Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1991;440:291–309. doi: 10.1113/jphysiol.1991.sp018709

The relationship between light, dopamine release and horizontal cell coupling in the mudpuppy retina.

C J Dong 1, J S McReynolds 1
PMCID: PMC1180153  PMID: 1687151

Abstract

1. The effect of different experimental conditions on electrical coupling between horizontal cells in the mudpuppy retina was studied by comparing the changes in responses to illumination of the central and peripheral portions of the receptive field, using centred spot and annulus stimuli. An increase in the amplitude of the response to a centred spot stimulus and a decrease in the amplitude of the response to a concentric annulus indicated a decrease in coupling, and vice versa. 2. Dopamine (10-250 microM) caused a decrease in coupling between horizontal cells. The uncoupling effect of dopamine was much greater in dark-adapted than in light-adapted retinas. The effect of the D1-receptor agonist SKF38393 was similar to that of dopamine. The effect of the D2-receptor agonist LY171555 on coupling was opposite to that of dopamine; this was attributed to a reduction in endogenous dopamine release. 3. The D1 antagonist SCH23390 (15 microM) caused an increase in coupling between horizontal cells. This effect was much greater in light-adapted than in dark-adapted retinas. 4. The glutamate analogue 2-amino-4-phosphonobutyrate (APB), which hyperpolarizes on-centre bipolar cells and blocks their responses to light, caused an increase in coupling between horizontal cells. This effect of APB was greater in light-adapted retinas than in dark-adapted retinas. The effect of APB on coupling could be reversed by the addition of dopamine, but the effect of dopamine on coupling could not be reversed by the addition of APB. These results suggest that APB increases horizontal cell coupling by causing a decrease in dopamine release. 5. In dark-adapted retinas, 2.5 min exposure to an adapting light caused a decrease in coupling between horizontal cells; the uncoupling effect of the adapting light was blocked in the presence of either SCH23390 or APB. 6. The results suggest that coupling between horizontal cells in the mudpuppy retina is decreased by dopamine acting at D1 receptors, that the release of dopamine affecting horizontal cells is greater under light-adapted conditions, and that the pathway by which exposure to light increases this dopamine release is mainly via on-centre bipolar cells.

