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Amacrine cells with neurotensin- and somatostatin-like immunoreactivities in three species of teleosts with different color vision

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Summary

Neurotensin- and somatostatin-like immunoreactivities were localized by pre-embedding techniques in retinal whole-mounts and radial sections of a monochromatic glass catfish (Kryptopterus bicirrhis), a dichromatic cichlid species (Aequidens pulcher), and the tetrachromatic roach (Rutilus rutilus). Both neuropeptides were observed in perikarya and processes of amacrine cells. For a precise identification of cell types, tangential and radial views were correlated with Golgiimpregnated material.

The dendritic pattern defining the morphological subtype of amacrine cells was determined by the given neuropeptide or by the species-specific degree of complexity of retinal structure and function. Neurotensin-like immunoreactivity was localized in amacrine cells of intermediate size, radial symmetry and dendrites with numerous varicosities; they were monostratified in sublayer 3 of the inner plexiform layer. This cell type was common to all three species. In the mono and dichromatic retinas, a single type of amacrine cell with somatostatinlike immunoreactivity was found with radially oriented, varicose dendrites in sublayer 5. In the tetrachromatic roach retina, two somatostatin-positive amacrine cell types were found with very different patterns of ramification; furthermore, both of these types occurred in more than one sublayer.

Possible functional implications for color vision of neuropeptide-specific amacrine cells with uniform morphology in all three species and those with a more varied morphology in the tetrachromatic roach are discussed.

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References

  • Ammermüller J, Weiler R (1981) The ramification pattern of amacrine cells within the inner plexiform layer of the carp retina. Cell Tissue Res 220:699–723

    Google Scholar 

  • Avery JA, Bowmaker JK, Djamgoz MBA, Downing JEG (1982) Ultraviolet sensitive receptors in a freshwater fish. J Physiol 334:23–24

    Google Scholar 

  • Brazeau P (1985) Somatostatin: a peptide at the origin of many debates. In: Lewin MJM, Bonfils S (eds) Regulatory peptides in digestive, nervous and endocrine systems. INSERM Symp 25 Elsevier, Amsterdam, pp 257–264

    Google Scholar 

  • Brecha N (1983) Retinal neurotransmitter: Histochemical and biochemical studies. In: Emson PC (ed) Chemical neuroanatomy. Raven Press, New York, pp 85–129

    Google Scholar 

  • Brecha N, Karten HJ, Schenker C (1981) Neurotensin-like and somatostatin-like immunoreactivity within amacrine cells of the retina. Neuroscience 6:1329–1340

    Google Scholar 

  • Brown B, Rivier J, Vale W (1979) Somatostatin: central nervous system actions on glucoregulation. Endocrinology 104:1709–1715

    Google Scholar 

  • Cajal SR (1893) La rétine des vertébrés. Cellule 9:17–257

    Google Scholar 

  • Dick E, Miller RF (1981) Peptides influence retinal ganglion cells. Neurosci Lett 26:131–135

    Google Scholar 

  • Djamgoz MBA, Downing JEG (1983) A quantitative analysis of cone photoreceptor-horizontal cell connectivity patterns at ribbon synapses in a cyprinid (roach) retina. J Physiol (Lond) 341:75p

  • Djamgoz MBA, Downing JEG, Wagner H-J (1985) The cellular origin of an unusual type of Spotential: an intracellular horseradish peroxidase study in a cyprinid fish. J Neurocytol 14:469–486

    Google Scholar 

  • Djamgoz MBA, Wagner H-J (1986) Intracellular staining of retinal neurons: Applications to studies of functional organization. In: Osborne N, Chader J (eds) Progr Ret Res 4, Pergamon Press, New York

    Google Scholar 

  • Dodd J, Kelly JS (1978) Is Somatostatin an excitatory transmitter in the hippocampus? Nature 273:674–675

    Google Scholar 

  • Douglas R, Wagner H-J (1984) Action spectrum of photomechanical cone contraction in the catfish retina. Invest Ophthalmol Vis Sci 25:534–538

    Google Scholar 

  • Downing JEG (1983) Functionally identified interneurons in the vertebrate (fish) retina: electrophysiological, ultrastructural and pharmacological studies. Ph D Thesis. University of London

  • 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

    Google Scholar 

  • Eldred WD, Zucker C, Karten HJ, Yazulla S (1983) Comparison of fixation and penetration enhancement techniques for use in ultrastructural immunocytochemistry. J Histochem Cytochem 31:285–292

    Google Scholar 

  • Famiglietti EV (1985) Starburst amacrine cells: Morphological constancy and systematic variations in an anisotropic field of rabbit retinal neurons. J Neurosci 5:562–577

    Google Scholar 

  • Fukuda M, Kuwayama S, Shiosaka S, Inagaki S, Ishimoto I, Shimizu Y, Takagi H, Sakanaka M, Takatsuki K, Senba E, Tohyama M (1981) Localization of vasoactive intestinal polypeptide and neurotensin immunoreactivity in the avian retina. Curr Eye Res 1:115–118

    Google Scholar 

  • Hashimoto Y, Kato A, Inokuchi M, Watanabe K (1976) Reexamination of horizontal cells in the carp with procion yellow electrode. Vision Res 16:25–29

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of avidin-biotin-peroxidase complex in immunperoxidase techniques. J Histochem Cytochem 29:577–580

    CAS  PubMed  Google Scholar 

  • loffe S, Havlicek V, Friesen H, Chernick V (1978) Effect of somatostatin (SRIF) and L-glutamate on neurons of the sensimotor cortex in awake habituated rabbits. Brain Res 153:414–418

