Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1978 Feb 1;71(2):157–175. doi: 10.1085/jgp.71.2.157

Feedback synaptic interaction in the dragonfly ocellar retina

PMCID: PMC2215705  PMID: 205624

Abstract

The intracellular response of the ocellar nerve dendrite, the second order neuron in the retina of the dragonfly ocellus, has been modified by application of various drugs and a model developed to explain certain features of that response. Curare blocked the response completely. Both picrotoxin and bicuculline eliminated the "off" overshoot. Bicuculline also decreased the size of response and the sensitivity. gamma-Aminobutyric acid (GABA), however, increased the size of response. The evidence indicates the possibility that the receptor transmitter is acetylcholine and is inhibitory to the ocellar nerve dendrite whereas the feedback transmitter from the ocellar nerve dendrite may be GABA and is facilitory to receptor transmitter release. The model of synaptic feedback interaction developed to be consistent with these results has certain important features. It suggests that the feedback transmitter is released in the dark to increase input sensitivity from receptors in response to dim light. This implies that the dark potential of the ocellar nerve dendrite may be determined by a dynamic equilibrium established by synaptic interaction between it and the receptor terminals. Such a system is also well suited to signalling phasic information about changes in level of illumination over a wide range of intensities, a characteristic which appears to be a significant feature of the dragonfly median ocellar response.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Barker J. L., Nicoll R. A. Gamma-aminobutyric acid: role in primary afferent depolarization. Science. 1972 Jun 2;176(4038):1043–1045. doi: 10.1126/science.176.4038.1043. [DOI] [PubMed] [Google Scholar]
  2. Bisti S., Iosif G., Marchesi G. F., Strata P. Pharmacological properties of inhibitions in the cerebellar cortex. Exp Brain Res. 1971;14(1):24–37. doi: 10.1007/BF00234908. [DOI] [PubMed] [Google Scholar]
  3. Brunelli M., Castellucci V., Kandel E. R. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science. 1976 Dec 10;194(4270):1178–1181. doi: 10.1126/science.186870. [DOI] [PubMed] [Google Scholar]
  4. COOMBS J. S., ECCLES J. C., FATT P. The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol. 1955 Nov 28;130(2):326–374. doi: 10.1113/jphysiol.1955.sp005412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carlsson A., Lindqvist M., Dahlström A., Fuxe K., Masuoka D. Effects of the amphetamine group on intraneuronal brain amines in vivo and in vitro. J Pharm Pharmacol. 1965 Aug;17(8):521–523. doi: 10.1111/j.2042-7158.1965.tb07717.x. [DOI] [PubMed] [Google Scholar]
  6. Castellucci V., Kandel E. R. Presynaptic facilitation as a mechanism for behavioral sensitization in Aplysia. Science. 1976 Dec 10;194(4270):1176–1178. doi: 10.1126/science.11560. [DOI] [PubMed] [Google Scholar]
  7. Cervetto L., MacNichol E. F., Jr Inactivation of horizontal cells in turtle retina by glutamate and aspartate. Science. 1972 Nov 17;178(4062):767–768. doi: 10.1126/science.178.4062.767. [DOI] [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. Chappell R. L., Dowling J. E. Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J Gen Physiol. 1972 Aug;60(2):121–147. doi: 10.1085/jgp.60.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Curtis D. R., Duggan A. W., Felix D., Johnston G. A. Bicuculline and central GABA receptors. Nature. 1970 Nov 14;228(5272):676–677. doi: 10.1038/228676a0. [DOI] [PubMed] [Google Scholar]
