Summary
Using immunocytochemical methods, we have been able to demonstrate serotonin-like immunoreactivity (SLI) in amacrine and bipolar cells of the turtle retina. Inhibition of monoamine oxidase with pargyline drastically increases the amount of 5-hydroxytryptamine within both cell types. The indoleamine 6-hydroxytryptamine is taken up by both cell types and both types are destroyed within 10 days following intraocular injection of 5,7-dihydroxyryptamine. Increasing the external potassium concentration induces release of serotonin in both cell types. Our data support the idea that these neurons use serotonin during neuronal processing. Morphologically, amacrine and bipolar cells with SLI can be subdivided into two and three subclasses, respectively, based on their ramification pattern within the inner plexiform layer. A comparison of the morphological data with those of intracellularly stained amacrine and bipolar cells suggests that all bipolar cells with SLI are center-hyperpolarizing cells and all amacrine cells center-depolarizing cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aghajanian GK, Wang RY (1978) Physiology and pharmacology of central serotonergic neurons. In: Lipton ME, Killam KF, DiMascio A (eds) Psychopharmacology — A generation of progress. Raven, New York
Barker PC, Quay WB (1969) 5-Hydroxytryptamine metabolism in early embryogenesis and the development of brain and retinal tissues. Brain Res 12:273–295
Baumgarten HG, Björklund A (1976) Neurotoxic indoleamines and monoamine neurons. Ann Rev Pharmacol Toxicol 16:101–107
Baumgarten HG, Klemm HP, Schlossberger HG (1984) In vivo metabolism of 14C-5-HT, 14C-5,6-DHT and 14C-5,7-DHT by MAO/COMT/Aldehyde dehydrogenase in rat brain. In: Schlossberger HG, Kochen W, Linzen B, Steihart H (eds) Progress in tryptophan and serotonin research. W. de Gruyter, Berlin, New York, pp 241–249
Björklund A, Baumgarten HG, Nobin A (1974) Chemical lesioning of central monoamine axons by means of 5,6-dihydroxytryptamine and 5,7-dihydroxytryptamine. Adv Biochem Psychopharmacol 10:13–33
Brown KT (1969) A linear area centralis extending across the turtle retina and stabilized to the horizon by non visual cues. Vision Res 9:1053–1062
Bruun A, Ehinger B, Sytsma VM (1984) Neurotransmitter localisation in the skate retina. Brain Res 295:233–248
Cajal SRy (1882) La rétine des vertèbres. Cellule 9:121–146
Cawthon RM, Breakefield XO (1979) Differences in A and B forms of monoamine oxidase (MAO) revealed by limited proteolysis and peptide mapping. Nature 281:692–694
Ehinger B, Floren I (1976) Indoleamine-accumulating neurons in the retina of rabbit, cat and goldfish. Cell Tissue Res 175:37–48
Ehinger B, Floren I (1978) Chemical removal of indoleamine-accumulating terminals in rabbit and goldfish retina. Exp Eye Res 26:321–327
Ehinger B, Floren I (1980) Retinal indoleamine-accumulating neurons Neurochemistry 1:209
Eldred WD, Karten HJ (1983) Characterization and quantification of peptidergic amacrine cells in the turtle retina: Enkephalin, neurotensin and glucagon. J Comp Neurol 221:371–381
Famiglietti EV, Kaneko A, Tachibana M (1977) Neuronal architecture of ON and OFF pathways to ganglion cells in carp. Science 189:1267–1269
Hauschild DC, Laties AM (1973) An indoleamine containing cell in chick retina. Invest Opthalmol 12:537–540
Kaneko A (1970) Physiological and morphological identification of horizontal, bipolar, amacrine cells in goldfish retina. J Physiol 207:623–633
Kolb H (1982) The morphology of the bipolar cells, amacrine cells and ganglion cells in the retina of the turtle Pseudemys scripta elegans. Phil Trans R Soc Lond 298:355–393
Marc RE (1982) Spatial organization of neurochemically classified interneurons of the goldfish retina. I. Local patterns. Vision Res 22:589–602
