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Biophysical Journal logoLink to Biophysical Journal
. 1994 Jul;67(1):57–63. doi: 10.1016/S0006-3495(94)80454-0

Rate of quantal transmitter release at the mammalian rod synapse.

R Rao 1, G Buchsbaum 1, P Sterling 1
PMCID: PMC1225334  PMID: 7919023

Abstract

Under scotopic conditions, the mammalian rod encodes either one photon or none within its integration time. Consequently the signal presented to its synaptic terminal is binary. The synapse has a single active zone that releases neurotransmitter quanta tonically in darkness and pauses briefly in response to a rhodopsin isomerization by a photon. We asked: what minimum tonic rate would allow the postsynaptic bipolar cell to distinguish this pause from an extra-long interval between quanta due to the stochastic timing of release? The answer required a model of the circuit that included the rod convergence onto the bipolar cell and the bipolar cell's signal-to-noise ratio. Calculations from the model suggest that tonic release must be at least 40 quanta/s. This tonic rate is much higher than at conventional synapses where reliability is achieved by employing multiple active zones. The rod's synaptic mechanism makes efficient use of space, which in the retina is at a premium.

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Selected References

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

  1. Ashmore J. F., Copenhagen D. R. An analysis of transmission from cones to hyperpolarizing bipolar cells in the retina of the turtle. J Physiol. 1983 Jul;340:569–597. doi: 10.1113/jphysiol.1983.sp014781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashmore J. F., Copenhagen D. R. Different postsynaptic events in two types of retinal bipolar cell. Nature. 1980 Nov 6;288(5786):84–86. doi: 10.1038/288084a0. [DOI] [PubMed] [Google Scholar]
  3. Barlow H. B., Levick W. R., Yoon M. Responses to single quanta of light in retinal ganglion cells of the cat. Vision Res. 1971;Suppl 3:87–101. doi: 10.1016/0042-6989(71)90033-2. [DOI] [PubMed] [Google Scholar]
  4. Baylor D. A., Nunn B. J., Schnapf J. L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J Physiol. 1984 Dec;357:575–607. doi: 10.1113/jphysiol.1984.sp015518. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Betz W. J., Bewick G. S. Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J Physiol. 1993 Jan;460:287–309. doi: 10.1113/jphysiol.1993.sp019472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boycott B. B., Kolb H. The connections between bipolar cells and photoreceptors in the retina of the domestic cat. J Comp Neurol. 1973 Mar 1;148(1):91–114. doi: 10.1002/cne.901480106. [DOI] [PubMed] [Google Scholar]
  7. Ceccarelli B., Hurlbut W. P., Iezzi N. Effect of alpha-latrotoxin on the frog neuromuscular junction at low temperature. J Physiol. 1988 Aug;402:195–217. doi: 10.1113/jphysiol.1988.sp017200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cervetto L., Piccolino M. Synaptic transmission between photoreceptors and horizontal cells in the turtle retina. Science. 1974 Feb 1;183(4123):417–419. doi: 10.1126/science.183.4123.417. [DOI] [PubMed] [Google Scholar]
  9. Chun M. H., Han S. H., Chung J. W., Wässle H. Electron microscopic analysis of the rod pathway of the rat retina. J Comp Neurol. 1993 Jun 22;332(4):421–432. doi: 10.1002/cne.903320404. [DOI] [PubMed] [Google Scholar]
  10. Dacheux R. F., Raviola E. The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J Neurosci. 1986 Feb;6(2):331–345. doi: 10.1523/JNEUROSCI.06-02-00331.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Edwards F. A., Konnerth A., Sakmann B. Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J Physiol. 1990 Nov;430:213–249. doi: 10.1113/jphysiol.1990.sp018289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freed M. A., Smith R. G., Sterling P. Rod bipolar array in the cat retina: pattern of input from rods and GABA-accumulating amacrine cells. J Comp Neurol. 1987 Dec 15;266(3):445–455. doi: 10.1002/cne.902660310. [DOI] [PubMed] [Google Scholar]