  11. Curtis D. R., Duggan A. W., Felix D., Johnston G. A. Bicuculline, an antagonist of GABA and synaptic inhibition in the spinal cord of the cat. Brain Res. 1971 Sep 10;32(1):69–96. doi: 10.1016/0006-8993(71)90156-9. [DOI] [PubMed] [Google Scholar]
  12. Curtis D. R., Duggan A. W., Felix D., Johnston G. A., McLennan H. Antagonism between bicuculline and GABA in the cat brain. Brain Res. 1971 Oct 8;33(1):57–73. doi: 10.1016/0006-8993(71)90305-2. [DOI] [PubMed] [Google Scholar]
  13. Curtis D. R., Felix D. The effect of bicuculline upon synaptic inhibition in the cerebral and cerebellar corticles of the cat. Brain Res. 1971 Nov;34(2):301–321. doi: 10.1016/0006-8993(71)90283-6. [DOI] [PubMed] [Google Scholar]
  14. Curtis D. R., Watkins J. C. The pharmacology of amino acids related to gamma-aminobutyric acid. Pharmacol Rev. 1965 Dec;17(4):347–391. [PubMed] [Google Scholar]
  15. DEL CASTILLO J., KATZ B. Changes in end-plate activity produced by presynaptic polarization. J Physiol. 1954 Jun 28;124(3):586–604. doi: 10.1113/jphysiol.1954.sp005131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DUCHATEAU G., FLORKIN M., LECLERCQ J. Concentrations des bases fixes et types de composition de la base totale de l'hémolymphe des insectes. Arch Int Physiol. 1953 Nov;61(4):518–549. doi: 10.3109/13813455309146555. [DOI] [PubMed] [Google Scholar]
  17. Dale H. H., Feldberg W., Vogt M. Release of acetylcholine at voluntary motor nerve endings. J Physiol. 1936 May 4;86(4):353–380. doi: 10.1113/jphysiol.1936.sp003371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Davidoff R. A., Aprison M. H. Picrotoxin antagonism of the inhibition of interneurons by glycine. Life Sci. 1969 Jan 1;8(1):107–112. doi: 10.1016/0024-3205(69)90299-9. [DOI] [PubMed] [Google Scholar]
  19. Davidoff R. A. Gamma-aminobutyric acid antagonism and presynaptic inhibition in the frog spinal cord. Science. 1972 Jan 21;175(4019):331–333. doi: 10.1126/science.175.4019.331. [DOI] [PubMed] [Google Scholar]
  20. DeFeudis F. V. Amino acids as central neurotransmitters. Annu Rev Pharmacol. 1975;15:105–130. doi: 10.1146/annurev.pa.15.040175.000541. [DOI] [PubMed] [Google Scholar]
  21. DeFeudis F. V. Amino acids as central neurotransmitters. Annu Rev Pharmacol. 1975;15:105–130. doi: 10.1146/annurev.pa.15.040175.000541. [DOI] [PubMed] [Google Scholar]
  22. Dowling J. E., Boycott B. B. Organization of the primate retina: electron microscopy. Proc R Soc Lond B Biol Sci. 1966 Nov 15;166(1002):80–111. doi: 10.1098/rspb.1966.0086. [DOI] [PubMed] [Google Scholar]
  23. Dowling J. E., Chappell R. L. Neural organization of the median ocellus of the dragonfly. II. Synaptic structure. J Gen Physiol. 1972 Aug;60(2):148–165. doi: 10.1085/jgp.60.2.148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Engberg I., Thaller A. On the interaction of picrotoxin with GABA and glycine in the spinal cord. Brain Res. 1970 Apr 1;19(1):151–154. doi: 10.1016/0006-8993(70)90244-1. [DOI] [PubMed] [Google Scholar]
  26. Flock A., Lam D. M. Neurotransmitter synthesis in inner ear and lateral line sense organs. Nature. 1974 May 10;249(453):142–144. doi: 10.1038/249142a0. [DOI] [PubMed] [Google Scholar]
  27. GLOWINSKI J., AXELROD J. EFFECT OF DRUGS ON THE UPTAKE, RELEASE, AND METABOLISM OF H3-NOREPINEPHRINE IN THE RAT BRAIN. J Pharmacol Exp Ther. 1965 Jul;149:43–49. [PubMed] [Google Scholar]
