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Ultrastructure of the macaque ciliary ganglion

  • Published:
Journal of Neurocytology

Summary

The primate ciliary ganglion is an obligatory relay in the pathways that control the lens and pupil for the near response and the light reflex, two functions which have been the target of increasing inquiry in behavioural physiology paradigms. This investigation provides a comprehensive description of the ultrastructure of the ciliary ganglion in the rhesus monkey (Macaca mulatta). The results indicate that the ciliary ganglion contains a heterogeneous population of neurons in terms of somatic size, cytoplasmic contents and somatodendritic distribution of terminals. Variations in the clear and dense-cored vesicle content of the synaptic profiles present in the ganglion suggest that the synaptic inputs are also heterogeneous and may mediate separate functions. Several characteristic ultrastructural features of the macaque ciliary ganglion are noteworthy. Despite the large size of the neuronal somata, most cells do not exhibit contacts directly onto the somatic membrane. However, the few somata that do receive direct input often display several axosomatic contacts. The vast majority of synaptic interactions occur in the perisomatic neuropil, where the postsynaptic elements consist of simple and complex somatic appendages, as well as dendrites with their appendages. There is little neuropil independent of these immediately perisomatic regions. In some cases, axonal terminals form the central element of complex glomeruli, in which they are presynaptic to numerous spine-like profiles. In other cases, axon terminals and their postsynaptic targets are found within shallow depressions in the somatic membrane or, occasionally, deeply embedded within the borders of the postganglionic neuron. The somata and all the non-myelinated neuronal elements are surrounded by interdigitating, electron-dense processes of satellite cells. These glial cells are sometimes found in shallow recesses, or deeply embedded within the borders of the neuronal somata. The complexity of the ultrastructure of the ciliary ganglion in the macaque suggests that this ganglion may not be a simple relay in the parasympathetic outflow to the eye, but may instead be the site of neuronal processing of the preganglionic input.

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References

  • Akagi, Y., Ibata, Y. &Sano, Y. (1976) The sympathetic innervation of the ciliary body and trabecular meshwork of the cat.Cell and Tissue Research 173, 261–9.

    Google Scholar 

  • Akert, K., Glicksman, M. A., Lang, W., Grob, P. &Huber, A. (1980) The Edinger-Westphal nucleus in the monkey. A retrograde tracer study.Brain Research 184, 491–8.

    Google Scholar 

  • Akert, K., Pfenninger, K. &Sandri, C. (1967) The fine structure of synapses in the subfornical organ of the cat.Zeitschrift für Zellforschung und mikroskopische Anatomie 81, 537–56.

    Google Scholar 

  • Burde, R. M. (1988) Disparate visceral neuronal pools subserve spinal cord and ciliary ganglion in the monkey: a double labeling approach.Brain Research 440, 177–80.

    Google Scholar 

  • Burde, R. M. &Loewy, A. D. (1980) Central origin of oculomotor parasympathetic neurons in the monkey.Brain Research 198, 434–9.

    Google Scholar 

  • Cantino, D. &Mugnaini, E. (1974) Adrenergic innervation of the parasympathetic ciliary ganglion in the chick.Science 185, 279–81.

    Google Scholar 

  • Cantino, D. &Mugnaini, E. (1975) The structural basis for electrotonic coupling in the avian ciliary ganglion. A study with thin sectioning and freeze-fracturing.Journal of Neurocytology 4, 505–36.

    Google Scholar 

  • Chiba, T., Black, A. C., Jr. &Williams, T. H. (1977) Evidence for dopamine-storing interneurons and paraneurons in rhesus monkey sympathetic ganglia.Journal of Neurocytology 6, 441–53.

    Google Scholar 

  • Christensen, K. (1936) Sympathetic and parasympathetic nerves in the orbit of the cat.Journal of Anatomy 70, 225–32.

    Google Scholar 

  • Clarke, R. J., Coimbra, C. J. P. &Alessio, M. L. (1985) Distribution of parasympathetic motoneurons in the oculomotor complex innervating the ciliary ganglion in the marmoset (Callithrix jacchus).Acta Anatomica 121, 53–8.

