Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-08T14:28:38.539Z Has data issue: false hasContentIssue false

Synaptic circuitry of neuropeptide-containing amacrine cells in the retina of the cane toad, Bufo marinus

Published online by Cambridge University Press:  02 June 2009

Bao-Song Zhu
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia Adelaide, Australia
Ian Gibbins
Affiliation:
Department of Anatomy and Histology, School of Medicine, The Flinders University of South Australia Adelaide, Australia

Abstract

Synaptic connections of amacrine cells with substance P-like or neuropeptide Y-like immunoreactivity (SP-LI or NPY-LI) in the retina of the cane toad, Bufo marinus, were investigated using ultrastructural immunocytochemistry. The perikarya of SP-LI or NPY-LI amacrine cells were located in the innermost row of the inner nuclear layer. The synapses associated with SP-LI amacrine cells were distributed mainly in sublaminae 3 and 4 with about 10% in sublamina 1 of the inner plexiform layer. The synapses formed by NPY-LI amacrine cells were found in sublaminae 1, 2, and 4 with approximately equal frequency. Of a total of 175 SP-LI profiles, 56% were in presynaptic positions and 44% in postsynaptic positions. The synaptic inputs to SP-LI profiles predominantly derived from other unlabeled amacrine cell dendrites, and to a lesser extent, from bipolar cell terminals. The majority of synaptic outputs from SP-LI amacrine cell dendrites were directed onto unlabeled amacrine cell processes. The SP-LI profiles also made synapses onto bipolar cell terminals and formed synapses onto presumed ganglion cell dendrites. Of a total of 200 NPY-LI profiles, 48% were in presynaptic positions and 52% in postsynaptic positions. The profiles of NPY-LI amacrine cells mainly received their synaptic inputs from other unlabeled amacrine cell processes, and to a lesser extent, from bipolar cell terminals. The majority of NPY-LI amacrine cell profiles gave their synaptic outputs onto unlabeled amacrine cell dendrites, and others formed synapses onto presumed ganglion cell processes. These results suggest that these two populations of neuropeptide-containing amacrine cells in the Bufo retina are involved in different synaptic circuits.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ayoub, G.S. & Matthews, G. (1992). Substance P modulates calcium current in retinal bipolar neurons. Visual Neuroscience 8, 539544.CrossRefGoogle ScholarPubMed
Brecha, N.C., Eldred, W., Kuljis, R.O. & Karten, H.J. (1984). Identification and localization of biologically active peptides in the vertebrate retina. Progress in Retinal Research 3, 185226.CrossRefGoogle Scholar
Cuenca, N. & Kolb, H. (1989). Morphology and distribution of neurons immunoreactive for substance P in the turtle retina. Journal of Comparative Neurology 290, 391411.CrossRefGoogle ScholarPubMed
Dick, E. & Miller, R.F. (1981). Peptides influence retinal ganglion cells. Neuroscience Letters 26, 131135.CrossRefGoogle ScholarPubMed
Dowling, J.E., Ehinger, B. & FlorÉn, I. (1980). Fluorescence and electron microscopical observations on the amine-accumulating neurons of the Cebus monkey retina. Journal of Comparative Neurology 192, 665685.CrossRefGoogle ScholarPubMed
Downing, J.E. & Djamgoz, M.B. (1993). Electrophysiological effects of tachykinin analogues on ganglion cell activity in cyprinid fish retina. Neuropeptides 24, 109116.CrossRefGoogle ScholarPubMed
Ehinger, B. & Holmgren, I. (1979). Electron microscopy of the indoleamine-accumulating neurons in the retina of the rabbit. Cell and Tissue Research 197, 175194.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. & Kolb, H. (1976). Structural basis for ON- and OFF- center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle ScholarPubMed
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 12671269.CrossRefGoogle Scholar
Gábriel, R., Zhu, B.-S. & Straznicky, C. (1992). Synaptic contacts of tyrosine hydroxylase-immunoreactive elements in the inner plexi-form layer of the retina of Bufo marinus. Cell and Tissue Research 267, 525534.CrossRefGoogle Scholar
