Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1987 Aug 1;90(2):229–259. doi: 10.1085/jgp.90.2.229

Dynamics of the ganglion cell response in the catfish and frog retinas

PMCID: PMC2228836  PMID: 3498795

Abstract

Responses were evoked from ganglion cells in catfish and frog retinas by a Gaussian modulation of the mean luminance. An algorithm was devised to decompose intracellularly recorded responses into the slow and spike components and to extract the time of occurrence of a spike discharge. The dynamics of both signals were analyzed in terms of a series of first-through third-order kernels obtained by cross- correlating the slow (analog) or spike (discrete or point process) signals against the white-noise input. We found that, in the catfish, (a) the slow signals were composed mostly of postsynaptic potentials, (b) their linear components reflected the dynamics found in bipolar cells or in the linear response component of type-N (sustained) amacrine cells, and (c) their nonlinear components were similar to those found in either type-N or type-C (transient) amacrine cells. A comparison of the dynamics of slow and spike signals showed that the characteristic linear and nonlinear dynamics of slow signals were encoded into a spike train, which could be recovered through the cross- correlation between the white-noise input and the spike (point process signals. In addition, well-defined spike correlates could predict the observed slow potentials. In the spike discharges from frog ganglion cells, the linear (or first-order) kernels were all inhibitory, whereas the second-order kernels had characteristics of on-off transient excitation. The transient and sustained amacrine cells similar to those found in catfish retina were the sources of the nonlinear excitation. We conclude that bipolar cells and possibly the linear part of the type- N cell response are the source of linear, either excitatory or inhibitory, components of the ganglion cell responses, whereas amacrine cells are the source of the cells' static nonlinearity.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

