Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T17:10:53.484Z Has data issue: false hasContentIssue false
  • English
  • Français

Tracer coupling between fish rod horizontal cells: Modulation by light and dopamine but not the retinal circadian clock

Published online by Cambridge University Press:  20 July 2007

CHRISTOPHE RIBELAYGA  and
STUART C. MANGEL
CHRISTOPHE RIBELAYGA
Affiliation:
Department of Neuroscience, The Ohio State University College of Medicine, Columbus, Ohio
STUART C. MANGEL
Affiliation:
Department of Neuroscience, The Ohio State University College of Medicine, Columbus, Ohio
Get access Rights & Permissions [Opens in a new window]

Abstract

Horizontal cells are second order neurons that receive direct synaptic input from photoreceptors. In teleosts horizontal cells can be divided into two categories, cone-connected and rod-connected. Although the anatomy and physiology of fish cone horizontal cells have been extensively investigated, less is known about rod horizontal cells. This study was undertaken to determine whether light and/or the circadian clock regulate gap junctional coupling between goldfish rod horizontal cells. We used fine-tipped, microelectrode intracellular recording to monitor rod horizontal cells under various visual stimulation conditions, and tracer (biocytin) iontophoresis to visualize their morphology and evaluate the extent of coupling. Under dark-adapted conditions, rod horizontal cells were extensively coupled to cells of like-type (homologous coupling) with an average of ∼120 cells coupled. Under these conditions, no differences were observed between day, night, the subjective day, and subjective night. In addition, under dark-adapted conditions, application of the dopamine D2-like agonist quinpirole (1 μM), the D2-like antagonist spiperone (10 μM), or the D1-like antagonist SCH23390 (10 μM) had no effect on rod horizontal cell tracer coupling. In contrast, the extent of tracer coupling was reduced by ∼90% following repetitive light (photopic range) stimulation of the retina or application of the D1-agonist SKF38393 (10 μM) during the subjective day and night. We conclude that similarly to cone horizontal cells, rod horizontal cells are extensively coupled to one another in darkness and that the extent of coupling is dramatically reduced by bright light stimulation or dopamine D1-receptor activation. However, in contrast to cone horizontal cells whose light responses are under the control of the retinal clock, the light responses of rod horizontal cells under dark-adapted conditions were similar during the day, night, subjective day, and subjective night thus demonstrating that they are not under the influence of the circadian clock.

Keywords

Gap junctionsHorizontal cellsDopamine receptorsCircadian rhythmRod pathway
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 333 - 344
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

