately 500 neurons, 16.2% of the neurons were observed to contain both SP and LENK, while 19.2% of the neurons were observed to contain SP only and 12.6% were observed to contain LENK only. Retrograde-labeling studies involving horseradish peroxidase injections into the ciliary ganglion revealed that EW was the sole source of input to the ciliary ganglion and all, or nearly all, neurons in EW innervate the ciliary ganglion.

Immunohistochemical labeling of the ciliary ganglion neurons with an antiserum against choline acetyltransferase revealed that approximately 900 choroidal neurons and approximately 600 ciliary neurons are present in the ganglion, all of which receive cholinergic preganglionic endings. Of the choroidal neurons, 94% receive butonal terminals containing both SP and LENK, while only 2% receive SP+ only boutonal endings and 2% receive LENK+ only butonal endings. Of the ciliary neurons, 25% receive cap-like endings containing both SP and LENK, 30% receive cap-like endings containing only SP and 3% receive cap-like endings containing only LENK. Total unilateral lesions of EW resulted in the loss of all SP+ or LENK+ terminals in the ipsilateral ganglion. Subtotal EW lesions that spared either part of EWM or part of EWL revealed that boutonal endings arise from EWM neurons and cap-like endings from EWL neurons.

The present results suggest that the choroidal neurons, which regulate choroidal blood flow, may be relatively uniform in their functional properties since they nearly all receive boutonal endings from EWM that co-contain SP, LENK, and acetylcholine. In contrast, the ciliary neurons, which receive their preganglionic input from EWL, may consist of at least three major functionally distinct subgroups: (1) those receiving SP/LENK/acetylcholine-containing cap-like endings; (2) those receiving SP/acetylcholine-containing cap-like endings; and (3) those receiving acetylcholine-containing cap-like endings. The functional diversity of ciliary neurons may in part be related to the fact that some ciliary neurons innervate the iris and others the ciliary body.

Keywords

Substance PEnkephalinAcetylcholineCo-occurrenceAccommodationPupilChoroidImmunohistochemistry
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 5 , May 1991 , pp. 451 - 472
Copyright
Copyright © Cambridge University Press 1991

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References

Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anatomical Record 94, 239–247.CrossRefGoogle ScholarPubMed
Akert, K., Glickman, M.A., Lang, W., Grob, P. ' Huber, A. (1980). The Edinger–Westphal nucleus in the monkey. A retrograde tracer study. Brain Research 184, 491–498.CrossRefGoogle ScholarPubMed
Anderson, K.D. ' Reiner, A. (1990 a). The extensive co-occurrence of substance P and dynorphin in striatal projection neurous: an evolutionarily conserved feature of basal gangila organization. Journal of Comparative Neurology 295, 339–369.CrossRefGoogle Scholar
Anderson, K.D. ' Reiner, A. (1990 b). The distribution and relative abundance of neurons in the pigeon forebrain containing somatostatin, neuropeptide Y, or both. Journal of Comparative Neurology 299, 261–282.CrossRefGoogle ScholarPubMed
Ariens-Kappers, C.U., Huber, G.C. ' Crosby, E.C. (1936). The Comparative Anatomy of the Nervous System of Vertebrates, including Man. New York: McMillan Co.Google Scholar
Armstrong, E. (1982). A look at relative brain size in mammals. Neuroscience Letters 34, 101–104.CrossRefGoogle Scholar