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

  1. Ariel M., Daw N. W. Pharmacological analysis of directionally sensitive rabbit retinal ganglion cells. J Physiol. 1982 Mar;324:161–185. doi: 10.1113/jphysiol.1982.sp014105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BARLOW H. B. Summation and inhibition in the frog's retina. J Physiol. 1953 Jan;119(1):69–88. doi: 10.1113/jphysiol.1953.sp004829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baylor D. A., Fettiplace R. Synaptic drive and impulse generation in ganglion cells of turtle retina. J Physiol. 1979 Mar;288:107–127. [PMC free article] [PubMed] [Google Scholar]
  4. Bryant H. L., Segundo J. P. Spike initiation by transmembrane current: a white-noise analysis. J Physiol. 1976 Sep;260(2):279–314. doi: 10.1113/jphysiol.1976.sp011516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chappell R. L., Naka K., Sakuranaga M. Dynamics of turtle horizontal cell response. J Gen Physiol. 1985 Sep;86(3):423–453. doi: 10.1085/jgp.86.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Dowling J. E. Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates. Proc R Soc Lond B Biol Sci. 1968 Jun 11;170(1019):205–228. doi: 10.1098/rspb.1968.0034. [DOI] [PubMed] [Google Scholar]
  8. Dowling J. E., Werblin F. S. Organization of retina of the mudpuppy, Necturus maculosus. I. Synaptic structure. J Neurophysiol. 1969 May;32(3):315–338. doi: 10.1152/jn.1969.32.3.315. [DOI] [PubMed] [Google Scholar]
  9. Eggermont J. J., Johannesma P. M., Aertsen A. M. Reverse-correlation methods in auditory research. Q Rev Biophys. 1983 Aug;16(3):341–414. doi: 10.1017/s0033583500005126. [DOI] [PubMed] [Google Scholar]
  10. Frumkes T. E., Miller R. F., Slaughter M., Dacheux R. F. Physiological and pharmacological basis of GABA and glycine action on neurons of mudpuppy retina. III. Amacrine-mediated inhibitory influences on ganglion cell receptive-field organization: a model. J Neurophysiol. 1981 Apr;45(4):783–804. doi: 10.1152/jn.1981.45.4.783. [DOI] [PubMed] [Google Scholar]
  11. GERSTEIN G. L., KIANG N. Y. An approach to the quantitative analysis of electrophysiological data from single neurons. Biophys J. 1960 Sep;1:15–28. doi: 10.1016/s0006-3495(60)86872-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hochstein S., Shapley R. M. Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. J Physiol. 1976 Nov;262(2):265–284. doi: 10.1113/jphysiol.1976.sp011595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kaneko A. Receptive field organization of bipolar and amacrine cells in the goldfish retina. J Physiol. 1973 Nov;235(1):133–153. doi: 10.1113/jphysiol.1973.sp010381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Knight B. W., Toyoda J. I., Dodge F. A., Jr A quantitative description of the dynamics of excitation and inhibition in the eye of Limulus. J Gen Physiol. 1970 Oct;56(4):421–437. doi: 10.1085/jgp.56.4.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Marchiafava P. L. Centrifugal actions on amacrine and ganglion cells in the retina of the turtle. J Physiol. 1976 Feb;255(1):137–155. doi: 10.1113/jphysiol.1976.sp011273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marchiafava P. L., Torre V. Self-facilitation of ganglion cells in the retina of the turtle. J Physiol. 1977 Jun;268(2):335–351. doi: 10.1113/jphysiol.1977.sp011860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Marchiafava P. L., Weiler R. The photoresponses of structurally identified amacrine cells in the turtle retina. Proc R Soc Lond B Biol Sci. 1982 Feb 22;214(1196):403–415. doi: 10.1098/rspb.1982.0019. [DOI] [PubMed] [Google Scholar]
  18. Marmarelis P. Z., Naka K. I. Nonlinear analysis and synthesis of receptive-field responses in the catfish retina. I. Horizontal cell leads to ganglion cell chain. J Neurophysiol. 1973 Jul;36(4):605–618. doi: 10.1152/jn.1973.36.4.605. [DOI] [PubMed] [Google Scholar]
  19. Mizunami M., Tateda H., Naka K. Dynamics of cockroach ocellar neurons. J Gen Physiol. 1986 Aug;88(2):275–292. doi: 10.1085/jgp.88.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Naka K. I., Itoh M. A., Chappell R. L. Dynamics of turtle cones. J Gen Physiol. 1987 Feb;89(2):321–337. doi: 10.1085/jgp.89.2.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Naka K. Functional organization of catfish retina. J Neurophysiol. 1977 Jan;40(1):26–43. doi: 10.1152/jn.1977.40.1.26. [DOI] [PubMed] [Google Scholar]
  22. Naka K., Marmarelis P. Z., Chan R. Y. Morphological and functional identifications of catfish retinal neurons. III. Functional identification. J Neurophysiol. 1975 Jan;38(1):92–131. doi: 10.1152/jn.1975.38.1.92. [DOI] [PubMed] [Google Scholar]
  23. RUSHTON W. A. VISUAL ADAPTATION. Proc R Soc Lond B Biol Sci. 1965 Mar 16;162:20–46. doi: 10.1098/rspb.1965.0024. [DOI] [PubMed] [Google Scholar]
  24. Sakai H. M., Naka K., Dowling J. E. Ganglion cell dendrites are presynaptic in catfish retina. Nature. 1986 Feb 6;319(6053):495–497. doi: 10.1038/319495a0. [DOI] [PubMed] [Google Scholar]
  25. Sakuranaga M., Naka K. Signal transmission in the catfish retina. I. Transmission in the outer retina. J Neurophysiol. 1985 Feb;53(2):373–389. doi: 10.1152/jn.1985.53.2.373. [DOI] [PubMed] [Google Scholar]
  26. Sakuranaga M., Naka K. Signal transmission in the catfish retina. II. Transmission to type-N cell. J Neurophysiol. 1985 Feb;53(2):390–410. doi: 10.1152/jn.1985.53.2.390. [DOI] [PubMed] [Google Scholar]
  27. Sakuranaga M., Naka K. Signal transmission in the catfish retina. III. Transmission to type-C cell. J Neurophysiol. 1985 Feb;53(2):411–428. doi: 10.1152/jn.1985.53.2.411. [DOI] [PubMed] [Google Scholar]
  28. Sakuranaga M., Sato S., Hida E., Naka K. Nonlinear analysis: mathematical theory and biological applications. Crit Rev Biomed Eng. 1986;14(2):127–184. [PubMed] [Google Scholar]
  29. Schellart N. A., Spekreijse H. Dynamic characteristics of retinal ganglion cell responses in goldfish. J Gen Physiol. 1972 Jan;59(1):1–21. doi: 10.1085/jgp.59.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thibos L. N., Werblin F. S. The response properties of the steady antagonistic surround in the mudpuppy retina. J Physiol. 1978 May;278:79–99. doi: 10.1113/jphysiol.1978.sp012294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tsutsu-ura M., Takauji M., Nagai T. Effects of external calcium reduction on biphasic potassium contractures and action of divalent cations on the calcium reduction in frog single twitch muscle fibers. Jpn J Physiol. 1984;34(3):485–495. doi: 10.2170/jjphysiol.34.485. [DOI] [PubMed] [Google Scholar]
  32. Victor J. D., Shapley R. M., Knight B. W. Nonlinear analysis of cat retinal ganglion cells in the frequency domain. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3068–3072. doi: 10.1073/pnas.74.7.3068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Victor J. D., Shapley R. M. Receptive field mechanisms of cat X and Y retinal ganglion cells. J Gen Physiol. 1979 Aug;74(2):275–298. doi: 10.1085/jgp.74.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Werblin F. S. Regenerative amacrine cell depolarization and formation of on-off ganglion cell response. J Physiol. 1977 Jan;264(3):767–785. doi: 10.1113/jphysiol.1977.sp011693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. de Boer R., Kuyper P. Triggered correlation. IEEE Trans Biomed Eng. 1968 Jul;15(3):169–179. doi: 10.1109/tbme.1968.4502561. [DOI] [PubMed] [Google Scholar]

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

RESOURCES