  28. Galindo A. GABA-picrotoxin interaction in the mammalian central nervous system. Brain Res. 1969 Aug;14(3):763–767. doi: 10.1016/0006-8993(69)90220-0. [DOI] [PubMed] [Google Scholar]
  29. Gerschenfeld H. M., Paupardin-Tritsch D. Ionic mechanisms and receptor properties underlying the responses of molluscan neurones to 5-hydroxytryptamine. J Physiol. 1974 Dec;243(2):427–456. doi: 10.1113/jphysiol.1974.sp010761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Glowinski J., Axelrod J. Effects of drugs on the disposition of H-3-norepinephrine in the rat brain. Pharmacol Rev. 1966 Mar;18(1):775–785. [PubMed] [Google Scholar]
  31. Godfraind J. M., Krnjević K., Pumain R. Doubtful value of bicuculline as a specific antagonist of GABA. Nature. 1970 Nov 14;228(5272):675–676. doi: 10.1038/228675a0. [DOI] [PubMed] [Google Scholar]
  32. Hartline H. K. Inhibitory interaction in the retina. UCLA Forum Med Sci. 1969;8:297–317. [PubMed] [Google Scholar]
  33. KIDD M. Electron microscopy of the inner plexiform layer of the retina in the cat and the pigeon. J Anat. 1962 Apr;96:179–187. [PMC free article] [PubMed] [Google Scholar]
  34. Kandel E. R., Tauc L. Heterosynaptic facilitation in neurones of the abdominal ganglion of Aplysia depilans. J Physiol. 1965 Nov;181(1):1–27. doi: 10.1113/jphysiol.1965.sp007742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kandel E. R., Tauc L. Mechanism of heterosynaptic facilitation in the giant cell of the abdominal ganglion of Aplysia depilans. J Physiol. 1965 Nov;181(1):28–47. doi: 10.1113/jphysiol.1965.sp007743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Kaneko A. Physiological and morphological identification of horizontal, bipolar and amacrine cells in goldfish retina. J Physiol. 1970 May;207(3):623–633. doi: 10.1113/jphysiol.1970.sp009084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kerkut G. A., Pitman R. M., Walker R. J. Iontophoretic application of acetylcholine and GABA onto insect central neurones. Comp Biochem Physiol. 1969 Nov 15;31(4):611–633. doi: 10.1016/0010-406x(69)90063-2. [DOI] [PubMed] [Google Scholar]
  38. McKenzie G. M., Szerb J. C. The effect of dihydroxyphenylalanine, pheniprazine and dextroamphetamine on the in vivo release of dopamine from the caudate nucleus. J Pharmacol Exp Ther. 1968 Aug;162(2):302–308. [PubMed] [Google Scholar]
  39. Miller J. J., McLennan H. The action of bicuculline upon acetylcholine-induced excitations of central neurones. Neuropharmacology. 1974 Aug;13(8):785–787. doi: 10.1016/0028-3908(74)90025-2. [DOI] [PubMed] [Google Scholar]
  40. 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]
  41. Murakami M., Shigematsu Y. Duality of conduction mechanism in bipolar cells of the frog retina. Vision Res. 1970 Jan;10(1):1–10. doi: 10.1016/0042-6989(70)90057-x. [DOI] [PubMed] [Google Scholar]
  42. Nicoll R. A. Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res. 1971 Dec 10;35(1):137–149. doi: 10.1016/0006-8993(71)90600-7. [DOI] [PubMed] [Google Scholar]
  43. Obata K., Takeda K., Shinozaki H. Further study on pharmacological properties of the cerebellar-induced inhibition of deiters neurones. Exp Brain Res. 1970 Nov 26;11(4):327–342. doi: 10.1007/BF00237907. [DOI] [PubMed] [Google Scholar]
  44. Oomura Y., Ono T., Sugimori M. Acetylcholine, an inhibitory transmitter in the rat lateral hypothalamus. Brain Res Bull. 1976 Jan-Feb;1(1):151–153. doi: 10.1016/0361-9230(76)90057-5. [DOI] [PubMed] [Google Scholar]
