Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-25T04:55:14.187Z Has data issue: false hasContentIssue false

Bipolar cells in the “grouped retina” of the elephantnose fish (Gnathonemus petersii)

Published online by Cambridge University Press:  06 September 2007

HANS-JOACHIM WAGNER
Affiliation:
Anatomisches Institut, Graduate School of Neural & Behavioural Sciences and International Max-Planck-Research School, Universität Tübingen, Germany

Abstract

To elucidate the specific properties of retinae with grouped photoreceptors the neural pathways in the outer and inner plexiform layer were studied. Photoreceptor bundles in this species consist of more than 100 rods and up to 50 cones, and are usually regarded as functional units. Golgi impregnation in thick and thin sections and light microscopy were used to identify bipolar cell types linking photoreceptors to amacrine and/or ganglion cells. Nine different types were distinguished based on their dendritic morphology and the position of the axon terminal in the inner plexiform layer. Small cells have dendritic fields smaller than the diameter of a photoreceptor bundle and are contacted mostly by cones. The dendritic field size of bushy cells matches that of a photoreceptor bundle; they are contacted mainly by rods. Flat cells receive about equal input from rods and cones; their dendritic field size exceeds the bundle diameter. Within the three major classes there are subtypes addressing three sublaminae of the inner plexiform layer, the proximal On-centre region (sl b), the distal Off-centre region (sl a) and a central sublayer (sl c) probably with transient activity. These observations suggest that cone vision has a spatial acuity better than the “bundle grain”. In rod dominated vision the resolution matches that of the bundles; for this pathway, the hypothesis of the bundle as a functional unit is confirmed. The mesopic flat cell pathway has a resolution inferior to the “bundle grain”; it may therefore be dedicated to movement detection.

Type
Research Article
Copyright
© 2007 Cambridge University Press

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

Best, A.C.G. & Nicol, J.A.C. (1979). On the eye of the goldeye Hiodon alosoides. (Teleostei, Hiodontidae). Journal of Zoology (London) 188, 309332.Google Scholar
Ciali, S. (1988). Spectral sensitivity and retinal anatomy of the weakly electric fish, Gnathonemus petersii. PhD thesis, p. 170. New York: The City University of New York.
Collin, S.P., Hoskins, R.V. & Partridge, J.C. (1998). Seven retinal specializations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: A case study in visual optimization. Brain Behavior and Evolution 51, 291314.CrossRefGoogle Scholar
Connaughton, V.P., Graham, D. & Nelson, R. (2004). Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. Journal of Comparative Neurology 477, 371385.CrossRefGoogle Scholar
Douglas, R.H. & Wagner, H.-J. (1984). Action spectrum of photomechanical cone contraction in the catfish retina. Investigative Ophthalmology and Visual Science 25, 534538.Google Scholar
Famiglietti, E.V., Jr. & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193195.CrossRefGoogle Scholar
Famiglietti, E.V., Jr., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of On and Off pathways to ganglion cells in carp retina. Science 198, 12671269.CrossRefGoogle Scholar
Hawryshyn, C.W. & McFarland, W.L. (1987). Cone photoreceptor mechanisms and the detection of polarized light in fish. Journal of Comparative Physiology 160, 459465.CrossRefGoogle Scholar
Heiligenberg, W. (1991). Neural Nets In Electric Fish. Cambridge, MA: MIT Press.
Hirt, B. & Wagner, H.-J. (2005). The organization of the inner retina in a pure-rod deep-sea fish. Brain Behaviour Evolution 65, 157167.CrossRefGoogle Scholar
Land, M.F. & Nilsson, D.E. (2001). Animal Eyes. Oxford, UK: Oxford University Press.
Locket, N.A. (1977). Adaptations to the deep-sea environment. In Handbook of Sensory Physiology, ed. Crescitelli, F., pp. 67193. Berlin. Heidelberg: Springer-Verlag.CrossRef
Marc, R.E. (1999). The structure of vertebrate retinas. In The Retinal Basis of Vision, eds. Toyoda, J-I., Murakami, M., Kaneko, A. & Saito, T., pp. 322. Amsterdam: Elsevier.
Masland, R.H. (2001a). Neuronal diversity in the retina. Current Opinion in Neurobiology 11, 431436.Google Scholar
Masland, R.H. (2001b). The fundamental plan of the retina. Nature Neuroscience 4, 877886.Google Scholar
McEwan, M.R. (1938). A comparison of the retina of the mormyrids with that of various other teleosts. Acta Zoologica 19, 427465.CrossRefGoogle Scholar
Munk, O. (1975). On the eyes of two foveate notosudid teleosts, Scopelosuarus hoedti and Ahliesaurus berryi. Videnskabelige Meddelellser Dansk Naturhistorisk Forening 138, 87125.Google Scholar
Naka, K.-I. & Ohtsuka, T. (1975). Morphological and functional identifications of catfish retinal neurons. II. Morphological identification. Journal of Neurophysiology 38, 7291.Google Scholar
Richardson, K.C., Jarett, L. & Finke, E.H. (1960). Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technology 35, 313323.CrossRefGoogle Scholar
Rodieck, R.W. (1998). The First Steps In Seeing. Sunderland MA: Sinauer Assoc.
Scholes, J.H. (1975). Colour receptors and their synaptic connexions, in the retina of a cyprinid fish. Philosophical Transactions of the Royal Society B 270, 61118.CrossRefGoogle Scholar
Sherry, D. & Yazulla, S. (1993). Goldfish BCs and axon terminal patterns: A Golgi study. Journal of Comparative Neurology 329, 188200.CrossRefGoogle Scholar
Stell, W.K. (1965). Correlation of retinal cytoarchitecture and ultrastructure in Golgi preparations. Anatomical Record 153, 389398.CrossRefGoogle Scholar
Stell, W.K. (1967). The structure and relationships of horizontal cells and photoreceptor bipolar synaptic complexes in goldfish retina. American Journal of Anatomy 120, 401424.CrossRefGoogle Scholar
Stell, W.K., Ishida, A.T. & Lightfoot, D.O. (1977). Structural basis for on- and off-center responses in retinal BCs. Science 198, 12691271.CrossRefGoogle Scholar
Wagner, H.-J. & Ali, M.A. (1978). Retinal organization in goldeye and mooneye. Revue Canadienne de Biologie 37, 6584.Google Scholar
Wässle, H., Grünert, U. & Martin, P.R. (1994). Immunocytochemical characterization and spatial distribution of midget bipolar cells in the macaque monkey retina. Vision Research 34, 561579CrossRefGoogle Scholar
Wu, S.M., Gao, F. & Maple, B.R. (2000). Functional architecture of synapses in the inner retina: Segregation of visual signals by stratification of bipolar cell axon terminals. Journal of Neuroscience 20, 44624470.Google Scholar