    Google Scholar 

  • Ishimoto I, Millar T, Chubb IW, Morgan IG (1986) Somatostatin-immunoreactive amacrine cells of chicken retina: retinal mosa ic, ultrastructural features, and light-driven variations in peptide metabolism. Neuroscience 17:1217–1233

    Google Scholar 

  • Iversen LL, Nicoll RA, Vale WW (1978) Neurobiology of peptides. Neurosci Res Program Bull 16:211–370

    Google Scholar 

  • Kaneko A (1973) Receptive field organization of bipolar and amacrine cells in the goldfish retina. J Physiol (Lond) 235:133–153

    Google Scholar 

  • Kolb H, Nelson R (1984) Neural architecture in the cat retina. In: Osborne N, Chader J (eds) Progr Ret Res 3 Pergamon Press, New York, pp 21–60

    Google Scholar 

  • Krisch B, Leonhardt H (1979) Demonstration of a somatostatinlike activity in retinal cells of the rat. Cell Tissue Res 204:127–140

    Google Scholar 

  • Levine JS, MacNichol EF (1979) Visual pigments in teleost fishes: effects of habitat, microhabitat and behaviour on visual system evolution. Sensory Prog 3:95–131

    Google Scholar 

  • Li H-B, Watt CB, Lam DM-K (1985) The coexistence of two neuroactive peptides in a subpopulation of retinal amacrine cells. Brain Res 345:176–180

    Google Scholar 

  • Lin C-T, Li H-Z, Wu JY (1983) Immunocytochemical localization of L-glutamate decarboxylase, gamma-aminobutyric acid trans-aminase, cysteine sulfinic acid decarboxylase, aspartate amino-transferase and somatostatin in rat retina. Brain Res 270:273–283

    Google Scholar 

  • Marshak DW (1986) Synapses of peptide immunoreactive neurons in macaque retina. Invest Ophthalmol Vis Sci 27:331

    Google Scholar 

  • Marshak DW, Yamada T, Stell WK (1984) Synaptic contacts of somatostat-inimmunoreactive amacrine cells in goldfish retina. J Comp Neurol 225:44–52

    Google Scholar 

  • Masland RH, Tauchi M (1986) The cholinergic amacrine cell. TINS 9:218–223

    Google Scholar 

  • Miller RF (1979) The neuronal basis of ganglioncell receptive-field organization and physiology of amacrine cells. In: Schmitt FO, Worden FG (eds) The neurosciences. MIT Press pp 227–244

  • Naka K, Carraway NRG (1975) Morphological and functional identification of catfish retinal neurons. I. Classical morphology. J Neurophysiol 38:53–71

    Google Scholar 

  • Pickel VM (1981) Immunocytochemical methods. In: Heimer L, Robards MJ (eds) Neuroanatomical tracttracing methods. Plenum Press, New York London:483–510

    Google Scholar 

  • Rodieck RW (1986) Starburst amacrine cells of the primate retina. Invest Ophthalmol Vis Sci 27:331

    Google Scholar 

  • Sagar SM, Marshall PE, Landis DMD (1985) Immunoreactive somatostatin in the rat retina: light microscopic immunocyto chemistry and Chromatographic characterization. Brain Res 336:235–242

    Google Scholar 

  • Sagar SM, Marshall PE, Onesti ST, Landis DMD (1986) Somatostatin immunocytochemistry in the rabbit retina. Invest Ophthalmol Vis Sci 27:316–322

    Google Scholar 

  • Smiley JF, Basinger SF (1986) Somatostatin immunoreactivity in the Xenopus laevis retina is found in the glycinergic interplexiform cell. Invest Ophthalmol Vis Sci 27:184

    Google Scholar 

  • Spira AW, Shimizu Y, Rorstad OP (1984) Localization, Chromatographic characterization, and development of somatostatin-like immunoreactivity in the guinea pig retina. J Ncurosci 3069:3079

    Google Scholar 

  • Stell WK (1984) Putative peptide transmitters, amacrine cell diversity and function in the inner plexiform layer. In: Gallego A, Gouras P (eds) Neurocircuitry of the retina. A Cajal Memorial. Elsevier, Amsterdam

    Google Scholar 

  • Stell WK, Lightfoot DO (1975) Colour specific interconnections of cones and horizontal cells in the retina of the goldfish. J Comp Neurol 159:473–502

    Google Scholar 

  • Wagner E, Wagner H-J, Djamgoz MBA (1987) Amakrine Zelltypen der Plötzenretina: Klassifizierung und Korrelation von Golgiimprägnierten und HRP-injizierten Zellen. Verh Anat Ges (in press)

  • Weiler R (1978) Horizontal cells of the carp retina: Golgi impreg nation and procionyellow injection. Cell Tissue Res 195:515–526

    Google Scholar 

  • Weiler R, Ball AK (1984) Colocalization of neurotensinlike immunoreactivity and Hglycine uptake system in sustained amacrine cells of the turtle retina. Nature 311:759–761

    Google Scholar 

  • Werblin FS (1970) Responses of retinal cells to moving spots: intra cellular recording in Necturux maculosus. J Neurophysiol 33:342–350

    Google Scholar 

  • Yamada T, Marshak D, Basinger S, Walsh J, Morley J, Stell WK (1980) Somatostatin-like immunoreactivity in the retina. Proc Natl Acad Sci USA 77:1691–1695

    Google Scholar 

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Dedicated to Prof. A. Oksche on the occasion of his 60th birthday

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Wagner, H.J., Zeutzius, I. Amacrine cells with neurotensin- and somatostatin-like immunoreactivities in three species of teleosts with different color vision. Cell Tissue Res. 248, 663–673 (1987). https://doi.org/10.1007/BF00216497

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