Bloch, B., Baird, A., Ling, N., Benoit, R. ' Guillemin, R. (1983). Immunohistochemical evidence that brain enkephalins arise from a precursor similar to adrenal preproenkephalin. Brain Research 263, 251–257.CrossRefGoogle ScholarPubMed
Boyd, R.T., Jacob, M.H., Couturier, S., Ballivet, M. ' Berg, D.K. (1988). Expression and regulation of neuronal acetylcholine receptor mRNA in chick ciliary ganglia. Neuron 1, 495–502.CrossRefGoogle ScholarPubMed
Brecha, N.C. ' Karten, H.J. (1981). Organization of the avian accessory optic system. Annals of the New York Academy of Sciences 374, 215–229.CrossRefGoogle ScholarPubMed
Burde, R.M. ' Loewy, A.D. (1980). Central origin of oculomotor parasympathetic neurons in the monkey. Brain Research 198, 434–439.CrossRefGoogle ScholarPubMed
Cabot, J.B., Reiner, A. ' Bogan, N. (1982). Avian bulbospinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories, and laminar terminations. In Progress in Brain Research, ed. Kuypers, H.G.J.M. ' Martin, G.F. pp. 79–108New York: ElsevierGoogle Scholar
Cantino, D. ' Mugnaini, E. (1974). Adrenergic innervation of the parasympathetic ciliary ganglion in the chick. Science 185, 279–280.CrossRefGoogle ScholarPubMed
Carpenter, M.B. ' Sutin, J. (1983). Human Neuroanatomy, 8th edition. Baltimore, Maryland: Williams and Wilkins.Google Scholar
Chiappinelli, V.A., Feng, C. ' McMahon, L. (1989). Presynaptic responses to opioid peptides and substance P in the avian ciliary ganglion. Investigative Ophthalmology and Visual Science (Suppl) 30, 125.Google Scholar
Clarke, R.J., Coimbra, C.J.P. ' Alessio, M.L. (1985). Distribution of parasympathetic motorneurones in the oculomotor complex innervating the cliary ganglion in the marmoset (Callithrix jacchus). Acta Anatomica 121, 53–58.CrossRefGoogle Scholar
Cowan, W.M. ' Wenger, E. (1968). Degenration in the nucleus of origin of the preganglionic fibers to the chick ciliary ganglion following early removal of the optic vesicle. Journal of Experimental zoology 168, 105–124.CrossRefGoogle Scholar
Cuello, A.C., Galfre, G. ' Milstein, C. (1979). Detection of substance P in the central nervous system by a monoclonal antibody. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3532–3536.CrossRefGoogle ScholarPubMed
Cuello, A.C., Milstein, C., Coutre, R., Wright, B., Priestley, J.V. ' Jarvis, J., (1984). Characterization and immunocytochemical application of monoclonal antibodies against enkephalins. Journal of Histochemistry and Cytochemistry 32, 947–957.CrossRefGoogle ScholarPubMed
Davis, R., Koelle, G.B. ' Sanville, U.J. (1984). Electron-microscopic localization of acetylcholinesterase and butyrylcholinesterase in the ciliary ganglion of the cat. Journal of Histochemistry and Cytochemistry 32, 849–861.Google Scholar
Dryer, S.E. ' Chiappinelli, V.A. (1983). Kappa-bungarotoxin: an intracellular study demonstrating blockade of neuronal nicotinic receptors by a snake neurotoxin. Brain Research 289, 317–321.CrossRefGoogle ScholarPubMed
Dryer, S.E. ' Chiappinelli, V.A. (1985 a). Substance P depolarizes nerve terminals in an autonomic ganglion. Brain Research 336, 190–194.CrossRefGoogle Scholar
Dryer, S.E. ' Chiappinelli, V.A. (1985 b). Properties of choroid and ciliary neurons in the avain ganglion and evidence for substance P as a neurostramitter. Journal of Neuroscience 5, 2654–2661.CrossRefGoogle Scholar
Dryer, S.E. ' Chiappinelli, V.A. (1985 c). Electrophysiological evidence for substance P as a neurotransmitter in the ciliary ganglion. Society for Neuroscience Abstracts 11, 707.Google Scholar
