Summary
Putative cholinergic neurons in the photosensory pineal organ of a cyprinid teleost, the European minnow, were studied by use of choline acetyltransferase (ChAT) immunocytochemistry and acetylcholinesterase (AChE) histochemistry. Pinealofugally projecting neurons were visualized using retrograde HRP-filling through their cut axons. For comparison, the distribution of choline acetyltransferase immunoreactivity (ChAT-IR) and AChE-positive elements in the retina was investigated.
While the distributional patterns of ChAT-IR and strongly AChE-positive perikarya in the retina are similar and may represent the same neuronal population, ChAT-IR and AChE-positive elements in the pineal organ appear to belong to separate populations. In the retina, small- to medium-sized perikarya in the inner nuclear layer, and small perikarya in the ganglion cell layer are ChAT-IR and AChE positive. The entire inner plexiform layer is AChE positive, while only sublaminae 1, 2 and 4 are ChAT-IR. No indication of cholinergic activity was observed in the optic axon layer.
In the pineal organ, ChAT-IR is restricted to small perikarya situated rostrally and dorsally in the pineal end-vesicle. AChE-positive neurons are present throughout the pineal end-vesicle and the pineal stalk. The pineal tract (the pinealofugally projecting axons of intrapineal neurons) is strongly AChE positive, but displays no ChAT-IR. The distribution of pinealofugally projecting neurons, labeled with retrogradely transported HRP, is markedly dissimilar to that of the ChAT-IR elements. It is proposed that the photosensory pineal organ transmits photic information to the brain via a non-cholinergic pathway. The possibility that the ChAT-IR neurons represent small local interneurons is discussed in the light of comparative physiological and anatomical findings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amthor FR, Oyster CW, Takahashi ES (1984) Morphology of on-off direction-selective ganglion cells in the rabbit retina. Brain Res 298:187–190
Barlow HB, Hill RM, Levick WR (1964) Retinal ganglion cells responding selectivey to direction and speed of image motion in the rabbit. J Physiol (Lond) 173:377–407
Beaudet A, Burkhalter A, Reubi J-C, Cuénod M (1981) Selective bidirectional transport of 3H-D-asparate in the pigeon retinotectal pathway. Neuroscience 6:2021–2034
Contestable A, Zannoni N (1975) Histochemical localization of acetylcholinesterase in the cerebellum and optic tectum of four freshwater teleosts. Histochemistry 45:279–288
Dodt E (1963) Photosensitivity of the pineal organ in the teleost, Salmo irideus (Gibbons). Experientia 19:642–643
Eckenstein F, Sofroniew MV (1983) Identification of central cholinergic neurons containing both choline acetyltransferase and of central neurons containing only acetylcholinesterase. J Neurosci 3:2286–2291
Eckenstein F, Barde YA, Thoenen H (1981) Production of specific antibodies to choline acetyltransferase purified from pig brain. Neuroscience 6:993–1000
Ekström P (1985) Anterograde and retrograde labeling of central neuronal systems with horseradish peroxidase under in vitro conditions. J Neurosci Methods 15:21–35
Ekström P, Korf H-W (1985) Pineal neurons projecting to the brain of the rainbow trout, Salmo gairdneri Richardson (Teleostei). In vitro retrograde filling with horseradish peroxidase. Cell Tissue Res 240:693–700
Holmgren N (1917) Zur Frage der Epiphysen-Innervation bei Teleostiern. Folia Neurobiol 1:1–15
Holmgren N (1918) Über die Epiphysennerven von Clupea sprattus und harengus. Ark Zool 11 (25):1–5
Karnovsky MJ, Roots L (1963) A “direct-coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12:219–221
Kuljis RO, Karten HJ (1983) Modifications in the laminar organization of peptide-like immunoreactivity in the anuran optic tectum following retinal deafferentiation. J Comp Neurol 217:239–251
Kuljis RO, Krause JE, Karten HJ (1984) Peptide-like immunoreactivity in anuran optic nerve fibers. J Comp Neurol 226:222–237