    Google Scholar 

  • De Lorenzo, A. J. (1960) The fine structure of synapses in the ciliary ganglion of the chick.Journal of Biophysical and Biochemical Cytology 7, 31–6.

    Google Scholar 

  • Ehinger, B. &Falck, B. (1970) Uptake of some catecholamines and their precursors into neurons of the rat ciliary ganglion.Acta Physiologica Scandinavia 78, 132–41.

    Google Scholar 

  • Eranko, O., Soinila, S. &Paivarinta, H. (editors) (1980)Histochemistry and Cell Biology of Autonomic Neurons, SIF cells and Paraneurons. Advances in Biochemical Pharmacology, Vol. 25. New York: Raven Press.

    Google Scholar 

  • Erichsen, J. T., Evinger, C. &May, P. J. (1991) Pupillary and accommodative pre- and postganglionic neurons in the monkey and cat.Society for Neuroscience Abstracts 17, 461.

    Google Scholar 

  • Erichsen, J. T., Evinger, C. &May, P. J. (1992) Toward a functional anatomy of the cat Edinger-Westphal nucleus.Society for Neuroscience Abstracts 18, 855.

    Google Scholar 

  • Erichsen, J. T., Karten, H. J., Eldred, W. D. &Brecha, N. C. (1982) Localization of substance P-like and enkephalin-like immunoreactivity within preganglionic terminals of the avian ciliary ganglion: light and electron microscopy.Journal of Neuroscience 2, 994–1003.

    Google Scholar 

  • Fletcher, G. H. &Chiappinelli, V. A. (1992) An inward rectifier is present in presynaptic nerve terminals in the chick ciliary ganglion.Brain Research 575, 103–12.

    Google Scholar 

  • Forehand, C. J. (1987) Ultrastructural analysis of the distribution of synaptic boutons from labeled preganglionic axons on rabbit ciliary neurons.Journal of Neuroscience 7, 3274–81.

    Google Scholar 

  • Forehand, C. J. &Purves, D. (1984) Regional innervation of rabbit ciliary ganglion cells by the terminals of preganglionic axons.Journal of Neuroscience 4, 1–12.

    Google Scholar 

  • Gamlin, P. D. R. &Mays, L. E. (1992) Dynamic properties of medial rectus motoneurons during vergence eye movements.Journal of Neurophysiology 67, 64–74.

    Google Scholar 

  • Grillo, M. A. (1970) Cytoplasmic inclusions resembling nucleoli in sympathetic neurons of adult rats.Journal of Cell Biology 45, 100–17.

    Google Scholar 

  • Grimes, P. A. &Von Sallmann, L. (1960) Comparative anatomy of the ciliary nerves.Archives of Ophthalmology 64, 111–21.

    Google Scholar 

  • Grimes, P. A., McGlinn, A. M. &Stone, R. A. (1990) An immunohistochemically distinct population of cat ciliary ganglion cells.Brain Research 535, 323–6.

    Google Scholar 

  • Hanaichi, T., Sato, T., Iwamoto, T., Malavasi-Yamashiro, J., Hoshino, M. &Mizuno, N. (1986) A stable lead by modification of Sato's method.Journal of Electron Microscopy 4, 306.

    Google Scholar 

  • Hayat, M. A. (1981)Principles and Techniques of Electron Microscopy. Biological Applications. Rockville: Aspen Publishers Inc.

    Google Scholar 

  • 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.

    Google Scholar 

  • Huikuri, K. (1969) Electron microscopic observations on the granular vesicles in the ciliary ganglion of the rat.Experimentia 25, 1067–8.

    Google Scholar 

  • Hume, R. I. &Purves, D. (1983) Apportionment of the terminals from single preganglionic axons to target neurons in the rabbit ciliary ganglion.Journal of Physiology 383, 259–75.

    Google Scholar 

  • Hutchins, J. B. &Hollyfield, J. G. (1984) Autoradiographic identification of muscarinic receptors in human iris smooth muscle.Experimental Eye Research 38, 515–25.

    Google Scholar 

  • Ishikawa, S., Sekiya, H. &Kondo, Y. (1990) The center for controlling the near reflex in the midbrain of the monkey: a double labelling study.Brain Research 519, 217–22.