GÁbriel, R., Zhu, B.-S. & Straznicky, C. (1993). Synaptic contacts of serotonin-like immunoreactive and 5,7-dihydroxytryptamine-accumulating neurons in the anuran retina. Neuroscience 54, 11031114.CrossRefGoogle ScholarPubMed
Glickman, R.D., Adolph, A.R. & Dowling, J.E. (1982). Inner plexi-form circuits in the carp retina: Effects of cholinergic agonists, GABA, and substance P on the ganglion cells. Brain Research 234, 8199.CrossRefGoogle Scholar
Hiscock, J. & Straznicky, C. (1989a). Morphological characterization of substance P-like immunoreactive amacrine cells in the anuran retina. Vision Research 29, 298310.CrossRefGoogle ScholarPubMed
Hiscock, J. & Straznicky, C. (1989b). Neuropeptide Y-like immunoreactive amacrine cells in the retina of Bufo marinus. Brain Research 494, 5564.CrossRefGoogle ScholarPubMed
Hiscock, J. & Straznicky, C. (1991). Substance P-immunoreactive neurons in the retina of two lizards. Archives of Histology and Cytology 54, 321337.CrossRefGoogle ScholarPubMed
Holmgren-Taylor, I. (1982). Electron microscopical observation on the indoleamine-accumulating neurons and their synaptic connections in the retina of the cat. Journal of Comparative Neurology 208, 144156.CrossRefGoogle ScholarPubMed
Isayama, T. & Eldred, W.D. (1988). Neuropeptide Y-immunoreactive amacrine cells in the retina of the turtle Pseudemys scripta elegans. Journal of Comparative Neurology 271, 5666.CrossRefGoogle ScholarPubMed
Isayama, T., Polak, J. & Eldred, W.D. (1988). Synaptic analysis of amacrine cells with neuropeptide Y-like immunoreactivity in turtle retina. Journal of Comparative Neurology 275, 452459.CrossRefGoogle ScholarPubMed
Masland, R.H. (1988). Amacrine cells. Trends in Neuroscience 11, 405410.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1987). Transmitter circuits in the vertebrate retina. Progress in Neurobiology 28, 5596.CrossRefGoogle ScholarPubMed
Sandell, J.H., Masland, R.H., Raviola, E. & Dacheux, R.F. (1989). Connections of indoleamine-accumulating cells in the rabbit retina. Journal of Comparative Neurology 283, 303313.CrossRefGoogle ScholarPubMed
Stone, S. & SchÜtte, M. (1991). Physiological and morphological properties of OFF- and ON-center bipolar cells in the Xenopus retina: Effects of glycine and GABA. Visual Neuroscience 7, 363376.CrossRefGoogle ScholarPubMed
Straznicky, C. & Hiscock, J. (1994). Neuropeptide Y-immunoreactive neurons in the retina of two Australian lizards. Archives of Histology and Cytology 57, 151160.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative input from GABAergic amacrine cells. Visual Neuroscience 1, 297305.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1990). The mosaic of amacrine cells in the mammalian retina. Progress in Retinal Research 9, 49100.CrossRefGoogle Scholar
Weiler, R. (1981). The distribution of center-depolarizing and center-hyperpolarizing bipolar cell ramifications within the inner plexiform layer of turtle retina. Journal of Comparative Physiology 144, 459464.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M. & Zucker, C.L. (1985). Synaptic organization of substance P-like immunoreactive amacrine cells in goldfish retina. Journal of Comparative Neurology 231, 232238.CrossRefGoogle ScholarPubMed
Zalutsky, R.A. & Miller, R.F. (1990). The physiology of substance P in rabbit retina. Journal of Neuroscience 10, 394402.CrossRefGoogle ScholarPubMed
Zhu, B.-S. & Straznicky, C. (1990a). Dendritic morphology and retinal distribution of tyrosine hydroxylase-like immunoreactive amacrine cells in bufo marinus. Anatomy and Embryology 181, 365371.CrossRefGoogle ScholarPubMed
Zhu, B.-S. & Straznicky, C. (1990b). Morphology and distribution of serotonin-like immunoreactive amacrine cells in the retina of Bufo marinus. Visual Neuroscience 5, 371378.CrossRefGoogle ScholarPubMed
Zhu, B.-S., Gabriel, R. & Straznicky, C. (1992). Serotonin synthesis and accumulation by neurons of the anuran retina. Visual Neuroscience 9, 377388.CrossRefGoogle ScholarPubMed
Zhu, B.-S., Straznicky, C. & Gibbins, I. (1995). Synaptic circuitry of serotonin-synthesizing and serotonin-accumulating amacrine cells in the retina of the cane toad, Bufo marinus. Visual Neuroscience 12, 1119.CrossRefGoogle ScholarPubMed