Dryer, S.E. ' Chiappinelli, V.A. (1985 d). An intracellular study of synaptic transmission and dendritic morphology in sympathetic neurons of the chick embryo. Developmental Brain Research 22, 99–111.CrossRefGoogle Scholar
Erichsen, J.T. ' Evinger, C. (1985). Transsynaptic retrograde studies of the nucleus of Edinger–Westphal and the oculomotor system. Society for Neuroscience Abstracts 11, 1040.Google Scholar
Erichsen, J.T. ' Evinger, C. (1989). A unique subpopulation of medial rectus motorneurons and its relationship with the nucleus of Edinger-Westphal. Society for Neuroscience Abstracts 15, 240.Google Scholar
Erichsen, J.T.Karten, H.J., Eldred, W.D. ' Brecha, N.C. (1982 a). Localization of substance P-like abd enkephalin-like immunoreactivity within preganglionic terminals of the avian ciliary ganglion: light and electron microscopy. Journal of Neuroscience 2, 994–1003CrossRefGoogle Scholar
Erichsen, J.T., Reiner, A. ' Karten, H.J. (1982 b). The co-occurrence of substance P-like and leucine-enkephalin-like immunoreactives in neurons and fibers of the avian nervous system. Nature (London) 295, 407–410.Google Scholar
Erichsen, J.T., Keyser, K.T., Zukin, R.S. ' Karten, H.J. (1984). Optiate receptors: characterization in the avian ciliary ganglion. Society for Neuroscience Abstracts 10, 989.Google Scholar
Evinger, C. (1988). Extraocular motor nuclei: location, morphology, and afferents. in Neuroanatomy of the Oculomotor System, ed. Buttner-Ennever, J.A. pp. 81–117. New York: Elsevier Science Publishers.Google Scholar
Fitzgerald, M.E.C., Vana, B.A. ' Reiner, A. (1990 a). Evidence for retinal pathology following interruption of neural regulation of choroidal blood flow: Möller cells express GFAP following lesions of the nucleus of Edinger-Westphal in pigeons. Current Eye Research 9(6), 583–598.CrossRefGoogle Scholar
Fitzgerald, M.E.C., Vana, B.A. ' Reiner, A. (1990 b). Control of choroidal blood flow by the nucleus of Edinger-Westphal: a laster-Doppler study. Investigative Ophthamology and Visual Science 31, 2483–2492.Google ScholarPubMed
Gallagher, J.P., Griffith, W.H., ' Schinnick-Gallagher, P. (1982). Cholinergic transmission in cat parasympathetic ganglia. Journal of Physiology (London) 332, 473–486.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R., Reiner, A., Erichsen, J.T., Cohen, D.H. ' Karten, J.J. (1984). The neural substrate for the pupillary light reflex in pigeons. Journal of Comparative Neurology 226, 523–543.CrossRefGoogle Scholar
Gamlin, P.D.R., Reiner, A., Karten, H.J. (1982). Substance P-containing neurons of the avian suprachiasmatic nucleus project directly to the nucleus of Edinger-Westphal. Proceedings of the National Academy of Sciences of the U.S.A. 79, 3891–3895.CrossRefGoogle Scholar
Gherezghiher, T., Hey, J. ' Koss, M. (1989). Cholinergic control of intraocular pressure. Investigative Ophthalmology and Visual Science (Suppl.) 30, 20.Google Scholar
Grimes, P.A., McGlinn, A. ' Stone, R.A. (1990). Neuropeptide localization in cat ciliary ganglion. Investigative Ophthalmology and Visual Sciences (Suppl.) 31, 40.Google Scholar
Hara, H., Kobayashi, S., Sugita, k. ' Tsukahara, S. (1982). Innervation of dog ciliary ganglion. Histochemistry 76, 295–301.CrossRefGoogle ScholarPubMed
Hess, A. (1965). Developmental changes in the structure of the synapse on the myelinated cell bodies of the chicken ciliary ganglion. Journal of Cell Biology 25, 1–19.CrossRefGoogle ScholarPubMed
