Skip to main content
Log in

Ganglion Cells with Sustained Activity in the Fish Retina and Their Possible Function in Evaluation of Visual Scenes

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Background extracellular spike activity of single ganglion cells was recorded from axon terminals in the optic tectum of living immobilized fish. The sizes of the receptive fields of ON and OFF units with sustained responses (USR) amounted to 4–5° and were comparable with those of feature detectors. Generation of spike discharges by USR required contrast between the center and periphery of the receptive field. When there was no contrast, no spike activity appeared. The magnitude of the reaction was monotonically dependent on the level of this contrast. USR of both the ON and OFF types were connected with three types of cone (L, M, S). Both the center and periphery of the receptive field displayed color opponency, the center and periphery of the receptive field being opponent in terms of this characteristic. In other words, USR were double opponent and may thus take part in color discrimination. The simultaneous operation of feature detectors and ganglion cells with baseline activity separated into ON and OFF channels is represented retinotopically and may provide tectum opticum neurons with the visual scene information required for their function of controlling external attention.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. T. W. Cronin and R. H. Douglas, “Seeing and doing: how vision shapes animal behaviour,” Phil. Trans. R. Soc. B., 369 (2014).

  2. I. H. Bianco, A. R. Kampff, and F. Engert, “Prey capture behavior evoked by simple visual stimuli in larval zebrafish,” Front. Syst. Neurosci., 5, 10 (2011).

  3. T. W. Dunn, C. Gebhardt, E. A. Naumann, et al., “Neural circuits underlying visually evoked escapes in larval zebrafish,” Neuron, 89, 613–628 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. D. P. M. Northmore, “The optic tectum,” in: Encyclopedia of Fish Physiology: From Genome to Environment, A. P. Farrell (ed.), Elsevier, London (2011), pp. 131–142.

  5. A. D. Springer, S. S. Easter, and B. W. Agranoff, “The role of the optic tectum in various visually mediated behaviors of goldfish,” Brain Res., 128, 393–404 (1977).

    CAS  PubMed  Google Scholar 

  6. A. J. Barker and H. Baier, “Sensorimotor decision making in the zebrafish tectum,” Curr. Biol., 25, 2804–2814 (2015).

    CAS  PubMed  Google Scholar 

  7. W. I. Mangrum, J. E. Dowling, and E. D. Cohen, “A morphological classification of ganglion cells in the zebrafish retina,” Vis. Neurosci., 19, 767–779 (2002).

    PubMed  Google Scholar 

  8. E. Robles, A. Filosa, and H. Baier, “Precise lamination of retinal axons generates multiple parallel input pathways in the tectum,” J. Neurosci., 33, 5027–5039 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. J. E. Cook, D. L. Becker, and R. Kapila, “Independent mosaics of large inner-and outer-stratified ganglion cells in the goldfish retina,” J. Comp. Neurol., 318, 355–366 (1992).

    CAS  PubMed  Google Scholar 

  10. J. E. Cook, T. A. Podugolnikova, and S. L. Kondrashev, “Speciesdependent variation in the dendritic stratification of apparently homologous retinal ganglion cell mosaics in two neoteleost fishes,” Vision Res., 39, 2615–2631 (1999).

    CAS  PubMed  Google Scholar 

  11. G. D. Field and E. J. Chichilnisky, “Information processing in the primate retina: Circuitry and coding,” Annu. Rev. Neurosci., 30, 1–30 (2007).

    CAS  PubMed  Google Scholar 

  12. R. H. Masland, “The neuronal organization of the retina,” Neuron, 76, 266–280 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. J. Johnston and L. Lagnado, “What the fish’s eye tells the fish’s brain,” Neuron, 76, 257–259 (2012).

    CAS  PubMed  Google Scholar 

  14. E. Robles, E. Laurell, and H. Baier, “The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity,” Curr. Biol., 24, 2085–2096 (2014).

    CAS  PubMed  Google Scholar 

  15. M. Jacobson and R. M. Gaze, “Types of visual response from single units in the optic tectum and optic nerve of the goldfish,” Q. J. Exp. Physiol., 49, 199–209 (1964).

    CAS  PubMed  Google Scholar 

  16. N. Nikolaou, A. S. Lowe, A. S. Walker, et al., “Parametric functional maps of visual inputs to the tectum,” Neuron, 76, 317–324 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. V. Kassing, G. Engelman, and R. Kurtz, “Monitoring of single-cell responses in the optic tectum of adult zebrafish with dextran-coupled calcium dyes delivered via local electroporation,” PLoS One, 8, e62846 (2013).