Full text

PDF
291

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baldridge W. H., Ball A. K., Miller R. G. Dopaminergic regulation of horizontal cell gap junction particle density in goldfish retina. J Comp Neurol. 1987 Nov 15;265(3):428–436. doi: 10.1002/cne.902650310. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Colburn T. R., Schwartz E. A. Linear voltage control of current passed through a micropipette with variable resistance. Med Biol Eng. 1972 Jul;10(4):504–509. doi: 10.1007/BF02474198. [DOI] [PubMed] [Google Scholar]
  4. DeVries S. H., Schwartz E. A. Modulation of an electrical synapse between solitary pairs of catfish horizontal cells by dopamine and second messengers. J Physiol. 1989 Jul;414:351–375. doi: 10.1113/jphysiol.1989.sp017692. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dong C. J., McReynolds J. S. APB increases apparent coupling between horizontal cells in mudpuppy retina. Vision Res. 1989;29(5):541–544. doi: 10.1016/0042-6989(89)90040-0. [DOI] [PubMed] [Google Scholar]
  6. Dowling J. E., Ehinger B. The interplexiform cell system. I. Synapses of the dopaminergic neurons of the goldfish retina. Proc R Soc Lond B Biol Sci. 1978 Apr 13;201(1142):7–26. doi: 10.1098/rspb.1978.0030. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Kaneko A. Electrical connexions between horizontal cells in the dogfish retina. J Physiol. 1971 Feb;213(1):95–105. doi: 10.1113/jphysiol.1971.sp009370. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Knapp A. G., Dowling J. E. Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. 1987 Jan 29-Feb 4Nature. 325(6103):437–439. doi: 10.1038/325437a0. [DOI] [PubMed] [Google Scholar]
  11. Kurz-Isler G., Wolburg H. Gap junctions between horizontal cells in the cyprinid fish alter rapidly their structure during light and dark adaptation. Neurosci Lett. 1986 Jun 6;67(1):7–12. doi: 10.1016/0304-3940(86)90199-0. [DOI] [PubMed] [Google Scholar]
  12. Lamb T. D. Spatial properties of horizontal cell responses in the turtle retina. J Physiol. 1976 Dec;263(2):239–255. doi: 10.1113/jphysiol.1976.sp011630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lasater E. M., Dowling J. E. Dopamine decreases conductance of the electrical junctions between cultured retinal horizontal cells. Proc Natl Acad Sci U S A. 1985 May;82(9):3025–3029. doi: 10.1073/pnas.82.9.3025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mangel S. C., Dowling J. E. Responsiveness and receptive field size of carp horizontal cells are reduced by prolonged darkness and dopamine. Science. 1985 Sep 13;229(4718):1107–1109. doi: 10.1126/science.4035351. [DOI] [PubMed] [Google Scholar]
  15. Mangel S. C., Dowling J. E. The interplexiform-horizontal cell system of the fish retina: effects of dopamine, light stimulation and time in the dark. Proc R Soc Lond B Biol Sci. 1987 Jun 22;231(1262):91–121. doi: 10.1098/rspb.1987.0037. [DOI] [PubMed] [Google Scholar]
  16. Miyachi E., Murakami M. Decoupling of horizontal cells in carp and turtle retinae by intracellular injection of cyclic AMP. J Physiol. 1989 Dec;419:213–224. doi: 10.1113/jphysiol.1989.sp017870. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nawy S., Sie A., Copenhagen D. R. The glutamate analog 2-amino-4-phosphonobutyrate antagonizes synaptic transmission from cones to horizontal cells in the goldfish retina. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1726–1730. doi: 10.1073/pnas.86.5.1726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Negishi K., Teranishi T., Kato S. A GABA antagonist, bicuculline, exerts its uncoupling action on external horizontal cells through dopamine cells in carp retina. Neurosci Lett. 1983 Jun 30;37(3):261–266. doi: 10.1016/0304-3940(83)90441-x. [DOI] [PubMed] [Google Scholar]
  19. Nguyen-Legros J., Versaux-Botteri C., Vigny A., Raoux N. Tyrosine hydroxylase immunohistochemistry fails to demonstrate dopaminergic interplexiform cells in the turtle retina. Brain Res. 1985 Jul 29;339(2):323–328. doi: 10.1016/0006-8993(85)90098-8. [DOI] [PubMed] [Google Scholar]
  20. Piccolino M., Neyton J., Gerschenfeld H. M. Decrease of gap junction permeability induced by dopamine and cyclic adenosine 3':5'-monophosphate in horizontal cells of turtle retina. J Neurosci. 1984 Oct;4(10):2477–2488. doi: 10.1523/JNEUROSCI.04-10-02477.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Piccolino M., Neyton J., Witkovsky P., Gerschenfeld H. M. gamma-Aminobutyric acid antagonists decrease junctional communication between L-horizontal cells of the retina. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3671–3675. doi: 10.1073/pnas.79.11.3671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Slaughter M. M., Miller R. F. 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science. 1981 Jan 9;211(4478):182–185. doi: 10.1126/science.6255566. [DOI] [PubMed] [Google Scholar]
  23. Teranishi T., Negishi K., Kato S. Dopamine modulates S-potential amplitude and dye-coupling between external horizontal cells in carp retina. Nature. 1983 Jan 20;301(5897):243–246. doi: 10.1038/301243a0. [DOI] [PubMed] [Google Scholar]
  24. Tornqvist K., Yang X. L., Dowling J. E. Modulation of cone horizontal cell activity in the teleost fish retina. III. Effects of prolonged darkness and dopamine on electrical coupling between horizontal cells. J Neurosci. 1988 Jul;8(7):2279–2288. doi: 10.1523/JNEUROSCI.08-07-02279.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Van Buskirk R., Dowling J. E. Isolated horizontal cells from carp retina demonstrate dopamine-dependent accumulation of cyclic AMP. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7825–7829. doi: 10.1073/pnas.78.12.7825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Weiler R., Kolbinger W., Kohler K. Reduced light responsiveness of the cone pathway during prolonged darkness does not result from an increase of dopaminergic activity in the fish retina. Neurosci Lett. 1989 Apr 24;99(1-2):214–218. doi: 10.1016/0304-3940(89)90292-9. [DOI] [PubMed] [Google Scholar]
  27. Witkovsky P., Eldred W., Karten H. J. Catecholamine- and indoleamine-containing neurons in the turtle retina. J Comp Neurol. 1984 Sep 10;228(2):217–225. doi: 10.1002/cne.902280208. [DOI] [PubMed] [Google Scholar]
  28. 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]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES