CELLULAR BASIS FOR ROD-CONE INTERACTIONS IN THE OUTER RETINA

  • David Križaj Depts. of Ophthalmology and Physiology University of California San Francisco School of Medicine San Francisco CA 94143-0730
  • Marko Hawlina University Eye Clinic Medical Centre Ljubljana Zaloška 29a 1000 Ljubljana Slovenia
Keywords: photoreceptor, dopamine, horizontal cell, adaptational process

Abstract

Background. At least twice daily our retinas move between a light adapted, cone-dominated (photopic) state and a dark-adapted, color-blind and highly light-sensitive roddominated (scotopic) state. In between is a rather ill-defined transitional state called the mesopic state in which retinal circuits express both rod and cone signals. Consequently, in the mesopic state the retinal output to the brain contained in the firing patterns of the ganglion cells consists of information derived from both rod and cone signals. Morphology, physiology and psychophysics all contributed to an understanding that the two systems are not independent but interact extensively via both pooling and mutual inhibition. This review lays down a rationale for such rod-cone interactions in the vertebrate retinas. It suggests that the important functional roles of rod-cone interactions is in that they shorten the duration of the mesopic state. As a result, the retina is maintained in either in the (rod-dominated) high sensitivity photon counting mode or in the second mode which emphasizes temporal transients and spatial resolution (the cone-dominated photopic state).

Conclusions. Experimental evidence for pre- and postsynaptic mixing of rod and cone signals in the retina is shown together with the preeminent neuromodulatory role of both light and dopamine in controling inter-actions between rod and cone signals. Dopamine is shown to be both necessary and sufficient to mediate light adaptation in the retina.

Downloads

Download data is not yet available.

References

Aguilar M, Stiles WS. Saturation of the rod mechanism of the retina at high levels of saturation. Optica Acta 1954; 1: 59–65.

MacLeod DIA. Rods cancel cones in flicker. Nature 1972; 235: 173–4.

Sandberg MA, Berson EL, Effron M. Rod-cone interaction in the distal human retina. Science 1983; 212: 829–31.

Alexander KR, Fishman GA, Derlacki DJ. Mechanisms of rod-cone interaction: evidence from congenital stationary nightblindness. Vision Res 1988; 28: 575–83.

Xin D, Bloomfield S. Comparison of responses of AII amacrine cells in the dark and light-adapted rabbit retina. Visual Neurosci 1999; 16: 653–65.

Stone S, Buck SL, Dacey DM. Pharmacological dissection of rod and cone bipolar input to the AII amacrine in macaque retina. Invest Ophthalmol and Vis Sci 1997; 38: S689–9.

Verweij J, Dacey DM, Peterson BB, Buck SL. Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina. Vision Res 1999; 39: 3662–72.

Steinberg RH. Rod-cone interaction in S-potentials from the cat retina. J Physiol 1969; 9: 1331–44.

Raviola E, Gilula NB. Gap junctions between photoreceptor cells in the vertebrate retina. Proc Nat’l Acad Sci USA 1973; 70: 1677–81.

Nelson R. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. J Comp Neurol 1977; 172: 109–35.

Rodieck RW, Rushton WAH. Cancellation of rod signals by cones, and cone signals by rods in the cat retina. J Physiol 1976; 254: 775–85.

Enroth-Cugell C, Hertz BG, Lennie P. Convergence of rod and cone signals in the cat’s retina. J Physiol 1977; 269: 297–318.

Schwartz EA. Cones excite rods in the retina of the turtle. J Physiol 1975; 246: 639–51.

Goldberg SH, Frumkes TE, Nygaard RW. Inhibitory influence of unstimulated rods in the human retina. Science 1983; 221: 180–2.

Hassin G, Witkovsky P. Intracellular recording from identified photoreceptors and horizontal cells of the Xenopus retina. Vision Res 1983; 23: 921–31.

Arden GB, Hogg CR. Rod-cone interaction and analysis of retinal disease. Br J Ophthalmol 1985; 69: 404–15.

Dong CJ, Qian HH, McReynolds JS, Yang XL, Liu YM. Suppression of conedriven responses by rods in the isolated frog retina. Visual Neurosci 1988; 1: 331–8.

Frumkes TE, Eysteinsson T. Suppressive rod-cone interaction in the vertebrate retina: intracellular records from Xenopus and Necturus. J Neurophysiol 1988; 57: 1361–82.