  14. Gleason E., Borges S., Wilson M. Synaptic transmission between pairs of retinal amacrine cells in culture. J Neurosci. 1993 Jun;13(6):2359–2370. doi: 10.1523/JNEUROSCI.13-06-02359.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grünert U., Martin P. R. Rod bipolar cells in the macaque monkey retina: immunoreactivity and connectivity. J Neurosci. 1991 Sep;11(9):2742–2758. doi: 10.1523/JNEUROSCI.11-09-02742.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heuser J. E., Reese T. S., Dennis M. J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jack J. J., Redman S. J., Wong K. Modifications to synaptic transmission at group Ia synapses on cat spinal motoneurones by 4-aminopyridine. J Physiol. 1981 Dec;321:111–126. doi: 10.1113/jphysiol.1981.sp013974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kaneko A. Physiology of the retina. Annu Rev Neurosci. 1979;2:169–191. doi: 10.1146/annurev.ne.02.030179.001125. [DOI] [PubMed] [Google Scholar]
  19. Kolb H., Linberg K. A., Fisher S. K. Neurons of the human retina: a Golgi study. J Comp Neurol. 1992 Apr 8;318(2):147–187. doi: 10.1002/cne.903180204. [DOI] [PubMed] [Google Scholar]
  20. Kolb H. The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations. J Neurocytol. 1977 Apr;6(2):131–153. doi: 10.1007/BF01261502. [DOI] [PubMed] [Google Scholar]
  21. Korn H., Faber D. S. Quantal analysis and synaptic efficacy in the CNS. Trends Neurosci. 1991 Oct;14(10):439–445. doi: 10.1016/0166-2236(91)90042-s. [DOI] [PubMed] [Google Scholar]
  22. Larkman A., Stratford K., Jack J. Quantal analysis of excitatory synaptic action and depression in hippocampal slices. Nature. 1991 Mar 28;350(6316):344–347. doi: 10.1038/350344a0. [DOI] [PubMed] [Google Scholar]
  23. MacLeod D. I., Chen B., Crognale M. Spatial organization of sensitivity regulation in rod vision. Vision Res. 1989;29(8):965–978. doi: 10.1016/0042-6989(89)90111-9. [DOI] [PubMed] [Google Scholar]
  24. Mastronarde D. N. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J Neurophysiol. 1983 Feb;49(2):325–349. doi: 10.1152/jn.1983.49.2.325. [DOI] [PubMed] [Google Scholar]
  25. Nakatani K., Tamura T., Yau K. W. Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J Gen Physiol. 1991 Mar;97(3):413–435. doi: 10.1085/jgp.97.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogden T. E. The receptor mosaic of Aotes trivirgatus: distribution of rods and cones. J Comp Neurol. 1975 Sep 15;163(2):193–202. doi: 10.1002/cne.901630205. [DOI] [PubMed] [Google Scholar]
  27. Raviola E., Raviola G. Structure of the synaptic membranes in the inner plexiform layer of the retina: a freeze-fracture study in monkeys and rabbits. J Comp Neurol. 1982 Aug 10;209(3):233–248. doi: 10.1002/cne.902090303. [DOI] [PubMed] [Google Scholar]
  28. Redman S. Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev. 1990 Jan;70(1):165–198. doi: 10.1152/physrev.1990.70.1.165. [DOI] [PubMed] [Google Scholar]
  29. Sakitt B. Counting every quantum. J Physiol. 1972 May;223(1):131–150. doi: 10.1113/jphysiol.1972.sp009838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Smith R. G., Freed M. A., Sterling P. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. J Neurosci. 1986 Dec;6(12):3505–3517. doi: 10.1523/JNEUROSCI.06-12-03505.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Steinberg R. H., Reid M., Lacy P. L. The distribution of rods and cones in the retina of the cat (Felis domesticus). J Comp Neurol. 1973 Mar 15;148(2):229–248. doi: 10.1002/cne.901480209. [DOI] [PubMed] [Google Scholar]
  32. Sterling P., Freed M. A., Smith R. G. Architecture of rod and cone circuits to the on-beta ganglion cell. J Neurosci. 1988 Feb;8(2):623–642. doi: 10.1523/JNEUROSCI.08-02-00623.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tong G., Jahr C. E. Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron. 1994 Jan;12(1):51–59. doi: 10.1016/0896-6273(94)90151-1. [DOI] [PubMed] [Google Scholar]
  34. Trifonov I. U. Izuchenie sinapticheskoi peredachi mezhdu fotoretseptorom i gorizontal'noi kletkoi pri pomoshchi élektricheskikh razdrazhenii setchatki. Biofizika. 1968 Sep-Oct;13(5):809–817. [PubMed] [Google Scholar]
  35. Vaney D. I., Young H. M., Gynther I. C. The rod circuit in the rabbit retina. Vis Neurosci. 1991 Jul-Aug;7(1-2):141–154. doi: 10.1017/s0952523800011019. [DOI] [PubMed] [Google Scholar]
  36. Weibel E. R., Taylor C. R., Hoppeler H. The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10357–10361. doi: 10.1073/pnas.88.22.10357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Young H. M., Vaney D. I. Rod-signal interneurons in the rabbit retina: 1. Rod bipolar cells. J Comp Neurol. 1991 Aug 8;310(2):139–153. doi: 10.1002/cne.903100202. [DOI] [PubMed] [Google Scholar]
  38. von Gersdorff H., Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature. 1994 Feb 24;367(6465):735–739. doi: 10.1038/367735a0. [DOI] [PubMed] [Google Scholar]

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