Itoh, K., Konishi, A., Nomura, S., Mizuno, N., Nakamura, Y. ' Sugimoto, T. (1979). Application of coupled oxidation reaction to electron-microscopic demonstration of horseradish peroxidase: cobalt-glucose oxidase method. Brain Research 175, 341–346.CrossRefGoogle ScholarPubMed
Jampel, R.S. (1960). Convergence, divergence, pupillary reactions, and accomodation of the eyes from Faradic stimulation of the macaque brain. Journal of Comparative Neurology 115, 371–400.CrossRefGoogle Scholar
Jampel, R.S. ' Mindel, J. (1967). The nucleus for accommodation in the midbrain of the macaque. Investigative Ophthalmology 6, 40–50.Google ScholarPubMed
Johnson, D.C. ' Epstein, M.L. (1986). Monoclonal antibodies and polyvalent antiserum to chicken choline acetyltransferase. Journal of Neurochemistry 46, 968–976.CrossRefGoogle ScholarPubMed
Karten, H.J. ' Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia) Baltimore, Maryland: The Johns Hopkins Press.Google Scholar
katayama, Y. ' Nishi, S., (1984). Sites and mechanisms of actions of enkephalin in the feline parasympathetic ganglion. Journal of Physiology (London) 351, 111–121.CrossRefGoogle ScholarPubMed
Khachaturian, H., Lewis, M.E., ' Watson, S.J. (1983). Co-localization of proenkephalin peptides in rat brain regions. Brain Research 279, 369–373.CrossRefGoogle Scholar
Kondo, H., Katayama, Y. ' Yui, R. (1982). On the occurance and physiological effect of somatostalin in the ciliary ganglion of cats. Brain Research 247, 141–144.CrossRefGoogle ScholarPubMed
Landmesser, L. ' Pilar, G. (1970). Selective reinnervation of two cell populations in the adult pigeon ciliary ganglion. Journal of Physiology (London) 211, 203–216.CrossRefGoogle ScholarPubMed
Landmesser, L. ' Pilar, G. (1974). Synapse formation during embryogenesis on ganglion cells lacking a periphery. Journal of Physiology (London) 241, 715–736.CrossRefGoogle ScholarPubMed
Landmesser, L. ' Pilar, G., (1978). Interactions between neurons and their targets during in vivo synaptogenesis. Federation Proceedings 37, 2016–2022.Google ScholarPubMed
Lindberg, I. (1986). On the evolution of proenkaphalin. Trends in Pharmacological Science 7, 216–217.Google Scholar
Loewy, A.D., Saper, C.B. ' Yamodis, N.D., (1978). Re-evaluation of the efferent projections of the Edinger-Westphal nucleus. Brain Research 141, 153–159.CrossRefGoogle ScholarPubMed
Loring, R.H. ' Zigmond, R.E. (1987). Ultrastructural distribution of [125]-toxin bindings sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors. Journal of Neuroscience 7, 2152–2162.CrossRefGoogle ScholarPubMed
Lyman, D. ' Mugnaini, E. (1980). The avian accessory oculomotor nucleus. Society for Neuroscience Abstracts 6, 479.Google Scholar
Margiotta, J.F. ' Berg, D.K. (1986). Enkephalin and substance P modulate synaptic properties of chick ciliary ganglion neurons in cell culture. Neuroscience 18, 175–182.Google Scholar
Margioptta, J.F., Berg, D.K. ' Dionne, V.E. (1987). The properties and regulation of funtional acetylcholine receptors on chick ciliary ganglion neurons. Journal of Neuroscience 7, 3612–3622.CrossRefGoogle Scholar
Marwitt, R., Pilar, G. ' Weakly, J.N. (1971). Characterization of two ganglion cell populations in avaian ciliary ganglion. Brain Research 25, 317–334.Google Scholar
McLean, I.W. ' Nakane, P.K. (1974). Periodate-Iysine-paraformaldehyde fixative: a new fixative for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 1077–1083.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). Tetramethylbenzidine for horseradish peroxidase neurochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.CrossRefGoogle Scholar