Witkovsky P, Stone S, Besharse JC. Dopamine modifies the balance of rod and cone inputs to horizontal cells of the Xenopus retina. Brain Res 1988; 449: 332–6.

Witkovsky P, Shi XP. Slow light and dark-adaptation of horizontal cells in the Xenopus retina: a role for endogenous dopamine. Visual Neurosci 1991; 5: 405–13.

Stockman A, Sharpe LT, Ruther K, Nordby K. Two signals in the human rod visual system: a model based on electrophysiological data. Visual Neurosci 1995; 12: 951–70.

Witkovsky P, Schmitz Y, Akopian A, Krizaj D, Tranchina D. Gain of rod to horizontal cell synaptic transfer: relation to glutamate release and a dihydropyridine-sensitive calcium current. J Neurosci 1997; 17: 7297–306.

Krizaj D. The mesopic state: cellular mechanisms involved in pre- and postsynaptic mixing of rod and cone signals. Microscopy Res Tech 2000; 50: 347–59.

Wu SM. Synaptic transmission in the outer retina. Ann Rev Physiol 1994; 56: 141–68.

Attwell D, Wilson M, Wu SM. A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina. J Physiol 1984; 352: 703–37.

Yang XL, Wu SM. Modulation of rod-cone coupling by light. Science 1989; 244: 352–4.

Cook JE, Becker DL. Gap junctions in the vertebrate retina. Microscopy Res Tech 1995; 31: 408–19.

Krizaj D, Vu T, Copenhagen DR. On the shaping, modulation and synaptic transmission of rod and cone signals. In: Toyoda J, Murakami M, Kaneko A, Saito T eds. The retinal basis of vision. Amsterdam: Elsevier Press, 1999.

Krizaj D, Gabriel R, Owen GW, Witkovsky P. Dopamine D2 receptormodulation of rod-cone coupling in the Xenopus retina. J Comp Neurol 1998; 398: 529–38.

Wu SM, Yang XL. Electrical coupling between rods and cones in the tiger salamander retina. Proc Nat’l Acad Sci USA 1988; 85: 275–8.

Krizaj D, Witkovsky P. Effects of submicromolar concentrations of dopamine on photoreceptor to horizontal cell communication. Brain Res 1993; 627: 122–8.

Muresan Z, Besharse J. D2-like dopamine receptors in amphibian retina: localization with fluorescent ligands. J Comp Neurol 1993; 331: 149–60.

Derouiche A, Asan E. The dopamine D2 receptor subfamily in rat retina: ultrastructural immunogold and in situ hybridization studies. Eur J Neurosci 1999; 11: 1391–402.

Cohen AI, Todd RD, Harmon S, O’Malley SLO. Photoreceptors of mouse retinas possess D4 receptors coupled to adenylate cyclase. PNAS 1992; 89: 12093–7.

Akopian A, Krizaj D, Witkovsky P. Both high- and low voltage-activated calcium currents contribute to the light-evoked responses of luminosity horizontal cells in the Xenopus retina. Brain Res 1997; 762: 121–30.

Stella SL, Thoreson WB. Differential modulation of rod and cone calcium currents by cAMP and a D2 dopamine agonist. Invest Ophththalmol Vis Sci Suppl 1998; 39: 983–3.

Sibley DR. New insights into dopaminergic receptor function using antisense and genetically altered animals. Annu Rev Pharmacol Toxicol 1999; 39: 313–41.

Krizaj D, Copenhagen DR. Compartmentalization of calcium extrusion mechanisms in the outer and inner segments of photoreceptors. Neuron 1998; 21: 249–56.

Allbritton NL, Meyer T, Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-triphosphate. Science1 992; 258: 1812–5.

Copenhagen DR, Green D. Spatial spread of adaptation within the cone network of the turtle retina. J Physiol 1986; 393: 763–76.

Koulen P, Kuhn R, Wässle H, Brandstätter JH. Modulation of intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proc Nat’l Acad Sci 1999; 96: 9909–14.

Cai W, Porcho RG. Localization of metabotropic glutamate receptors mGluR1alpha and mGluR2/3 in the cat retina. J Comp Neurol 1999; 407: 427–37.

Anderson FE, Green CB. Symphony of rhythms in the Xenopus laevis retina. Microscopy Res Tech 2000; 50: 360–72.

Attwell D, Borges S, Wu SM, Wilson M. Signal clipping by the rod output synapse. Nature 1987; 328: 522–4.

Witkovsky P, Schutte M. The organization of dopaminergic neurons in vertebrate retinas. Visual Neurosci 1991; 7: 113–24.

Witkovsky P, Nicholson C, Rice ME, Bohmaker K, Meller E. Extracellular dopamine concentration in the retina of the clawed frog, Xenopus laevis. Proc Nat’l Acad Sci USA 1993; 90: 5667–71.

Bjelke B, Goldstein TM, Tinner B, Andersson C et al. Dopaminergic transmission in the retina: evidence for volume transmission. J Chem Neuroanat 1996; 12: 37–50.

Boatright JH, Hoel MJ, Iuvone PM. Stimulation of endogenous dopamine release and metabolism in amphibian retina by light- and K+-evoked depolarization. Brain Res 1989; 482: 164–8.

Witkovsky P, Stone S, Tranchina D. Photoreceptor to horizontal cell synaptic transfer in the Xenopus retina: modulation by dopamine ligands and a circuit model for interactions of rod and cone inputs. J Neurophysiol 1989; 62: 864–81.

Krizaj D, Akopian A, Witkovsky P. The effects of L-glutamate, AMPA, quisqualate and kainate on retinal horizontal cells depend on adaptational state: implications for rod-cone interactions. J Neurosci 1994; 14: 5661–71.

Frohlich E, Negishi K, Wagner HJ. The occurrence of dopaminergic interplexiform cells correlates with the presence of cones in the retinae of fish. Visual Neurosci 1995; 12: 359–69.

Dowling JE, Lasater EM, Van Buskirk R, Watling KJ. Pharmacological properties of isolated fish horizontal cells. Vision Res 1983; 23: 421–32.

Qian H, Ripps H. Receptive fields of rod-driven horizontal cells in the skate retina. J Gen Physiol 1992; 100: 457–78.

Veruki ML, Wässle H. Immunohistochemistry localization of dopamine D1 receptors in rat retina. Eur J Neurosci 1996; 8: 2286–97.

Krizaj D. Synaptic integration and neuromodulation at the photoreceptor output synapse: mechanisms and functional significance. PhD Thesis. New York: New York University, 1995.

Witkovsky P, Dearry O. Functional roles of dopamine in the vertebrate retina. Progress Retinal Res 1991; 11: 247–92.

Young LH, Dowling JE. Localization of cyclic adenosine monophosphate in the teleost retina: effects of dopamine and prolonged darkness. Brain Res 1989; 504: 57–63.

Knapp AG, Dowling JE. Dopamine enhances excitatory amino acid-gated conductances in retinal horizontal cells. Nature 1987; 325: 437–9.

Dubocovich M. Melatonin is a potent modulator of dopamine release in the retina. Nature 1983; 306: 782–4.

Hawlina M, Jenkins HG, Ikeda H. Diurnal variations in the ERG c-wave and retinal melatonin content in rats with inherited retinal dystrophy. Doc Ophthalmol 1992; 79: 141–50.

Hankins MW, Ikeda H 1994. Early abnormalities of retinal dopamine pathways in rats with hereditary retinal dystrophy. Doc Ophthalmol 86: 325–34.

Hawlina M. Role of melatonin and dopamine in an animal model of hereditary retinal dystrophy. PhD Thesis. London: University of London, 1995.

Hack I, Peichl L, Brandstätter H. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proc Nat’l Acad Sci USA 1999; 96: 14130–5.

Sharpe LT, Stockman A. Rod pathways: the importance of seeing nothing. TINS 1999; 22: 497–504.

Diamond JS, Copenhagen DR. The contribution of NMDA and non-NMDA receptors to the light-evoked input-output characteristics of retinal ganglion cells. Neuron 1993; 11: 725–38.

Levine MW, Frishman LJ, Enroth-Cugell C. Interactions between the rod and the cone pathways in the cat retina. Vision Res 1987; 27: 1093–104.

Laughlin SB. The role of sensory adaptation in the retina. J Exp Biol 1989; 146: 39–62.

O’Donnell P, Grace AA. Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 1993; 13: 3456–71.

How to Cite
1.
Križaj D, Hawlina M. CELLULAR BASIS FOR ROD-CONE INTERACTIONS IN THE OUTER RETINA. TEST ZdravVestn [Internet]. 1 [cited 5Aug.2024];71. Available from: http://vestnik-dev.szd.si/index.php/ZdravVest/article/view/1749
Section
Review