Adachi, A., Suzuki, Y., Nogi, T. & Ebihara, S. (1999). The relationship between ocular melatonin and dopamine rhythms in the pigeon: Effects of melatonin inhibition on dopamine release. Brain Research 815, 435–440.CrossRefGoogle Scholar
Baldridge, W.H. & Ball, A.K. (1991). Background illumination reduces horizontal cell receptive-field size in both normal and 6-hydroxydopamine-lesioned goldfish retinas. Visual Neuroscience 7, 441–450.CrossRefGoogle Scholar
Baldridge, W.H., Weiler, R. & Dowling, J.E. (1995). Dark-suppression and light sensitization of horizontal cell responses in the hybrid bass retina. Visual Neuroscience 12, 611–620.CrossRefGoogle Scholar
Burnside, B. (2001). Light and circadian regulation of retinomotor movement. Progress in Brain Research 131, 477–485.CrossRefGoogle Scholar
Cahill, G.M. & Besharse, J.C. (1995). Circadian rhythmicity in vertebrate retinas: Regulation by a photoreceptor oscillator. Progress in Retinal and Eye Research 14, 267–291.CrossRefGoogle Scholar
De Juan, J. & Garcia, M. (2001). Spinules and nematosomes in retinal horizontal cells: A “thorny” issue. Progress in Brain Research 131, 519–537.CrossRefGoogle Scholar
DeVries, S.H. & Schwartz, E.A. (1989). Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. Journal of Physiology (London) 414, 351–375.CrossRefGoogle Scholar
Dowling, J.E. & Ehinger, B. (1978). The interplexiform cell system. I. Synapses of the dopaminergic neurones of the goldfish retina. Proceedings of the Royal Society of London B 201, 7–26.Google Scholar
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge: Harvard University Press.
Dowling, J.E. (1991). Retinal neuromodulation: The role of dopamine. Visual Neuroscience 7, 87–97.CrossRefGoogle Scholar
Downing, J.E. & Djamgoz, M.B. (1989). Quantitative analysis of cone photoreceptor-horizontal cell connectivity patterns in the retina of a cyprinid fish: Electron microscopy of functionally identified and HRP-labelled horizontal cells. Journal of Comparative Neurology 289, 537–553.CrossRefGoogle Scholar
Green, C.B. & Besharse, J.C. (2004). Retinal circadian clocks and control of retinal physiology. Journal of Biological Rhythms 19, 91–102.CrossRefGoogle Scholar
Harsanyi, K. & Mangel, S.C. (1992). Activation of a D2 receptor increases electrical coupling between retinal horizontal cells by inhibiting dopamine release. Proceedings of the National Academy of Sciences USA 89, 9220–9224.CrossRefGoogle Scholar
Iuvone, M.P. (1995). Cell biology and metabolic activity of photoreceptor cells: Light-evoked and circadian regulation. In Neurobiology and Clinical Aspects of the Outer Retina, eds. Djamgoz, M.B.A., Archer, S.N. & Vallerga, S., pp. 25–55. London, England: Chapman & Hall.CrossRef
Iuvone, P.M., Tosini, G., Pozdeyev, N., Haque, R., Klein, D.C. & Chaurassia, S.S. (2005). Circadian clocks, clock networks, arylalkylamine N-acetyltransferase, and melatonin in the retina. Progress in Retinal and Eye Research 24, 433–456.CrossRefGoogle Scholar
Kaneko, A. & Yamada, M. (1972). S-potentials in the dark-adapted retina of the carp. Journal of Physiology (London) 227, 261–273.CrossRefGoogle Scholar
Knapp, A.G. & Dowling, J.E. (1987). Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325, 437–439.CrossRefGoogle Scholar
Kolbinger, W., Kohler, K., Oetting, H. & Weiler, R. (1990). Endogenous dopamine and cyclic events in the fish retina, I: HPLC assay of total content, release, and metabolic turnover during different light/dark cycles. Visual Neuroscience 5, 143–149.CrossRefGoogle Scholar
Lasater, E.M. (1987). Retinal horizontal cell gap junctional conductance is modulated by dopamine through a cyclic AMP-dependent protein kinase. Proceedings of the National Academy of Sciences USA 84, 7319–7323.CrossRefGoogle Scholar
Malchow, R.P. & Yazulla, S. (1988). Light adaptation of rod and cone luminosity horizontal cells of the retina of the goldfish. Brain Research 443, 222–230.CrossRefGoogle Scholar
Mangel, S.C. & Dowling, J.E. (1987). The interplexiform-horizontal cell system of the fish retina: Effects of dopamine, light stimulation and time in the dark. Proceedings of the Royal Society of London. Series B, Biological Sciences 231, 91–121.CrossRefGoogle Scholar
Mangel, S.C. (2001). Circadian clock regulation of neuronal light responses in the vertebrate retina. Progress in Brain Research 131, 505–518.CrossRefGoogle Scholar
Manglapus, M.K., Iuvone, P.M., Underwood, H., Pierce, M.E. & Barlow, R.B. (1999). Dopamine mediates circadian rhythms of rod-cone dominance in the Japanese quail retina. Journal of Neuroscience 19, 4132–4141.Google Scholar
Massey, S.C., O'Brien, J.J., Trexler, E.B., Li, W., Keung, J.W., Mills, S.L. & O'Brien, J. (2003). Multiple neuronal connexins in the mammalian retina. Cell Communication and Adhesion 10, 425–430.CrossRefGoogle Scholar