  18. S. J. Preuss, C. A. Triverdi, C. M. Berg-Maurer, et al., “Classification of object size in retinotectal microcircuits,” Curr. Biol., 24, 2376–2385 (2014).

    CAS  PubMed  Google Scholar 

  19. G. M. Zenkin and I. N. Pigarev, “Detector properties of the ganglion cells of the pike retina,” Biofizika, 14, 763–772 (1969).

    Google Scholar 

  20. E. M. Maximova, O. Yu. Orlov, and A. M. Dimentman, “Studies of the visual system in various marine fish species,” Vopr. Ikhtiol., 11, 893–899 (1971).

    Google Scholar 

  21. A. T. Aliper, A. A. Zaichikova, I. Damjanović, et al., “Updated functional segregation of retinal ganglion cell projections in the tectum of a cyprinid fish – Further elaboration based on microelectrode recordings,” Fish Physiol. Biochem., 45, 773–792 (2019).

    CAS  PubMed  Google Scholar 

  22. E. M. Maximova, A. T. Aliper, I. Damjanović, et al., “On the organization of receptive fields of retinal spot detectors projecting to the fish tectum: Analogies with the local edge detectors in frogs and mammals,” J. Comp. Neurol., 528, No. 8, pp. 1423–1435 (2020), https://doi.org/10.1002/cne.24824.

    Article  PubMed  Google Scholar 

  23. S. P. Mysore and E. I. Knudsen, “The role of a midbrain network in competitive stimulus selection,” Curr. Opin. Neurobiol., 21, 653–660 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. R. J. Krauzli, L. P. Lovejoy, and A. Zéno, “Superior colliculus and visual spatial attention,” Annu. Rev. Neurosci., 36, 165–182 (2013).

    Google Scholar 

  25. D. Sridharan, J. S. Schwarz, and E. I. Knudsen, “Selective attention in birds,” Curr. Biol., 24, R510–R513 (2014).

    CAS  PubMed  Google Scholar 

  26. M. Ben-Tov, O. Donchin, O. Ben-Shahar, and R. Segev, “Pop-out in visual search of moving targets in the archer fish,” Nat. Commun., 6, 1–11 (2015).

    Google Scholar 

  27. A. A. Kardamakis, K. Saitoh, and S. Grillner, “Tectal microcircuit generating visual selection commands on gaze-controlling neurons,” Proc. Natl. Acad. Sci. USA, 112, E1956–E1965 (2015).

    CAS  PubMed  Google Scholar 

  28. L. Zhaoping, “From the optic tectum to the primary visual cortex: Migration through evolution of the saliency map for exogenous attentional guidance,” Curr. Opin. Neurobiol., 40, 94–102 (2016).

    CAS  PubMed  Google Scholar 

  29. I. H. Bianco and F. Engert, “Visuomotor transformations underlying hunting behavior in zebrafish,” Curr. Biol., 25, 831–846 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. D. A. Neave, “The development of visual acuity in larval plaice (Pleuronectes platessa L.) and turbot (Scophthalmus maximus L.),” J. Exp. Mar. Biol. Ecol., 78, 167–175 (1984).

  31. S. Schaerer and C. Neumeyer, “Motion detection in goldfish investigated with the optomotor response is color blind”,” Vision Res., 36, 4025–4034 (1996).

  32. A. P. Dobberfuhl, J. F. P. Ullmann, and C. A. Shumway, “Visual acuity, environmental complexity, and social organization in African cichlid fishes,” Behav. Neurosci., 119, 1648–1655 (2005).

    PubMed  Google Scholar 

  33. M. F. Haug, O. Biehlmaier, K. P. Mueller, and S. C. F. Neuhauss, “Visual acuity in larval zebrafish: Behavior and histology,” Front. Zool., 7, 8 (2010).

    PubMed  PubMed Central  Google Scholar 

  34. V. V. Maximov, E. M. Maximova, and P. V. Maximov, “Direction selectivity in the goldfish tectum revisited,” Ann. N. Y. Acad. Sci., 1048, 198–205 (2005).

    PubMed  Google Scholar 

  35. I. Damjanović, E. M. Maximova, and V. V. Maximov, “On the organization of receptive fields of orientation-selective units recorded in the fish tectum,” J. Integr. Neurosci., 8, 323–344 (2009).

    PubMed  Google Scholar 

  36. V. V. Maximov, E. M. Maximova, I. Damjanović, and P. V. Maximov, “Detection and resolution of drifting gratings by motion detectors in the fish retina,” J. Integr. Neurosci., 12, 117–143 (2013).