Millar, T.J., Ishimoto, I.Epstein, M.L., Johnson, C.D. ' Morgan, I.G. (1987). Cholinergic amacrine cells of the chicken retina: a light and electron-microscope immunocytochemical study. Neuroscience 21, 725–743.Google Scholar
Narayanan, C.H. ' Narayanan, Y. (1976). An experimental inquiry into the central source of preganglionic fibers to the chick ciliary ganglion. Journal of Comparative Neurology 166, 101–109.CrossRefGoogle Scholar
Philippe, E. ' Tremblay, J.P. (1981). In Vivo stimulation of a cholinergic synapse of the chick ciliary ganglion induces a reduction in the number of dense core vesicles. Neuroscience Letters, 24, 307–312.CrossRefGoogle ScholarPubMed
Philippe, E. ' Tremblay, J.P. (1983). Increased number pre-area of peptidergic and cholinergic vesicles in synapses of the chick ciliary ganglion following 10 Hz in vivo stimulation. Neuroscience Letters, 35, 149–154.CrossRefGoogle Scholar
Pilar, G., Landmesser, L. ' Burstein, L. (1980). Competition for survival among developing ciliary ganglion cells. Journal of Neurophysiology 43, 233–254.CrossRefGoogle ScholarPubMed
Pilar, G.Tuttle, J.B. (1982). A simple neuronal system with range of uses: the avian ciliary ganglion. In Progress in Cholinergic Biology: Model Cholinergic Synapses ed. Goldberg, A. ' Hanin, I. pp. 213–247. New York: Raven Press.Google Scholar
Pilar, G. ' Vaughn, P.C. (1969). Electrophysiological investigations of the pigenon iris neuromusculer junctions. Comparative Biochemistry and Physiology 29, 51–72.CrossRefGoogle Scholar
Reiner, A. (1986). The co-occurrence of substance P-like immunore-activity and dynorphin-like immuoreactivity in striatopallidal and straitonigral projection neurons in birds and reptiles. Brain Research 371, 155–161.CrossRefGoogle Scholar
Reiner, A. (1987 a). A VIP-like peptide co-occurs with substance P and enkephalin in cholinergic preganglionic terminals of the avian ciliary ganglion. Neuroscience Letters 78, 22–28.CrossRefGoogle ScholarPubMed
Reiner, A. (1987 b). The distribution of proenkephalin-derived peptides in the central nervous system of turtle. Journal of Comparative Neurology 259, 65–91.CrossRefGoogle Scholar
Reiner, A. (1987 c). The presence of substance P/CGRP-containing fibers, VIP-containing fibers and numerous cholinergic fibers on blood vessels of the avian choroid. Investigative Ophthalmology and Visual Science (Suppl.) 28, 81.Google Scholar
Reiner, A. ' Carraway, R.C. (1987). Immunohistochemical and biochemical studies on Lys8-Asn9-Neurotensin 8–13 (LANT6)- related pepties in the basal ganglia of pigeons, turtles and hamster. Journal of Comparative Neurology 257, 453–476.CrossRefGoogle Scholar
Reiner, A., Davis, B.M.Brecha, N.C. ' Karten, H.J. (1984). The distribution of enkephalin-like immunoreactivity in the telencephalon of the adult and developing domestic chicken. Journal of Comparative Neurology 228, 245–262.CrossRefGoogle Scholar
Reiner, A., Eldred, W.D., Beinfeld, M.C. ' Krause, J.E. (1985). The co-occurance of a substance P-like peptide and cholecystokinin-8 in a fiber system of turtle contex. Journal of Neuroscience 5, 1522–1526CrossRefGoogle Scholar
Reiner, A., Fitzgerald, M.E.C. ' Gamlin, P.D.R. (1990). Central neural circuits controlling choroidal blood flow: a laser-Doppler study. Investigative Ophthalmology and Visual Science (Suppl.) 31, 38.Google Scholar
