Abstract
In the retinas of many species of lower vertebrates, retinal photoreceptors and pigment epithelium pigment granules undergo daily movements in response to both diurnal, and in the case of teleost cone photoreceptors, endogenous circadian signals. Typically, these cone movements take place at dawn and at dusk when teleosts are maintained on a cyclic light (LD) regime, and at expected dawn and expected dusk when animals are maintained in continuous darkness (DD). Because these movements are so strictly controlled, they provide an overt indicator of the stage of the underlying clock mechanism. In this study we report that both light-induced and circadian-driven cone myoid movements in the Midas cichlid (Cichlasoma citrinellum), occur normally in vitro. Many of the features of retinomotor movements found in vivo also occur in our culture conditions, including responses to light and circadian stimuli and dopamine. Circadian induced predawn contraction and maintenance of expected day position in response to circadian modulation, are also normal. Our studies suggest that circadian regulation of cone myoid movement in vitro is mediated locally by dopamine, acting via a D2 receptor. Cone myoid contraction can be induced at midnight and expected mid-day by dark culture with dopamine or the D2 receptor agonist LY171555. Further, circadian induced predawn contraction can be increased with either dopamine or LY171555, or may be reversed with the dopamine D2 antagonist, sulpiride. Sulpiride will also induce cone myoid elongation in retinal cultures at expected mid- day, but will not induce cone myoid elongation at dusk. In contrast, circadian cone myoid movements in vitro were unaffected by the D1 receptor agonist SCH23390, or the D1 receptor antagonist SKF38393. Our short-term culture experiments indicate that circadian regulation of immediate cone myoid movement does not require humoral control but is regulated locally within the retina. The inclusion of dopamine, or dopamine receptor agonists and antagonists in our cultures, has indicated that retinal circadian regulation may be mediated by endogenously produced dopamine, which acts via a D2 mechanism.
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Selected References
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- Besharse J. C., Iuvone P. M. Is dopamine a light-adaptive or a dark-adaptive modulator in retina? Neurochem Int. 1992 Feb;20(2):193–199. doi: 10.1016/0197-0186(92)90167-p. [DOI] [PubMed] [Google Scholar]
- Boatright J. H., Hoel M. J., Iuvone P. M. Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Res. 1989 Mar 13;482(1):164–168. doi: 10.1016/0006-8993(89)90555-6. [DOI] [PubMed] [Google Scholar]
- Brainard G. C., Morgan W. W. Light-induced stimulation of retinal dopamine: a dose-response relationship. Brain Res. 1987 Oct 20;424(1):199–203. doi: 10.1016/0006-8993(87)91211-x. [DOI] [PubMed] [Google Scholar]
- Cahill G. M., Besharse J. C. Light-sensitive melatonin synthesis by Xenopus photoreceptors after destruction of the inner retina. Vis Neurosci. 1992 May;8(5):487–490. doi: 10.1017/s0952523800005009. [DOI] [PubMed] [Google Scholar]
- Cohen A. I., Blazynski C. Dopamine and its agonists reduce a light-sensitive pool of cyclic AMP in mouse photoreceptors. Vis Neurosci. 1990 Jan;4(1):43–52. doi: 10.1017/s0952523800002753. [DOI] [PubMed] [Google Scholar]
- Dearry A., Burnside B. Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: I. Induction of cone contraction is mediated by D2 receptors. J Neurochem. 1986 Apr;46(4):1006–1021. doi: 10.1111/j.1471-4159.1986.tb00612.x. [DOI] [PubMed] [Google Scholar]
- Dearry A., Burnside B. Dopaminergic regulation of cone retinomotor movement in isolated teleost retinas: II. Modulation by gamma-aminobutyric acid and serotonin. J Neurochem. 1986 Apr;46(4):1022–1031. doi: 10.1111/j.1471-4159.1986.tb00613.x. [DOI] [PubMed] [Google Scholar]
- Dearry A., Burnside B. Light-induced dopamine release from teleost retinas acts as a light-adaptive signal to the retinal pigment epithelium. J Neurochem. 1989 Sep;53(3):870–878. doi: 10.1111/j.1471-4159.1989.tb11785.x. [DOI] [PubMed] [Google Scholar]
- Dearry A., Edelman J. L., Miller S., Burnside B. Dopamine induces light-adaptive retinomotor movements in bullfrog cones via D2 receptors and in retinal pigment epithelium via D1 receptors. J Neurochem. 1990 Apr;54(4):1367–1378. doi: 10.1111/j.1471-4159.1990.tb01971.x. [DOI] [PubMed] [Google Scholar]