    Google Scholar 

  • Jackson, P. C. (1986) Innervation of the iris by individual parasympathetic axons in the adult mouse.Journal of Physiology 378, 485–95.

    Google Scholar 

  • Johnson, D. A. &Purves, D. (1981) Post-natal reduction of neural unit size in the rabbit ciliary ganglion.Journal of Physiology 318, 143–59.

    Google Scholar 

  • Johnson, D. A. &Purves, D. (1983) Tonic and reflex synaptic activity recorded in ciliary ganglion cells of anaesthetized rabbits.Journal of Physiology 339, 599–613.

    Google Scholar 

  • Judge, S. J. &Cumming, B. G. (1986) Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation.Journal of Neurophysiology 55, 915–30.

    Google Scholar 

  • Kawai, Y., Tamai, Y. &Senba, E. (1993) Principal neurons as local circuit neurons in the rat superior cervical ganglion: The synaptology of the neuronal processes revealed by intracellular injection of biocytin.Journal of Comparative Neurology 328, 562–74.

    Google Scholar 

  • Kondo, H., Dun, N. J. &Pappas, G. D. (1980) A light and electron microscopic study of the rat superior cervical ganglion cells by intracellular HRP-labeling.Brain Research 197, 193–9.

    Google Scholar 

  • Kondo, H., Katayama, Y. &Yui, R. (1982) On the occurrence and physiological effect of somatostatin in the ciliary ganglion of cats.Brain Research 247, 141–4.

    Google Scholar 

  • Kuchiiwa, S., Kuchiiwa, T. &Suzuki, T. (1989) Comparative anatomy of the accessory ciliary ganglion in mammals.Anatomy and Embryology 180, 199–205.

    Google Scholar 

  • Kuwayama, Y., Grimes, P. A., Ponte, B. &Stone, R. A. (1987) Autonomic neurons supplying the rat eye and the infraorbital distribution of vasoactive intestinal polypeptide (VIP)-like immunoreactivity.Experimental Eye Research 44, 907–22.

    Google Scholar 

  • Landis, S. C., Jackson, P. C., Fredieu, J. R. &Thibault, J. (1987) Catecholaminergic properties of cholinergic neurons and synapses in adult rat ciliary ganglion.Journal of Neuroscience 7, 3574–87.

    Google Scholar 

  • Landmesser, L. &Pilar, G. (1976) Fate of ganglionic synapses and ganglion cell axons during normal and induced cell death.Journal of Cell Biology 68, 357–74.

    Google Scholar 

  • Leblanc, G. G. &Landis, S. C. (1988) Target specificity of neuropeptide Y-immunoreactive cranial parasympathetic neurons.Journal of Neuroscience 8, 146–55.

    Google Scholar 

  • Leblanc, G. G., Trimmer, B. A. &Landis, S. C. (1987) Neuropeptide Y-like immunoreactivity in rat cranial parasympathetic neurons: coexistence with vasoactive intestinal peptide and choline acetyltransferase.Proceedings of the National Academy of Sciences (USA) 84, 3511–5.

    Google Scholar 

  • Loewy, A. D., Saper, C. B. &Yamodis, N. D. (1978) Re-evaluation of the efferent projections of the Edinger-Westphal nucleus the cat.Brain Research 141, 153–9.

    Google Scholar 

  • Martin, A. R. &Pilar, G. (1963a) Dual mode of synaptic transmission in the avian ciliary ganglion.Journal of Physiology 168, 443–63.

    Google Scholar 

  • Martin, A. R. &Pilar, G. (1963b) Transmission through the ciliary ganglion of the chick.Journal of Physiology 168, 464–75.

    Google Scholar 

  • Matthews, M. R. (1980) Ultrastructural studies relevant to the possible functions of small granule-containing cells in the rat superior cervical ganglion. InHistochemistry and Cell Biology of Autonomic Interneurons, SIF Cells and Paraneurons. Advances in Biochemical Pharmacology, Vol. 25 (edited byEranko, O., Sionila, S. &Paivarinta, H.) pp. 77–86. New York: Raven Press.

