Abstract
Horizontal cells invaginate the photoreceptors in the retina and form reciprocal synaptic connections in the cone pedicles. In fish retina the pattern of synaptic connections is plastic and modulated by the ambient light conditions. Numerous dendritic spinules protrude from the terminal horizontal-cell dendrites into the cone pedicle when the retina is light-adapted and are retracted during dark adaptation. The retraction of spinules can be induced during maintained illumination by an injection of the putative cone transmitter L-glutamate or its analogue kainic acid into the vitreous humor. The formation and the retraction of spinules have a time course of minutes. Activation of protein kinase C through phorbol esters initiates the formation of spinules, but the retraction has not yet been linked to a specific second messenger. Herein we report that physiological concentrations of the glutamate analogs quisqualic acid and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid induce retraction of spinules during maintained illumination. (+/-)-trans-1-Amino-1,3-cyclopentanedicarboxylic acid, an agonist for the metabotropic quisqualic acid receptor, was without effect on spinule retraction. N-Methyl-D-aspartate and L-2-amino-4-phosphonobutyric acid, agonists at other types of glutamate receptors, were also without any effect. The effects of the active agonists persisted when synaptic transmission was blocked. In the presence of the ionotropic quisqualate receptor antagonist 6-cyclo-7-nitro-quinoxaline-2,3-dione the effects of all active agonists were blocked. These results demonstrate that activation of ionotropic quisqualate receptors on the horizontal-cell membrane can induce dendritic spinule retraction, a process associated with dark adaptation.
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- Ariel M., Lasater E. M., Mangel S. C., Dowling J. E. On the sensitivity of H1 horizontal cells of the carp retina to glutamate, aspartate and their agonists. Brain Res. 1984 Mar 12;295(1):179–183. doi: 10.1016/0006-8993(84)90828-x. [DOI] [PubMed] [Google Scholar]
- Baird J. G., Challiss R. A., Nahorski S. R. Role for ionotropic and metabotropic receptors in quisqualate-stimulated inositol polyphosphate accumulation in rat cerebral cortex. Mol Pharmacol. 1991 Jun;39(6):745–753. [PubMed] [Google Scholar]
- Barnard E. A., Henley J. M. The non-NMDA receptors: types, protein structure and molecular biology. Trends Pharmacol Sci. 1990 Dec;11(12):500–507. doi: 10.1016/0165-6147(90)90051-9. [DOI] [PubMed] [Google Scholar]
- Dowling J. E., Lasater E. M., Van Buskirk R., Watling K. J. Pharmacological properties of isolated fish horizontal cells. Vision Res. 1983;23(4):421–432. doi: 10.1016/0042-6989(83)90089-5. [DOI] [PubMed] [Google Scholar]
- Gilbertson T. A., Scobey R., Wilson M. Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science. 1991 Mar 29;251(5001):1613–1615. doi: 10.1126/science.1849316. [DOI] [PubMed] [Google Scholar]
- Honoré T., Davies S. N., Drejer J., Fletcher E. J., Jacobsen P., Lodge D., Nielsen F. E. Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science. 1988 Aug 5;241(4866):701–703. doi: 10.1126/science.2899909. [DOI] [PubMed] [Google Scholar]
- Ishida A. T., Fain G. L. D-aspartate potentiates the effects of L-glutamate on horizontal cells in goldfish retina. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5890–5894. doi: 10.1073/pnas.78.9.5890. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishida A. T., Kaneko A., Tachibana M. Responses of solitary retinal horizontal cells from Carassius auratus to L-glutamate and related amino acids. J Physiol. 1984 Mar;348:255–270. doi: 10.1113/jphysiol.1984.sp015108. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishida A. T. Responses of solitary retinal horizontal cells to L-glutamate and kainic acid are antagonized by D-aspartate. Brain Res. 1984 Apr 23;298(1):25–32. doi: 10.1016/0006-8993(84)91143-0. [DOI] [PubMed] [Google Scholar]
- Kaneko A., Shimazaki H. Effects of external ions on the synaptic transmission from photorecptors to horizontal cells in the carp retina. J Physiol. 1975 Nov;252(2):509–522. doi: 10.1113/jphysiol.1975.sp011155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaneko A. The functional role of retinal horizontal cells. Jpn J Physiol. 1987;37(3):341–358. doi: 10.2170/jjphysiol.37.341. [DOI] [PubMed] [Google Scholar]
- Lasater E. M., Dowling J. E., Ripps H. Pharmacological properties of isolated horizontal and bipolar cells from the skate retina. J Neurosci. 1984 Aug;4(8):1966–1975. doi: 10.1523/JNEUROSCI.04-08-01966.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murakami M., Otsu K., Otsuka T. Effects of chemicals on receptors and horizontal cells in the retina. J Physiol. 1972 Dec;227(3):899–913. doi: 10.1113/jphysiol.1972.sp010065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murphy S. N., Miller R. J. Two distinct quisqualate receptors regulate Ca2+ homeostasis in hippocampal neurons in vitro. Mol Pharmacol. 1989 May;35(5):671–680. [PubMed] [Google Scholar]
- Perlman I., Knapp A. G., Dowling J. E. Responses of isolated white perch horizontal cells to changes in the concentration of photoreceptor transmitter agonists. Brain Res. 1989 May 15;487(1):16–25. doi: 10.1016/0006-8993(89)90935-9. [DOI] [PubMed] [Google Scholar]
- Schoepp D., Bockaert J., Sladeczek F. Pharmacological and functional characteristics of metabotropic excitatory amino acid receptors. Trends Pharmacol Sci. 1990 Dec;11(12):508–515. doi: 10.1016/0165-6147(90)90052-a. [DOI] [PubMed] [Google Scholar]
- Slaughter M. M., Miller R. F. An excitatory amino acid antagonist blocks cone input to sign-conserving second-order retinal neurons. Science. 1983 Mar 11;219(4589):1230–1232. doi: 10.1126/science.6131536. [DOI] [PubMed] [Google Scholar]
- Tachibana M. Permeability changes induced by L-glutamate in solitary retinal horizontal cells isolated from Carassius auratus. J Physiol. 1985 Jan;358:153–167. doi: 10.1113/jphysiol.1985.sp015545. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wagner H. J. Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas. J Neurocytol. 1980 Oct;9(5):573–590. doi: 10.1007/BF01205026. [DOI] [PubMed] [Google Scholar]
- Weiler R., Janssen-Bienhold U. Spinule-type neurite outgrowth from horizontal cells during light adaptation in the carp retina: an actin-dependent process. J Neurocytol. 1993 Feb;22(2):129–139. doi: 10.1007/BF01181576. [DOI] [PubMed] [Google Scholar]
- Weiler R., Kohler K., Janssen U. Protein kinase C mediates transient spinule-type neurite outgrowth in the retina during light adaptation. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3603–3607. doi: 10.1073/pnas.88.9.3603. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weiler R., Kohler K., Kirsch M., Wagner H. J. Glutamate and dopamine modulate synaptic plasticity in horizontal cell dendrites of fish retina. Neurosci Lett. 1988 May 3;87(3):205–209. doi: 10.1016/0304-3940(88)90449-1. [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]
- Wu S. M., Dowling J. E. L-aspartate: evidence for a role in cone photoreceptor synaptic transmission in the carp retina. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5205–5209. doi: 10.1073/pnas.75.10.5205. [DOI] [PMC free article] [PubMed] [Google Scholar]