Levey AI, Wainer BH, Rye DB, Mufson EJ, Mesulam M-M (1984) Choline acetyltransferase-immunoreactive neurons intrinsic to rodent cortex and distinction from acetylcholinesterase-positive neurons. Neuroscience 13:341–353
Masland RH, Mills JW, Cassidy C (1984a) The functions of acetylcholine in the rabbit retina. Proc R Soc Lond [Biol] 223:121–139
Masland RH, Mills JW, Hayden SA (1984b) Acetylcholine-synthesizing amacrine cells: identification and selective staining by using radioautography and fluorescent markers. Proc R Soc Lond [Biol] 223:79–100
McGeer PL, McGeer EG, Peng JH (1984) Choline acetyltransferase: purification and immunohistochemical localization. Life Sci 34:2319–2338
McNulty JA (1984) Functional morphology of the pineal complex in cyclostomes, elasmobranchs, and bony fishes. Pineal Res Rev 2:1–40
Meissl H, Dodt E (1981) Comparative physiology of pineal photo-receptor organs. In: Oksche A, Pévet P (eds) The pineal organ: Photobiology — Biochronometry — Endocrinology. Elsevier/ North Holland Biomedical Press, pp 61–80
Meissl H, George SR (1984) Electrophysiological studies on neuronal transmission in the frog's photosensory pineal organ. The effect of amino acids and biogenic amines. Vision Res 24:1727–1734
Migani P, Contestabile A, Cristini G, Labanti V (1980) Evidence of intrinsic cholinergic circuits in the optic tectum of teleosts. Brain Res 194:125–135
Oksche A, Kirschstein H (1971) Weitere elektronenmikroskopische Untersuchungen am Pinealorgan von Phoxinus laevis (Teleostei, Cyprinidae). Z Zellforsch 112:572–588
Omura Y (1984) Pattern of synaptic connections in the pineal organ of the ayu, Plecoglossus altivelis (Teleostei). Cell Tissue Res 236:611–617
Omura Y, Ali MA (1980) Responses of pineal photoreceptors in the brook and rainbow trout. Cell Tissue Res 208:111–122
Oswald RE, Freeman JA (1980) Optic nerve transmitters in lower vertebrate species. Life Sci 27:527–533
Sofroniew MW, Schrell U (1982) Long-term storage and regular repeated use of diluted antisera in glass staining jars for increased sensitivity, reproducibility, and convenience of singleand two-color light microscopic immunocytochemistry. J Histochem Cytochem 30:504–511
Tauchi M, Masland RH (1984) The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond [Biol] 223:101–119
Tumosa N, Eckenstein F, Stell WK (1984) Immunocytochemical localization of putative cholinergic neurons in the goldfish retina. Neurosci Lett 48:255–259
Vigh-Teichmann I, Korf H-W, Oksche A, Vigh B (1982) Opsinimmunoreactive outer segments and acetylcholinesterase-positive neurons in the pineal complex of Phoxinus phoxinus (Teleostei, Cyprinidae). Cell Tissue Res 227:351–369
Villani L (1982) Ultrastructural distribution of choline acetyltransferase in the goldfish optic tectum. Basic Appl Histochem 26:99–105
Vollrath L (1981) The pineal organ. In: Oksche A, Vollrath L (eds) Handbuch der mikroskopischen Anatomie der Menschen VI/7. Springer, Berlin Heidelberg New York
Wainer BH, Bolam JP, Freund TF, Henderson Z, Totterdell S, Smith AD (1984a) Cholinergic synapses in the rat brain: a correlated light and electron microscopic immunohistochemical study employing a monoclonal antibody against choline acetyltransferase. Brain Res 308:69–76
Wainer BH, Levey AI, Mufson EJ, Mesulam M-M (1984b) Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem Int 6:163–182
Wässle H (1982) Morphological types and central projections of ganglion cells in the cat retina. In: Osborne N, Chader G (eds) Progress in retinal research. Pergamon, Oxford, pp 125–152
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Ekström, P., Korf, H.W. Putative cholinergic elements in the photosensory pineal organ and retina of a teleost, Phoxinus phoxinus L. (Cyprinidae). Cell Tissue Res. 246, 321–329 (1986). https://doi.org/10.1007/BF00215894
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00215894