    Google Scholar 

  • Matthews, M. R. (1983) The ultrastructure of junctions in sympathetic ganglia of mammals. InAutonomic Ganglia. (edited byElfvin, L. -G.) pp. 27–66. Philadelphia: John Wiley & Sons Ltd.

    Google Scholar 

  • May, P. J. (1990) Ultrastructure and connections of iris and ciliary motoneurons in the primate ciliary ganglion.Society for Neuroscience Abstracts 16, 903.

    Google Scholar 

  • May, P. J. (1992) A light and electron microscopic examination of the light evoked blink reflex pathways in the macaque.Society for Neuroscience Abstracts 18, 855.

    Google Scholar 

  • May, P. J., Porter, J. D. &Gamlin, P. D. R. (1992) Interconnections between the primate cerebellum and midbrain near-response regions.Journal of Comparative Neurology 315, 98–116.

    Google Scholar 

  • Mays, L. E., Porter, J. D., Gamlin, P. D. R. &Tello, C. A. (1986) Neuronal control of vergence eye movements: neurons encoding vergence velocity.Journal of Neurophysiology 56, 1007–21.

    Google Scholar 

  • Maxwell, J. S. &King, W. M. (1992) Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys.Journal of Neurophysiology 68, 1248–60.

    Google Scholar 

  • Meyer, D. L., Meyer-Hamme, S. &Schaefer, K.-P. (1972) Electrophysiological investigation of refractive state and accommodation in the rabbit's eye.Pflugers Archives of the European Journal of Physiology 332, 80–6.

    Google Scholar 

  • Mugnaini, E., Osen, K. K., Dahl, A.-L., Frierich, V. L., Jr. &Korte, G. (1980) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse.Journal of Neurocytology 9, 537–70.

    Google Scholar 

  • Olucha, F., Martinez-Garcia, F. &Lopez-Garcia, C. (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase.Journal of Neuroscience Methods 13, 131–8.

    Google 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, 307–12.

    Google Scholar 

  • Philippe, E. &Tremblay, J. P. (1983) Increased number pre-area of peptidergic and cholinergic vesicles in synapses of the chick ciliary ganglion following 10 Hzin vivo stimulation.Neuroscience Letters 35, 149–54.

    Google Scholar 

  • Pilar, G., Landmesser, L. &Burstein, L. (1980) Competition for survival among developing ciliary ganglion cells.Journal of Neurophysiology 43, 233–54.

    Google Scholar 

  • Pomeroy, S. L. &Purves, D. (1988) Neuron/glia relationships observed over intervals of several months in living mice.Journal of Cell Biology 107, 1167–75.

    Google Scholar 

  • Purves, D., Hadley, R. D. &Voyvodic, J. T. (1986) Dynamic changes in the dendritic geometry of individual neurons visualized over periods of up to three months in the superior cervical ganglia of living mice.Journal of Neuroscience 6, 1051–60.

    Google Scholar 

  • Purves, D. &Hume, R. I. (1981) The relationship of postsynaptic geometry to the number of presynaptic axons that innervate autonomic ganglion cells.Journal of Neuroscience 1, 441–52.

    Google Scholar 

  • Reiner, A., Erichsen, J. T., Cabot, J. B., Evinger, C., Fitzgerald, M. E. C. &Karten, H. J. (1991) Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion.Visual Neuroscience 6, 451–72.

    Google Scholar 

  • Ruskell, G. L. (1973) Sympathetic innervation of the ciliary muscle in monkeys.Experimental Eye Research 16, 183–90.

    Google Scholar 

  • Ruskell, G. L. &Griffiths, T. (1979) Peripheral nerve pathway to the ciliary muscle.Experimental Eye Research 28, 277–84.

    Google Scholar 

  • Rye, D. B., Saper, C. B., Wainer, B. H. (1984) Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing, and combination with immunocytochemistry.Journal of Histochemistry and Cytochemistry 32, 1145–53.

    Google Scholar 

  • Sekiya, H., Kawamura, K. &Ishikawa, S. (1984) Projections from the Edinger-Westphal complex of monkeys as studied by means of retrograde axonal transport of horseradish peroxidase.Archives Italiennes de Biologie 122, 311–19.