    PubMed  Google Scholar 

  37. A. T. Aliper, “Receptive field size in spontaneously activity ganglion cells in the Prussian carp retina,” Sens. Sistemy, 32, 8–13 (2018).

    Google Scholar 

  38. V. V. Maximov, E. M. Maximova, and P. V. Maximov, “Classification of directionally selective elements recorded in the Prussian carp tegmentum,” Sens. Sistemy, 19, 322–335 (2005).

    Google Scholar 

  39. I. Damjanović, E. M. Maximova, and V. V. Maximov, “Receptive field sizes of direction-selective units in the fish tectum,” J. Integr. Neurosci., 8, 77–93 (2009).

    PubMed  Google Scholar 

  40. P. V. Maximov and V. V. Maximov, “A hardware-software complex for electrophysiological studies of the fish visual system,” in: Abstr. Int. Symp. Ivan Djaja’s (Jaen Giaja) Belgrade School of Physiology, Belgrade, Serbia (2010).

  41. R. C. Gesteland, B. Howland, J. Y. Lettvin, and W. H. Pitts, “Comments on microelectrodes,” Proc. IRE, 47, 1856–1862 (1959).

    Google Scholar 

  42. C. Neumeyer, “Tetrachromatic color vision in goldfish. Evidence from color mixture experiments,” J. Comp. Physiol. A., 171, 639–649 (1992).

    Google Scholar 

  43. E. F. MacNichol, Jr., “A unifying presentation of photopigment spectra,” Vision Res., 26, 1543–1556 (1986).

    CAS  PubMed  Google Scholar 

  44. V. I. Govardovskii, N. Fyhrquist, T. Reuter, D. G. Kuzmin, and K. Donner, “In search of the visual pigment template,” Vis. Neurosci., 17, 509–28 (2000).

    CAS  PubMed  Google Scholar 

  45. E. M. Maximova, V. I. Govardovskii, P. V. Maximov, and V. V. Maximov, “Spectral sensitivity of direction-selective ganglion cells in the fish retina,” Ann. N. Y. Acad. Sci., 1048, 433–434 (2005).

    PubMed  Google Scholar 

  46. G. Svaetichin and E. F. MacNichol, Jr., “Retinal mechanisms for chromatic and achromatic vision,” Ann. N. Y. Acad. Sci., 74, 385–404 (1958).

    Google Scholar 

  47. E. F. MacNichol, Jr., M. L. Wolbarsht, and H. G. Wagner, “Electrophysiological evidence for a mechanism of color vision in the goldfish,” in: Light and Life, W. D. McElroy and B. Glass (eds.), Johns Hopkins Press, Baltimore (1961), pp. 795–814.

  48. E. F. MacNichol, Jr., “Three-pigment color vision,” Sci. Am., 211, 48–56 (1964).

    PubMed  Google Scholar 

  49. O. Yu. Orlov and E. M. Maximova, “S-potential sources as excitation pools,” Vision Res., 5, 573–582 (1965).

    CAS  PubMed  Google Scholar 

  50. G. Mitarai, “Chromatic properties of S-potentials in fish,” in: The S-Potential, B. D. Drujan and M. Laufer (eds.), Liss, New York (1982), pp. 137–150.

  51. W. K. Stell, R. Kretz, and D. O. Lightfoot, “Horizontal cell connectivity in goldfish,” in: The S-Potential, B. D. Drujan and M. Laufer (eds.), Liss, New York (1982), pp. 51–75.

  52. Y. N. Li, J. I. Matsui, and J. E. Dowling, “Specificity of the horizontal cell-photoreceptor connections in the zebrafish (Danio rerio) retina,” J. Comp. Neurol., 516, 442–453 (2009).

    PubMed  PubMed Central  Google Scholar 

  53. A. Meier, R. Nelson, and V. P. Connaughton, “Color processing in zebrafish retina,” Front. Cell. Neurosci., 12, 327 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. V. V. Maximov, E. M. Maximova, I. Damjanović, and P. V. Maximov, “Color properties of the motion detectors projecting to the goldfish tectum: I. A color matching study,” J. Integr. Neurosci., 13, 465–484 (2014).

    PubMed  Google Scholar 

  55. V. V. Maximov, E. M. Maximova, I. Damjanović, et al., “Color properties of the motion detectors projecting to the goldfish tectum: II. Selective stimulation of different chromatic types of cones,” J. Integr. Neurosci., 14, 31–52 (2015).

    PubMed  Google Scholar 

  56. E. M. Maximova, P. V. Maximov, I. Damjanović, et al., “Color properties of the motion detectors projecting to the goldfish tectum: III. Color-opponent interactions in the receptive field,” J. Integr. Neurosci., 14, 441–454 (2015).