McMahon, D.G., Zhang, D.Q., Ponomareva, L. & Wagner, T. (2001). Synaptic mechanisms of network adaptation in horizontal cells. Progress in Brain Research 131, 419–436.CrossRefGoogle Scholar
Missale, C., Nash, S.R., Robinson, S.W., Jaber, M. & Caron, M.G. (1998). Dopamine receptors: From structure to function. Physiological Reviews 78, 189–225.Google Scholar
Mora-Ferrer, C., Yazulla, S., Studholme, K.M. & Haak-Frendscho, M. (1999). Dopamine D1-receptor immunolocalization in goldfish retina. Journal of Comparative Neurology 411, 705–714.3.0.CO;2-Y>CrossRefGoogle Scholar
Murakami, M., Miyachi, E.I. & Takahashi, K.I. (1995). Modulation of gap junctions between horizontal cells by second messengers. Progress in Retinal and Eye Research 14, 197–221.CrossRefGoogle Scholar
Naka, K.I. & Rushton, W.A.H. (1967). The generation and spread of S-potentials in fish (Cyprinidae). Journal of Physiology (London) 192, 437–461.CrossRefGoogle Scholar
Pittendrigh, C.S. (1981). Circadian systems: General Perspective. In Handbook of Behavioral Neurobiology. Biological Rhythms Volume 4, ed. Aschoff, J., pp. 57–80. New York: Plenum Press.CrossRef
Ribelayga, C., Wang, Y. & Mangel, S.C. (2002). Dopamine mediates circadian clock regulation of rod and cone input to fish horizontal cells. Journal of Physiology (London) 544, 801–816.CrossRefGoogle Scholar
Ribelayga, C. & Mangel, S.C. (2003). Absence of circadian variation in gap-junctional coupling of cone horizontal cells reveals two dopamine systems in goldfish retina. Journal of Comparative Neurology 467, 243–253.CrossRefGoogle Scholar
Ribelayga, C., Wang, Y. & Mangel, S.C. (2004). A circadian clock in the fish retina regulates dopamine release via activation of melatonin receptors. Journal of Physiology (London) 554, 467–482.CrossRefGoogle Scholar
Schorderet, M. & Nowak, J.Z. (1990). Retinal dopamine D1 and D2 receptors: Characterization by binding or pharmacological studies and physiological functions. Cell and Molecular Neurobiology 10, 303–325.CrossRefGoogle Scholar
Stell, W.K. & Lightfoot, D.O. (1975). Colour-specific interconnections of cones and horizontal cells in the retina of the goldfish. Journal of Comparative Neurology 159, 473–501.CrossRefGoogle Scholar
Stell, W.K. & Harosi, F.I. (1976). Cone structure and visual pigment in the retina of the goldfish. Vision Research 16, 647–657.CrossRefGoogle Scholar
Teranishi, T. & Negishi, K. (1994). Double-staining of horizontal and amacrine cells by intracellular injection with Lucifer yellow and biocytin in carp retina. Neuroscience 59, 217–226.CrossRefGoogle Scholar
Tsukamoto, Y., Yamada, M. & Kaneko, A. (1987). Morphological and physiological studies of rod-driven horizontal cells with special reference to the question of whether they have axons and axon terminals. Journal of Comparative Neurology 255, 305–316.CrossRefGoogle Scholar
Vaney, D.I. (1991). Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neuroscience Letters 125, 187–190.CrossRefGoogle Scholar
Vaquero, C.F., Pignatelli, A., Partida, G.J. & Ishida, A.T. (2001). A dopamine- and protein kinase A-dependent mechanism for network adaptation in retinal ganglion cells. Journal of Neuroscience 21, 8624–8635.Google Scholar
Villa, P., Bedmar, M.D. & Baron, M. (1991). Studies on rod horizontal cell S-potential in dependence of the dark/light adapted state: A comparative study in Cyprinus carpio and Scyliorhinus canicula retinas. Vision Research 31, 425–435.CrossRefGoogle Scholar
Wang, Y. & Mangel, S.C. (1996). A circadian clock regulates rod and cone input to fish retinal cone horizontal cells. Proceedings of the National Academy of Sciences USA 93, 4655–4660.CrossRefGoogle Scholar
Wang, Y., Harsanyi, K. & Mangel, S.C. (1997). Endogenous activation of dopamine D2 receptors regulates dopamine release in the fish retina. Journal of Neurophysiology 78, 439–449.Google Scholar
Witkovsky, P. (2004). Dopamine and retinal function. Documenta Ophthalmologica 108, 17–40.CrossRefGoogle Scholar
Xin, D. & Bloomfield, S.A. (1999). Dark- and light-induced changes in coupling between horizontal cells in mammalian retina. Journal of Comparative Neurology 405, 75–87.3.0.CO;2-D>CrossRefGoogle Scholar
Yagi, T. (1986). Interactions between the soma and the axon terminal of retinal horizontal cells in Cyprinus carpio. Journal of Physiology (London) 375, 121–135.CrossRefGoogle Scholar
Yamada, M., Shigematsu, Y., Umetani, Y. & Saito, T. (1992). Dopamine decreases receptive field size of rod-driven horizontal cells in carp retina. Vision Research 32, 1801–1807.CrossRefGoogle Scholar
Yazulla, S. & Lin, Z.S. (1995). Differential effects of dopamine depletion on the distribution of 3H-SCH23390 and 3H-spiperone binding sites in the goldfish retina. Vision Research 17, 2409–2414.CrossRefGoogle Scholar