    Google Scholar 

  • Stone, R. A., McGlinn, A. M., Kuwayama, Y. &Grimes, P. A. (1988) Peptide immunoreactivity of the ciliary ganglion and its accessory cells in the rat.Brain Research 475, 389–92.

    Google Scholar 

  • Sugimoto, T., Itoh, K. &Mizuno, N. (1978) Direct projections from the Edinger-Westphal nucleus to the cerebellum and spinal cord in the cat: an HRP study.Neuroscience Letters 9, 17–22.

    Google Scholar 

  • Szentagothai, J. (1964) The structure of the autonomic interneuronal synapse.Acta Neurovegetativa 26, 339–59.

    Google Scholar 

  • Takahashi, K. (1967) Special somatic spine synapses in the ciliary ganglion of the chick.Zeitschrift für Zellforschung 83, 70–5.

    Google Scholar 

  • Takahashi, K. &Hama, K. (1965a) Some observations on the fine structure of the synaptic area in the ciliary ganglion of the chick.Zeitschrift für Zellforschung 67, 174–84.

    Google Scholar 

  • Takahashi, K. &Hama, K. (1965b) Some observations on the fine structure of nerve cell bodies and their satellite cells in the ciliary ganglion of the chick.Zeitschrift für Zellforschung 67, 835–43.

    Google Scholar 

  • Tobari, I. (1971a) Electron microscopic study of ciliary ganglion. I. Fine structure of the ciliary ganglion cell in cat.Acta Ophthalmologica Japan 75, 719–27.

    Google Scholar 

  • Tobari, I. (1971b) Electron microscopic study of ciliary ganglion. II. Fine structure of nerve endings in ciliary ganglion of adult cat.Acta Ophthalmologica Japan 75, 739–47.

    Google Scholar 

  • Toyoshima, K., Kawana, E. &Sakai, H. (1980) On the neuronal origin of the afferents to the ciliary ganglion in cat.Brain Research 185, 67–76.

    Google Scholar 

  • Tyrrell, S., Siegel, R. E. &Landis, S. C. (1992) Tyrosine hydroxylase and neuropeptide Y are increased in ciliary ganglia of sympathetcomized rats.Neuroscience 47, 985–98.

    Google Scholar 

  • Uemura, Y., Sugimoto, T., Nomura, S., Nagatsu, I. &Mizuno, N. (1987) Tyrosine hydroxylase-like immunoreactivity and catecholamine fluorescence in ciliary ganglion neurons.Brain Research 416, 200–3.

    Google Scholar 

  • Warwick, R. (1954) The ocular parasympathetic nerve supply and its mesencephalic sources.Journal of Anatomy 88, 71–93.

    Google Scholar 

  • Williams, T. H. &Palay, S. L. (1969) Ultrastructure of small neurons in the superior cervical ganglion.Brain Research 15, 17–34.

    Google Scholar 

  • Wolf, G. A., Jr. (1941) The ratio of preganglionic neurons to postganglionic neurons in the visceral nervous system.Journal of Comparative Neurology 75, 235–42.

    Google Scholar 

  • Yoshida, M. (1971) Uber die ultrastruktur der nervenzellen des ganglion ciliare beim affen (Macacus irus F. Cuvier).Kobe Journal of Medical Science 17, 65–73.

    Google Scholar 

  • Zhang, Y., Mays, L. E. &Gamlin, P. D. R. (1992) Characteristics of near response cells projecting to the oculomotor nucleus.Journal of Neurophysiology 67, 944–60.

    Google Scholar 

  • Zhang, Y. L., Tan, C. K. &Wotig, W. C. (1993) The ciliary ganglion of the cat: a light and electron microscopic study.Anatomy and Embryology 187, 591–9.

    Google Scholar 

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  1. Department of Anatomy, University of Mississippi Medical Center, 2500 North State Street, 39216-4505, Jackson, MS, USA

    P. J. May & S. Warren

  2. Department of Ophthalmology, University of Mississippi Medical Center, 2500 North State Street, 39216-4505, Jackson, MS, USA

    P. J. May

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May, P.J., Warren, S. Ultrastructure of the macaque ciliary ganglion. J Neurocytol 22, 1073–1095 (1993). https://doi.org/10.1007/BF01235750

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