  45. Ozawa S., Hagiwara S., Nicolaysen K., Stuart A. E. Signal transmission from photoreceptors to ganglion cells in the visual system of the giant barnacle. Cold Spring Harb Symp Quant Biol. 1976;40:563–570. doi: 10.1101/sqb.1976.040.01.052. [DOI] [PubMed] [Google Scholar]
  46. Pitman R. M., Kerkut G. A. Comparison of the actions of iontophoretically applied acetylcholine and gamma aminobutyric acid with the EPSP and IPSP in cockroach central neurons. Comp Gen Pharmacol. 1970 Jun;1(2):221–230. doi: 10.1016/0010-4035(70)90056-x. [DOI] [PubMed] [Google Scholar]
  47. RATLIFF F., HARTLINE H. K., MILLER W. H. Spatial and temporal aspects of retinal inhibitory interaction. J Opt Soc Am. 1963 Jan;53:110–120. doi: 10.1364/josa.53.000110. [DOI] [PubMed] [Google Scholar]
  48. RATLIFF F., MUELLER C. G. Synthesis of "on-off" and "of" responses in a visual-neural system. Science. 1957 Oct 25;126(3278):840–841. doi: 10.1126/science.126.3278.840-a. [DOI] [PubMed] [Google Scholar]
  49. STEIN L. SELF-STIMULATION OF THE BRAIN AND THE CENTRAL STIMULANT ACTION OF AMPHETAMINE. Fed Proc. 1964 Jul-Aug;23:836–850. [PubMed] [Google Scholar]
  50. Schmitt R. O., Dev P., Smith B. H. Electrotonic processing of information by brain cells. Science. 1976 Jul 9;193(4248):114–120. doi: 10.1126/science.180598. [DOI] [PubMed] [Google Scholar]
  51. Shimahara T., Tauc L. Heterosynaptic facilitation in the giant cell of Aplysia. J Physiol. 1975 May;247(2):321–341. doi: 10.1113/jphysiol.1975.sp010934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Straughan D. W., Neal M. J., Simmonds M. A., Collins G. G., Hill R. G. Evaluation of bicuculline as a GABA antagonist. Nature. 1971 Oct 1;233(5318):352–354. doi: 10.1038/233352a0. [DOI] [PubMed] [Google Scholar]
  53. Svenneby G., Roberts E. Bicuculline and N-methylbicuculline--competitive inhibitors of brain acetylcholinesterase. J Neurochem. 1973 Oct;21(4):1025–1026. doi: 10.1111/j.1471-4159.1973.tb07551.x. [DOI] [PubMed] [Google Scholar]
  54. TAKEUCHI A., TAKEUCHI N. On the permeability of end-plate membrane during the action of transmitter. J Physiol. 1960 Nov;154:52–67. doi: 10.1113/jphysiol.1960.sp006564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. TAUC L., GERSCHENFELD H. M. Cholinergic transmission mechanisms for both excitation and inhibition in molluscan central synapses. Nature. 1961 Oct 28;192:366–367. doi: 10.1038/192366a0. [DOI] [PubMed] [Google Scholar]
  56. Tomita T. Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb Symp Quant Biol. 1965;30:559–566. doi: 10.1101/sqb.1965.030.01.054. [DOI] [PubMed] [Google Scholar]
  57. Toyoda J., Nosaki H., Tomita T. Light-induced resistance changes in single photoreceptors of Necturus and Gekko. Vision Res. 1969 Apr;9(4):453–463. doi: 10.1016/0042-6989(69)90134-5. [DOI] [PubMed] [Google Scholar]
  58. USHERWOOD P. N., GRUNDFEST H. PERIPHERAL INHIBITION IN SKELETAL MUSCLE OF INSECTS. J Neurophysiol. 1965 May;28:497–518. doi: 10.1152/jn.1965.28.3.497. [DOI] [PubMed] [Google Scholar]
  59. Werblin F. S., Dowling J. E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J Neurophysiol. 1969 May;32(3):339–355. doi: 10.1152/jn.1969.32.3.339. [DOI] [PubMed] [Google Scholar]
  60. Woodward D. J., Hoffer B. J., Siggins G. R., Oliver A. P. Inhibition of Purkinje cells in the frog cerebellum. II. Evidence for GABA as the inhibitory transmitter. Brain Res. 1971 Oct 8;33(1):91–100. doi: 10.1016/0006-8993(71)90308-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES