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. 1976 Jul 1;70(1):178–192. doi: 10.1083/jcb.70.1.178

Synaptic activity of frog retinal photoreceptors. A peroxidase uptake study

PMCID: PMC2109803  PMID: 1084350

Abstract

The uptake of horseradish peroxidase (HRP) into membranous structures, detectable by light and electron microscopy, is used here to monitor the synaptic activity of photoreceptors of isolated frog retinas maintained in the dark or under various illumination conditions. The major findings are: (a) Neurotransmission from photoreceptor terminals seems to involve the same types of endocytic membrane-retrieval processes that occur at other nerve terminals. Presumably, the endocytic processes compensate for exocytic events associated with neurotransmission. The retrieved membrane is "recycled" to form vesicles. Some of these accumulate near the synaptic ribbons, perhaps indicating reutilization for exocytosis. On the other hand, some retrieved membrane evidently is degraded via multivesicular bodies that appear to undergo "retrograde" transport from the receptor synapses to the myoid regions. (b) Photoreceptor terminals take up much HRP in the dark. Steady illumination markedly decreases uptake by rods. Uptake by cones is notably reduced only at illumination intensities higher than those that have maximal effects on rods. (c) The decrease in rod HRP uptake with light is reversible when retinas are allowed to adapt to the dark, if the light exposures used were at intensities that bleach very little visual pigment. Such "recovery" is not observed after light exposures that bleach a considerable amount of visual pigment. The cones recover their dark levels of HRP uptake even after light exposures that bleach considerable amounts of visual pigment. The changes in HRP uptake that we observe parallel expectations for photoreceptor synaptic neurotransmission derived from indirect physiological evidence.

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Selected References

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  1. Alpern M., Rushton W. A., Torii S. Signals from cones. J Physiol. 1970 Apr;207(2):463–475. doi: 10.1113/jphysiol.1970.sp009073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baylor D. A., Hodgkin A. L. Changes in time scale and sensitivity in turtle photoreceptors. J Physiol. 1974 Nov;242(3):729–758. doi: 10.1113/jphysiol.1974.sp010732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bibb C., Young R. W. Renewal of glycerol in the visual cells and pigment epithelium of the frog retina. J Cell Biol. 1974 Aug;62(2):378–389. doi: 10.1083/jcb.62.2.378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boynton R. M., Whitten D. N. Visual adaptation in monkey cones: recordings of late receptor potentials. Science. 1970 Dec 25;170(3965):1423–1426. doi: 10.1126/science.170.3965.1423. [DOI] [PubMed] [Google Scholar]
  5. Brown J. E., Pinto L. H. Ionic mechanism for the photoreceptor potential of the retina of Bufo marinus. J Physiol. 1974 Feb;236(3):575–591. doi: 10.1113/jphysiol.1974.sp010453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bäckström A. C., Reuter T. Receptive field organization of ganglion cells in the frog retina: contributions from cones, green rods and red rods. J Physiol. 1975 Mar;246(1):79–107. doi: 10.1113/jphysiol.1975.sp010881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dowling J. E., Ripps H. Effect of magnesium on horizontal cell activity in the skate retina. Nature. 1973 Mar 9;242(5393):101–103. doi: 10.1038/242101a0. [DOI] [PubMed] [Google Scholar]
  8. Dowling J. E., Ripps H. S-potentials in the skate retina. Intracellular recordings during light and dark adaptation. J Gen Physiol. 1971 Aug;58(2):163–189. doi: 10.1085/jgp.58.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. FURUKAWA T., HANAWA I. Effects of some common cations on electroretinogram of the toad. Jpn J Physiol. 1955 Dec 15;5(4):289–300. doi: 10.2170/jjphysiol.5.289. [DOI] [PubMed] [Google Scholar]
  10. Fain G. L., Dowling J. E. Intracellular recordings from single rods and cones in the mudpuppy retina. Science. 1973 Jun 15;180(4091):1178–1181. doi: 10.1126/science.180.4091.1178. [DOI] [PubMed] [Google Scholar]
  11. Friend D. S., Farquhar M. G. Functions of coated vesicles during protein absorption in the rat vas deferens. J Cell Biol. 1967 Nov;35(2):357–376. doi: 10.1083/jcb.35.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  13. Heuser J. E., Reese T. S., Landis D. M. Functional changes in frog neuromuscular junctions studied with freeze-fracture. J Neurocytol. 1974 Mar;3(1):109–131. doi: 10.1007/BF01111936. [DOI] [PubMed] [Google Scholar]
  14. Holtzman E., Freeman A. R., Kashner L. A. Stimulation-dependent alterations in peroxidase uptake at lobster neuromuscular junctions. Science. 1971 Aug 20;173(3998):733–736. doi: 10.1126/science.173.3998.733. [DOI] [PubMed] [Google Scholar]
  15. Holtzman E., Teichberg S., Abrahams S. J., Citkowitz E., Crain S. M., Kawai N., Peterson E. R. Notes on synaptic vesicles and related structures, endoplasmic reticulum, lysosomes and peroxisomes in nervous tissue and the adrenal medulla. J Histochem Cytochem. 1973 Apr;21(4):349–385. doi: 10.1177/21.4.349. [DOI] [PubMed] [Google Scholar]
  16. Hood D. C., Hock P. A., Grover B. G. Dark adaptation of the frog's rods. Vision Res. 1973 Oct;13(10):1953–1963. doi: 10.1016/0042-6989(73)90066-7. [DOI] [PubMed] [Google Scholar]
  17. Hood D. C., Hock P. A. Recovery of cone receptor activity in the frog's isolated retina. Vision Res. 1973 Oct;13(10):1943–1951. doi: 10.1016/0042-6989(73)90065-5. [DOI] [PubMed] [Google Scholar]
  18. Hood D., Hock P. A. Light adaptation of the receptors: increment threshold functions for the frog's rods and cones. Vision Res. 1975 May;15(5):545–553. doi: 10.1016/0042-6989(75)90301-6. [DOI] [PubMed] [Google Scholar]
  19. Hurlbut W. P., Ceccarelli B. Transmitter release and recycling of synaptic vesicle membrane at the neuromuscular junction. Adv Cytopharmacol. 1974;2:141–154. [PubMed] [Google Scholar]
  20. Jorgensen O. S., Mellerup E. T. Endocytotic formation of rat brain synaptic vesicles. Nature. 1974 Jun 21;249(459):770–771. doi: 10.1038/249770a0. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Korenbrot J. I., Cone R. A. Dark ionic flux and the effects of light in isolated rod outer segments. J Gen Physiol. 1972 Jul;60(1):20–45. doi: 10.1085/jgp.60.1.20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. NILSSON S. E. AN ELECTRON MICROSCOPIC CLASSIFICATION OF THE RETINAL RECEPTORS OF THE LEOPARD FROG (RANA PIPIENS). J Ultrastruct Res. 1964 Jun;10:390–416. doi: 10.1016/s0022-5320(64)80018-6. [DOI] [PubMed] [Google Scholar]
  25. Nagasawa J., Douglas W. W., Schulz R. A. Micropinocytotic origin of coated and smooth microvesicles ("synaptic vesicles") in neurosecretory terminals of posterior pituitary glands demonstrated by incorporation of horseradish peroxidase. Nature. 1971 Jul 30;232(5309):341–342. doi: 10.1038/232341a0. [DOI] [PubMed] [Google Scholar]
  26. Naka K. I., Rushton W. A. S-potential and dark adaptation in fish. J Physiol. 1968 Jan;194(1):259–269. doi: 10.1113/jphysiol.1968.sp008406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Negishi K., Sugawara K. Evidence for the anoxia sensitivity of the synaptic region at the outer plexiform layer in the fish retina. Vision Res. 1973 May;13(5):983–987. doi: 10.1016/0042-6989(73)90077-1. [DOI] [PubMed] [Google Scholar]
  28. Normann R. A., Werblin F. S. Control of retinal sensitivity. I. Light and dark adaptation of vertebrate rods and cones. J Gen Physiol. 1974 Jan;63(1):37–61. doi: 10.1085/jgp.63.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Raviola E., Gilula N. B. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. J Cell Biol. 1975 Apr;65(1):192–222. doi: 10.1083/jcb.65.1.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schacher S. M., Holtzman E., Hood D. C. Uptake of horseradish peroxidase by frog photoreceptor synapses in the dark and the light. Nature. 1974 May 17;249(454):261–263. doi: 10.1038/249261a0. [DOI] [PubMed] [Google Scholar]
  31. Sillman A. J., Ito H., Tomita T. Studies on the mass receptor potential of the isolated frog retina. II. On the basis of the ionic mechanism. Vision Res. 1969 Dec;9(12):1443–1451. doi: 10.1016/0042-6989(69)90060-1. [DOI] [PubMed] [Google Scholar]
  32. Toyoda J., Hashimoto H., Anno H., Tomita T. The rod response in the frog and studies by intracellular recording. Vision Res. 1970 Nov;10(11):1093–1100. doi: 10.1016/0042-6989(70)90026-x. [DOI] [PubMed] [Google Scholar]
  33. Toyoda J. Membrane resistance changes underlying the bipolar cell response in the carp retina. Vision Res. 1973 Feb;13(2):283–294. doi: 10.1016/0042-6989(73)90107-7. [DOI] [PubMed] [Google Scholar]
  34. Turner P. T., Harris A. B. Ultrastructure of exogenous peroxidase in cerebral cortex. Brain Res. 1974 Jul 12;74(2):305–326. doi: 10.1016/0006-8993(74)90585-x. [DOI] [PubMed] [Google Scholar]

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