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.
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T. W. Cronin and R. H. Douglas, “Seeing and doing: how vision shapes animal behaviour,” Phil. Trans. R. Soc. B., 369 (2014).
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).
T. W. Dunn, C. Gebhardt, E. A. Naumann, et al., “Neural circuits underlying visually evoked escapes in larval zebrafish,” Neuron, 89, 613–628 (2016).
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.
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).
A. J. Barker and H. Baier, “Sensorimotor decision making in the zebrafish tectum,” Curr. Biol., 25, 2804–2814 (2015).
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).
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).
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).
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).
G. D. Field and E. J. Chichilnisky, “Information processing in the primate retina: Circuitry and coding,” Annu. Rev. Neurosci., 30, 1–30 (2007).
R. H. Masland, “The neuronal organization of the retina,” Neuron, 76, 266–280 (2012).
J. Johnston and L. Lagnado, “What the fish’s eye tells the fish’s brain,” Neuron, 76, 257–259 (2012).
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).
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).
N. Nikolaou, A. S. Lowe, A. S. Walker, et al., “Parametric functional maps of visual inputs to the tectum,” Neuron, 76, 317–324 (2012).
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).
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).
G. M. Zenkin and I. N. Pigarev, “Detector properties of the ganglion cells of the pike retina,” Biofizika, 14, 763–772 (1969).
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).
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).
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.
S. P. Mysore and E. I. Knudsen, “The role of a midbrain network in competitive stimulus selection,” Curr. Opin. Neurobiol., 21, 653–660 (2011).
R. J. Krauzli, L. P. Lovejoy, and A. Zéno, “Superior colliculus and visual spatial attention,” Annu. Rev. Neurosci., 36, 165–182 (2013).
D. Sridharan, J. S. Schwarz, and E. I. Knudsen, “Selective attention in birds,” Curr. Biol., 24, R510–R513 (2014).
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).
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).
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).
I. H. Bianco and F. Engert, “Visuomotor transformations underlying hunting behavior in zebrafish,” Curr. Biol., 25, 831–846 (2015).
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).
S. Schaerer and C. Neumeyer, “Motion detection in goldfish investigated with the optomotor response is color blind”,” Vision Res., 36, 4025–4034 (1996).
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).
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).
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).
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).
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).
A. T. Aliper, “Receptive field size in spontaneously activity ganglion cells in the Prussian carp retina,” Sens. Sistemy, 32, 8–13 (2018).
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).
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).
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).
R. C. Gesteland, B. Howland, J. Y. Lettvin, and W. H. Pitts, “Comments on microelectrodes,” Proc. IRE, 47, 1856–1862 (1959).
C. Neumeyer, “Tetrachromatic color vision in goldfish. Evidence from color mixture experiments,” J. Comp. Physiol. A., 171, 639–649 (1992).
E. F. MacNichol, Jr., “A unifying presentation of photopigment spectra,” Vision Res., 26, 1543–1556 (1986).
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).
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).
G. Svaetichin and E. F. MacNichol, Jr., “Retinal mechanisms for chromatic and achromatic vision,” Ann. N. Y. Acad. Sci., 74, 385–404 (1958).
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.
E. F. MacNichol, Jr., “Three-pigment color vision,” Sci. Am., 211, 48–56 (1964).
O. Yu. Orlov and E. M. Maximova, “S-potential sources as excitation pools,” Vision Res., 5, 573–582 (1965).
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.
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.
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).
A. Meier, R. Nelson, and V. P. Connaughton, “Color processing in zebrafish retina,” Front. Cell. Neurosci., 12, 327 (2018).
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).
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).
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).
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).
A. L. Byzov, “Retinal horizontal cells as regulators of synaptic transmission,” Ros. Fiziol. Zh., 53, 1115–1123 (1967).
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).
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).
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).
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).
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).
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).
N. W. Daw, “Goldfish retina: organization for simultaneous color contrast,” Science, 58, 942–944 (1967).
E. M. Maximova, A. M. Dimentman, V. V. Maximov, et al., “The physiological mechanisms of color constancy,” Neirofiziologiia, 7, 16–20 (1975).
J. R. Cronly-Dillon, “Units sensitive to direction of movement in goldfish tectum,” Nature, 203, 214–215 (1964).
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.
A. M. Granda and J. E. Fulbrook, “Classification of turtle retinal ganglion cells,” J. Neurophysiol, 62, 723–737 (1989).
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).
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).
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).
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).
T. Baden, P. Berens, K. Franke, et al., “The functional diversity of retinal ganglion cells in mouse,” Nature, 529, 345–350 (2016).
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Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 106, No. 4, pp. 486–503, April, 2020.
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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
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DOI: https://doi.org/10.1007/s11055-020-01047-1