Reiner, A., Karten, H.J., Gamlin, P.D.R. ' Erichsen, J.T. (1983 a). Parasympathetic control of ocular function: functional subdivisions and connections of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6, 140–145.Google Scholar
Reiner, A., Karten, H.J. ' Solina, A.R. (1983 b). Substance P: localization within paleostriatal-tegmental pathways in pigeons. Neuroscience 9, 61–85.Google Scholar
Role, L.W. (1984). Substance of P modulation of acetylcholine-induced currents in embryonic chicken sympathetic and ciliary ganglion neurons. Proceedings of the National Academy of Sciences of the U.S.A. 81, 2924–2928.CrossRefGoogle ScholarPubMed
Smith, M.A., Stollberg, J., Lindstrom, J.M. ' Berg, D.K. (1985). Characterization of a component in chick ciliary ganglia that crossreacts with monoclonal antibodies to muscle and electric organ acetylcholine receptor. Journal of Neurosciences 5, 2726–2731.Google Scholar
Sorenson, E.M., Parkinson, D., Dahl, J.L. ' Chiappinelli, V.A. (1989). Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. Journal of Comparative Neurology 281, 641–657.Google Scholar
Stjernschantz, J., Alm, A. ' Bill, A. (1976). Effects of intracranial oculomotor nerve stimulation on ocular blood flow in rabbits: modification by indomenthacin. Experimental Eye research 23, 461–469.CrossRefGoogle Scholar
Stjernschantz, J. ' Bill, A. (1979). Effect of intracranial stimulation of the oculomotor nerve on ocular blood flow in the monkey, cat, and rabbit. Investigative Ophthalmology and Visual Science 18, 99–103.Google Scholar
Terzuolo, C.A. (1951). Richerche sul ganglio ciliare degli Uccelli. Connessioni e mutamenti in relazione all's eta' e dopo recisione delle fibre pergangliari. Zum Zellforschung und Mikroskopische Anatomie 36, 255–267.CrossRefGoogle Scholar
Toyoshima, K., Kawana, E. ' Sakai, H. (1980). On the neuronal origin of the afferents to the ciliary ganglion in the cat. Brain Research, 67–76.CrossRefGoogle Scholar
Tremblay, J.P. ' Philippe, E. (1981). Morphological changes in presynaptic terminals of the chick ciliary ganglion after stimulation in vivo. A sterological study showing a net loss of total membrane. Experimental Brain Research 43, 439–446.Google Scholar
Wessendorf, M. ' Elde, R.P. (1985). Characterization of an immuno-fluorescence technique for the demonstration of co-existing neurotransmitters within nerve fibers and terminals. Journal of Histochemistry and Cytochemistry 33, 984–994.Google Scholar
White, J.D., Krause, J.E., Karten, H.J., ' McKelvy, J.F. (1985). Presence and ontogeny of enkephalin and substance P in the chick ciliary ganglion. Journal of Neurochemistry 45, 1319–1322.CrossRefGoogle ScholarPubMed
Wikler, K.C., Perez, G. ' Finlay, B.L. (1989). Duration of retinogenesis: its relationship to retinal organization in two cricetine rodents. Journal of Comparative Neurology 285, 157–176.CrossRefGoogle ScholarPubMed
Williams, R.C. ' Dockray, G.J. (1982). Differential distribution of Met-enkephalin and Met-enkephalin-Arg6-Phe7-like peptides revealed by immunohistochemistry. Brain Research 240, 167–170.CrossRefGoogle ScholarPubMed
Williams, R.G.. ' Dockray, G.J. (1983). Distribution of enkephalin-related peptides in rat brain: immunohistochemical studies using antisera to met-enkephalin and met-enkephalin Arg6Phe7. Neuroscience 9, 563–586.Google Scholar
Yoshida, K. (1953). Comparative anatomical and experimental studies on the oculomotor nucleus and neighboring nuclei. Acta Medica et Biologica 1, 143–161.Google Scholar