- Dearry A. Light onset stimulates tyrosine hydroxylase activity in isolated teleost retinas. Vision Res. 1991;31(3):395–399. doi: 10.1016/0042-6989(91)90092-j. [DOI] [PubMed] [Google Scholar]
- Godley B. F., Wurtman R. J. Release of endogenous dopamine from the superfused rabbit retina in vitro: effect of light stimulation. Brain Res. 1988 Jun 14;452(1-2):393–395. doi: 10.1016/0006-8993(88)90046-7. [DOI] [PubMed] [Google Scholar]
- Kirsch M., Wagner H. J. Release pattern of endogenous dopamine in teleost retinae during light adaptation and pharmacological stimulation. Vision Res. 1989;29(2):147–154. doi: 10.1016/0042-6989(89)90120-x. [DOI] [PubMed] [Google Scholar]
- Kohler K., Kolbinger W., Kurz-Isler G., Weiler R. Endogenous dopamine and cyclic events in the fish retina, II: Correlation of retinomotor movement, spinule formation, and connexon density of gap junctions with dopamine activity during light/dark cycles. Vis Neurosci. 1990 Nov;5(5):417–428. doi: 10.1017/s0952523800000547. [DOI] [PubMed] [Google Scholar]
- Kohler Konrad, Weiler Reto. Dopaminergic Modulation of Transient Neurite Outgrowth from Horizontal Cells of the Fish Retina is not Mediated by cAMP. Eur J Neurosci. 1990;2(9):788–794. doi: 10.1111/j.1460-9568.1990.tb00470.x. [DOI] [PubMed] [Google Scholar]
- Korenbrot J. I., Fernald R. D. Circadian rhythm and light regulate opsin mRNA in rod photoreceptors. Nature. 1989 Feb 2;337(6206):454–457. doi: 10.1038/337454a0. [DOI] [PubMed] [Google Scholar]
- LaVail M. M. Rod outer segment disc shedding in relation to cyclic lighting. Exp Eye Res. 1976 Aug;23(2):277–280. doi: 10.1016/0014-4835(76)90209-8. [DOI] [PubMed] [Google Scholar]
- McCormack C. A., Burnside B. A role for endogenous dopamine in circadian regulation of retinal cone movement. Exp Eye Res. 1992 Sep;55(3):511–520. doi: 10.1016/0014-4835(92)90125-c. [DOI] [PubMed] [Google Scholar]
- McCormack C. A., Burnside B. Effects of circadian phase on cone retinomotor movements in the Midas cichlid. Exp Eye Res. 1991 Apr;52(4):431–438. doi: 10.1016/0014-4835(91)90039-h. [DOI] [PubMed] [Google Scholar]
- McCormack C. A., Burnside B. Light and circadian modulation of teleost retinal tyrosine hydroxylase activity. Invest Ophthalmol Vis Sci. 1993 Apr;34(5):1853–1860. [PubMed] [Google Scholar]
- Nowak J. Z., Kazula A., Gołembiowska K. Melatonin increases serotonin N-acetyltransferase activity and decreases dopamine synthesis in light-exposed chick retina: in vivo evidence supporting melatonin-dopamine interaction in retina. J Neurochem. 1992 Oct;59(4):1499–1505. doi: 10.1111/j.1471-4159.1992.tb08466.x. [DOI] [PubMed] [Google Scholar]
- Nowak J. Z., Zurawska E. Dopamine in the rabbit retina and striatum: diurnal rhythm and effect of light stimulation. J Neural Transm. 1989;75(3):201–212. doi: 10.1007/BF01258631. [DOI] [PubMed] [Google Scholar]
- Pierce M. E., Besharse J. C. Circadian regulation of retinomotor movements. I. Interaction of melatonin and dopamine in the control of cone length. J Gen Physiol. 1985 Nov;86(5):671–689. doi: 10.1085/jgp.86.5.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weiler R., Kohler K., Kolbinger W., Wolburg H., Kurz-Isler G., Wagner H. J. Dopaminergic neuromodulation in the retinas of lower vertebrates. Neurosci Res Suppl. 1988;8:S183–S196. doi: 10.1016/0921-8696(88)90016-3. [DOI] [PubMed] [Google Scholar]
- Weiler R., Wagner H. J. Light-dependent change of cone-horizontal cell interactions in carp retina. Brain Res. 1984 Apr 23;298(1):1–9. doi: 10.1016/0006-8993(84)91141-7. [DOI] [PubMed] [Google Scholar]
- Witkovsky P., Shi X. P. Slow light and dark adaptation of horizontal cells in the Xenopus retina: a role for endogenous dopamine. Vis Neurosci. 1990 Oct;5(4):405–413. doi: 10.1017/s0952523800000493. [DOI] [PubMed] [Google Scholar]
- Witkovsky P., Stone S., Besharse J. C. Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Res. 1988 May 24;449(1-2):332–336. doi: 10.1016/0006-8993(88)91048-7. [DOI] [PubMed] [Google Scholar]
- Zawilska J. B., Iuvone P. M. Melatonin synthesis in chicken retina: effect of kainic acid-induced lesions on the diurnal rhythm and D2-dopamine receptor-mediated regulation of serotonin N-acetyltransferase activity. Neurosci Lett. 1992 Jan 20;135(1):71–74. doi: 10.1016/0304-3940(92)90138-w. [DOI] [PubMed] [Google Scholar]