Marchiafava PL, Torre V (1978) The responses of amacrine cells to light and intracellularly applied currents. J Physiol Lond 276:83–102
Marchiafava PL, Weiler R (1980) Intracellular analysis and structural correlates of the organization of inputs to ganglion cells in the retina of the turtle. Proc R Soc Lond 208:103–113
Marchiafava PL, Weiler R (1982) The photoresponses of structurally identified amacrine cells in the turtle retina. Proc R Soc Lond 214:403–415
Negishi K, Teranishi T, Kalto S (1981) Similarity in spatial distribution between dopaminergic cells and indoleamine accumulating-cells of carp retina. Acta Histochem Cytochem 14:449–460
Negishi K, Teranishi T, Kato S (1981) 5,7-Dihydroxytryptamine destroys indoleamine-accumulating cell bodies in carp retina. Acta Histochem Cytochem 14:654–660
Nelson R, Famiglietti EV, Kolb H (1978) Intracellular staining reveals different levels of stratification for ON and OFF center ganglion cells in cat retina. J Neurophysiol 41:472–483
Osborne NN (ed) (1982) Biology of serotonergic transmission. John Wiley & Sons Ltd, Sussex
Osborne NN, Patel S (1984) Postnatal development of serotonin accumulating neurones in the rabbit retina and an immunohisto-chemical analysis of the uptake and release of serotonin. Exp Eye Res 38:611–620
Osborne NN, Nesselhut T, Nicholas DA, Patel S, Cuello AC (1982) Serotonin containing neurones in vertebrate retinas. J Neurochem 39:1519–1528
Quay WB (1965) Indole derivates of pineal and related neural and retinal tissues. Pharmacol Rev 17:321–345
Quay WB (1965) Retinal and pineal hydroxyindole-O-methyl transferase activity in vertebrates. Life Sci 4:983–991
Schwartz EA (1974) Responses of bipolar cells in the retina of the turtle. J Physiol 236:211–224
Steinbusch HWM, Verhofstad AAJ, Joosten HWJ (1978) Localisation of serotonin in the central nervous system by immunohistochemistry: Description of a specific and sensitive technique and some applications. Neuroscience 3:811–819
Suzuki E, Noguchi E, Miyake S, Yagi K (1977) Occurrence of 5-hydroxytryptamine in chick retina. Experientia 33:927
Tornqvist K, Hansson CH, Ehinger B (1983) Immunohistochemical and quantitative analysis of 5-hydroxytryptamine in the retina of some vertebrates. Neurochem Int 5:299–308
Weiler R (1981) The distribution of center-depolarizing and centerhyperpolarizing bipolar cell ramifications within the inner plexiform layer of turtle retina. J Comp Physiol 144:459–464
Weiler R, Ball AK (1984) Colocalisation of neurotensin-like immunoreactivity and 3H-glycine uptake system in sustained amacrine cells of turtle retina. Nature 311:759–761
Weiler R, Marchiafava PL (1981) Physiological and morphological study of the inner plexyform layer in the turtle retina. Vision Res 21:1635–1638
Welsh JH (1964) The quantitative distribution of 5-hydroxytryptamine in the nervous system, eyes and other organs of some vertebrates. In: Comparative Neurochemistry, Proceedings of the 5th International Neurochemistry Symposium. Pergamon Press, Oxford, pp 355–366
Werblin FS, Dowling JE (1969) Organisation of the retina of the mudpuppy Necturus maculosus. II. Intracellular recording. J Neurophysiol 32:737–744
Witkovsky P, Eldred W, Karten HJ (1984) Catecholamineand indoleamine-containing neurons in the turtle retina. J Comp Neurol 228:217–225
Author information
Authors and Affiliations
Additional information
This work was supported by the Deutsche Forschungsgemeinschaft, Sonderforschungsbereich 220
Rights and permissions
About this article
Cite this article
Weiler, R., Schütte, M. Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle, Pseudemys scripta elegans . Cell Tissue Res. 241, 373–382 (1985). https://doi.org/10.1007/BF00217183
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00217183