In all animals the optic tectum (OT) (or superior colliculi in mammals) provides guidance for external attention; this is not the only function of the tectum but is critically important for the development of behavioral visual reactions. In fish, the OT is the main primary visual center. It receives signals from most ganglion cells (GC) of different (known) types in the retina. Knowledge of the properties – both structural and physiological – of the neurons in the OT is important for understanding the mechanisms organizing behavior. We recorded extracellular electrical activity in the OT in living adult fish (Carassius auratus gibelio). Simultaneous recordings were made of the responses of retinal GC (from their axon terminals) and tectal neurons (TN), probably from cell bodies. Four types of TN are described with directional selectivity (DS) (henceforth these neurons are termed DS TN) at different (defined) depths of the OT. In addition to these, rare sporadic spikes lacking DS and arising on stimulation at any locus in a large area were consistently recorded simultaneously (superficially) with the responses of caudorostral DS GC with the electrode in one position. These are presumptively the responses of superficial tectal neurons (superficial inhibitory neurons, SIN). Various different types of stimulation were applied with the aim of obtaining clear SIN responses. Comparison of the results of our electrophysiological studies with published data (most studies in this direction have used calcium imaging in transparent Danio rerio fry) showed that DS TN were identical to glutamatergic periventricular interneurons in the OT, while SIN were identical to GABAergic inhibitory interneurons (SIN). These latter presumptively mediate detection of the main object (pop-out) in the field of vision.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aliper, A. T., Zaichikova, A. A., Damjanović, I., 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, No. 2, 773–792 (2019).
Barker, A. J. and Baier, H., “Sensorimotor decision making in the zebrafish tectum,” Curr. Biol., 25, No. 21, 2804–2814 (2015).
Barker, A. J. and Baier, H., “SINs and SOMs: neural microcircuits for size tuning in the zebrafish and mouse visual pathway,” Front. Neural Circ., 7, 89 (2013).
Bene, F. Del, Wyart, C., et al., “Filtering of visual information in the tectum by an identified neural circuit,” Science, 330, No. 6004, 669–673 (2010).
Ben-Tov, M., Donchin, O., Ben-Shahar, O., and Segev, R., “Pop-out in visual search of moving targets in the archer fish,” Nat. Commun., 6, No. 1, 1–11 (2015).
Damjanović, I., Maximov, P., Aliper, A., et al., “Putative targets of direction- selective retinal ganglion cells in the tectum opticum of cyprinid fish,” Brain Res., 1708, 20–26 (2019).
Damjanović, I., Maximova, E. M., and Maximov, V. V., “On the organization of receptive fields of orientation-selective units recorded in the fish tectum,” J. Integr. Neurosci., 8, 323–344 (2009).
Gabriel, J. P., Trivedi, C. A., Maurer, C. M., et al., “Layer-specific targeting of direction-selective neurons in the zebrafish optic tectum,” Neuron, 76, No. 6, 1147–1160 (2012).
Gesteland, R. C., Lettvin, J. Y., Howland, B., et al., “Comments on microelectrodes,” Proc. IRE, 47, No. 11, 1856–1862 (1959).
Grama, A. and Engert, F., “Direction selectivity in the larval zebrafish tectum is mediated by asymmetric inhibition,” Front. Neural Circ., 4, No. 6, 59 (2012).
Hunter, P. R., Lowe, A. S., Thompson, I. D., and Meyer, M. P., “Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity,” J. Neurosci., 33, No. 35, 13940– 13945 (2013).
Kardamakis, A. A., Saitoh, K., and Grillner, S., “Tectal microcircuit generating visual selection commands on gaze-controlling neurons,” Proc. Natl. Acad. Sci. USA, 112, No. 15, E1956–E1965 (2015).
Kinoshita, M. and Ito, E., “Roles of periventricular neurons in retinotectal transmission in the optic tectum,” Prog. Neurobiol., 79, No. 2, 112–121 (2006).
Lazareviċ, L., Rogač, L., and Rakiċ, L., “Cytoarchitectonic analysis of tectum opticum in Serranus scriba,” Iugosl. Physiol. Pharmacol. Acta, 34, No. 2, 335–341 (1998).
Maximov, V. V., Maximova, E. M., and Maximov, P. V., “ Classification of directionally selective elements projecting to the tectum in Prussian carp,” Sens. Sistemy, 23, No. 1, 13–23 (2009).
Maximov, V. V., Maximova, E. M., and Maximov, P. V., “Classification of directionally selective elements recorded in the Prussian carp tectum,” Sens. Sistemy, 19, No. 4, 322–335 (2005a).
Maximov, V. V., Maximova, E. M., and Maximov, P. V., “Direction selectivity in the goldfish tectum revisited,” Ann. N.Y. Acad. Sci., 1048, 198–205 (2005b).
Maximova, E., Pushchin, I., Maximov, P., and Maximov, V., “Presynaptic and postsynaptic single-unit responses in the goldfish tectum as revealed by a reversible synaptic transmission blocker,” J. Integr. Neurosci., 11, No. 2, 183–191 (2012).
Nevin, L. M., Robles, E., Baier, H., and Scott, E. K., “Focusing on optic tectum circuitry through the lens of genetics,” BMC Biol., 8, No. 1, 126 (2010).
Nikolaou, N. and Meyer, M. P., “Lamination speeds the functional development of visual circuits,” Neuron, 88, No. 5, 999–1013 (2015).
Nikolaou, N., Lowe, A. S., Walker, A. S., et al., “Parametric functional maps of visual inputs to the tectum,” Neuron, 76, No. 2, 317–324 (2012).
Northmore, D. P. M., “The optic tectum,” in: Encyclopedia of Fish Physiology: From Genome to Environment, Farrell, A. P. (eds.), Elsevier (2011), pp. 131–142.
Preuss, S. J., Trivedi, C. A., Vom Berg-Maurer, C. M., et al., “Classification of object size in retinotectal microcircuits,” Curr. Biol., 24, No. 20, 2376–2385 (2014).
Robles, E., Filosa, A., and Baier, H., “Precise lamination of retinal axons generates multiple parallel input pathways in the tectum,” J. Neurosci., 33, No. 11, 5027–5039 (2013).
Robles, E., Smith, S. J., and Baier, H., “Characterization of genetically targeted neuron types in the zebrafish optic tectum,” Front. Neural Circ., 5, No. 1 (2011).
Walker, A. S., Burrone, J., and Meyer, M. P., “Functional imaging in the zebrafish retinotectal system using RGECO,” Front. Neural Circ., 7, 34 (2013).
Yin, C., Li, X., and Du, J., “Optic tectal superficial interneurons detect motion in larval zebrafish,” Protein Cell, 10, 238–248 (2019).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Sensornye Sistemy, Vol. 35, No. 1, pp. 11–21, January–March, 2021.
Rights and permissions
About this article
Cite this article
Zaichikova, A.A., Damjanović, I., Maximov, P.V. et al. Neurons in the Optic Tectum of Fish: Electrical Activity and Selection of Appropriate Stimulation. Neurosci Behav Physi 51, 993–1001 (2021). https://doi.org/10.1007/s11055-021-01157-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11055-021-01157-4