    Google Scholar 

  57. P. V. Maximov, A. T. Aliper, and E. M. Maximova, “Colour-specific responses of the goldfish retinal ganglion cells revealed by cone-isolated visual stimulation,” in: Abstr. 25th Symp. Int. Colour Vision Society, Riga, Latvia (2019).

  58. A. L. Byzov, “Retinal horizontal cells as regulators of synaptic transmission,” Ros. Fiziol. Zh., 53, 1115–1123 (1967).

    CAS  Google Scholar 

  59. E. M. Maximova, “Effect of intracellular polarization of horizontal cells on the activity of the ganglion cells in the fish retina,” Biofizika, 14, 537–544 (1969).

    Google Scholar 

  60. M. Kamermans, B. W. Vandijk, and H. Spekreijse, “Color opponency in cone-driven horizontal cells in carp retina – aspecific pathways between cones and horizontal cells,” J. Gen. Physiol., 97, 819–843 (1991).

    CAS  PubMed  Google Scholar 

  61. J. Y. Lettvin, H. R. Maturana, W. S. McCulloch, and W. H. Pitts, “What frog’s eye tells to the frog’s brain,” Proc. IRE, 47, 1940–1951 (1959).

    Google Scholar 

  62. D. J. Margolis and P. B. Detwiler, “Different mechanisms generate maintained activity in ON and OFF retinal ganglion cells,” J. Neurosci., 27, 5994–6005 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. B. Krieger, M. Qiao, D. L. Rousso, et al., “Four alpha ganglion cell types in mouse retina: Function, structure, and molecular signatures,” PLoS One, 12, e0180091 (2017).

  64. V. Maximov, O. Orlov, and T. Reuter, “Chromatic properties of the retinal afferents in the thalamus and the tectum of the frog (Rana temporaria),” Vision Res., 25, 1037–1049 (1985).

    CAS  PubMed  Google Scholar 

  65. N. W. Daw, “Goldfish retina: organization for simultaneous color contrast,” Science, 58, 942–944 (1967).

    Google Scholar 

  66. E. M. Maximova, A. M. Dimentman, V. V. Maximov, et al., “The physiological mechanisms of color constancy,” Neirofiziologiia, 7, 16–20 (1975).

    Google Scholar 

  67. J. R. Cronly-Dillon, “Units sensitive to direction of movement in goldfish tectum,” Nature, 203, 214–215 (1964).

    CAS  PubMed  Google Scholar 

  68. B. Liège and G. Galand, “Types of single-unit visual responses in the trout’s optic tectum,” in: Visual Information Processing and Control of Motor Activity, A. Gudikov (ed.), Bulgarian Academy of Sciences Press, Sofia (1971), pp. 63–65.

  69. A. M. Granda and J. E. Fulbrook, “Classification of turtle retinal ganglion cells,” J. Neurophysiol, 62, 723–737 (1989).

    CAS  PubMed  Google Scholar 

  70. B. J. O’Brien, T. Isayama, and D. M. Berson, “Light responses of morphologically identified cat ganglion cells,” Invest. Ophthalmol. Vis. Sci., 40, ARVO Abstract 815 (1999).

  71. M. van Wyk, W. R. Taylor, and D. I. Vaney, “Local edge detectors: A substrate for fine spatial vision at low temporal frequencies in rabbit retina,” J. Neurosci., 26, 13,250–13,263 (2006).

    Google Scholar 

  72. S. Venkataramani and W. R. Taylor, “Orientation selectivity in rabbit retinal ganglion cells is mediated by presynaptic inhibition,” J. Neurosci., 30, 15,664–15,676 (2010).

    CAS  Google Scholar 

  73. I. Damjanović, E. M. Maximova, A. T. Aliper, et al., “Opposing motion inhibits responses of direction-selective ganglion cells in the fish retina,” J. Integr. Neurosci., 14, 53–72 (2015).

    PubMed  Google Scholar 

  74. T. Baden, P. Berens, K. Franke, et al., “The functional diversity of retinal ganglion cells in mouse,” Nature, 529, 345–350 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. M. Maximova.

Additional information

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 106, No. 4, pp. 486–503, April, 2020.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maximova, E.M., Aliper, A.T., Damjanović, I.Z. et al. Ganglion Cells with Sustained Activity in the Fish Retina and Their Possible Function in Evaluation of Visual Scenes. Neurosci Behav Physi 51, 123–133 (2021). https://doi.org/10.1007/s11055-020-01047-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-020-01047-1

Keywords

Navigation