Direction selectivity of the retinotectal system of fish: findings based on microelectrode extracellular recordings of the tectum opticum

Authors

  • Ilija Damjanović Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  • Alexey Aliper Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  • Paul Maximov Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  • Alisa Zaichikova Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia
  • Zoran Gačić University of Belgrade, Institute for Multidisciplinary Research, Belgrade, Serbia
  • Elena Maximova Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, Russia

DOI:

https://doi.org/10.2298/ABS221216003D

Keywords:

tectum opticum, motion detectors, retinal direction-selective, direction-selective ganglion cells, direction-selective tectal neurons

Abstract

Paper description:

  • Fish are a convenient model for studying the visual system because of the common variety of visual pigments, regularity of the morphology of the retina, and structural plan of the brain’s visual centers.
  • An understanding of the mechanisms of the visual system and its development and its evolutionary aspect can be gained by combining data obtained using electrophysiology on adults, Ca2+ imaging on transparent larvae of Danio rerio, behavioral experiments and observations of visually guided behavior in the wild.
  • In this review article, our findings are compared with the results of authors examining direction selectivity in the fish retinotectal system.

Abstract: Vision in fish plays an important role in different forms of visually guided behavior. The visual system of fish is available for research by different methods; it is a convenient experimental model for studying and understanding the mechanisms of vision in general. Responses of retinal direction-selective (DS) ganglion cells (GCs) are recorded extracellularly from their axon terminals in the superficial layers of the tectum opticum (TO). They can be divided into three distinct groups according to the preferred directions of stimulus movement: caudorostral, dorsoventral and ventrodorsal. Each of these groups comprises both ON and OFF units in equal proportions. Relatively small receptive fields (3-8°) and fine spatial resolution characterize retinal DS units as local motion detectors. Conversely, the responses of direction-selective tectal neurons (DS TNs) are recorded at two different tectal levels, deeper than the zone of retinal DS afferents. They are characterized by large receptive fields (up to 60°) and are indifferent to any sign of contrast, i.e., they can be considered as ON-OFF-type units. Four types of ON-OFF DS TNs preferring different directions of motion have been recorded. The preferred directions of three types of DS TNs match the preferred directions of three types of DS GCs. Matching the three preferred directions of ON and OFF DS GCs and ON-OFF DS TNs has allowed us to hypothesize that the GCs with caudorostral, ventrodorsal and dorsoventral preferences are input neurons for the corresponding types of DS TNs. On the other hand, the rostrocaudal preference in the fourth type of DS TNs, recorded exclusively in the deep tectal zone, is an emergent property of the TO. In this review, our findings are compared with the results of other authors examining direction selectivity in the fish retinotectal system.

Downloads

Download data is not yet available.

References

Maximov VV, Maximova EM, Maximov PV. Direction selectivity in the goldfish tectum revisited. Ann NY Acad Sci. 2005;1048:198-205. https://doi.org/10.1196/annals.1342.018

Nikolaou N, Lowe AS, Walker AS, Abbas F, Hunter PR, Thompson ID, Meyer MP. Parametric functional maps of visual inputs to the tectum. Neuron. 2012;76:317-24. https://doi.org/10.1016/j.neuron.2012.08.040

Northmore DPM. The optic tectum. In: Farrell AP, editor. Encyclopedia of fish physiology: from genome to environment. London: Elsevier; 2011. p 131-42. https://doi.org/10.1111/j.1095-8649.2012.03269.x

Robles E, Laurell E, Baier H. The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity. Curr Biol. 2014;24:2085-96. https://doi.org/10.1016/j.cub.2014.07.080

Lettvin JY, Maturana, HR, McCulloch WS, Pitts, WH. What the frog's eye tells the frog's brain. Proc Inst Radiol Eng NY. 1959; 47:1940-51. https://doi.org/10.1109/JRPROC.1959.287207

Maturana HR, Lettvin JY, McCulloch WS, Pitts WH. Anatomy and physiology of vision in the frog. J Gen Physiol. 1960;43:129-75. https://doi.org/10.1085/jgp.43.6.129

Gesteland RC, Howland B, Lettvin JY, Pitts WH. Comments on microelectrodes. Proc Inst Radio. Eng NY. 1959;47:1856-62. https://doi.org/10.1109/JRPROC.1959.287156

Jacobson M, Gaze RM. Types of visual response from single units in the optic tectum and optic nerve of the goldfish. Q J Exp Physiol. 1964;49:199-209. https://doi.org/10.1113/expphysiol.1964.sp001720

Cronly-Dillon JR. Units sensitive to direction of movement in goldfish tectum. Nature. 1964;203:214-5. https://doi.org/10.1038/203214a0

Liege B, Galand G. Types of single-unit visual responses in the trout's optic tectum. In: Gudikov A editor. Visual Information Processing and Control of Motor Activity. Sofia: Bulgarian Academy of Sciences; 1971. p. 63-5.

Maximova EM, Orlov OYu, Dimentnman AM. Investigation of visual system of some marine fishes. Voprocy Ichtiologii. 1971; 11:893-9. Russian.

Maximova EM, Dimentman AM, Maximov VV, Nikolayev PP, Orlov OY. The physiological mechanisms of colour constancy. Neirofiziologiya. 1975;7:21-6. Russian. https://doi.org/10.1007/BF01063019

Wartzok D, Marks WB. Directionally selective visual units recorded in optic tectum of the goldfish. J Neurophysiol. 1973;36:588-604. https://doi.org/10.1152/jn.1973.36.4.588

Zenkin GM, Pigarev IN. Detector properties of the ganglion cells of the pike retina. Biofizika. 1969;14:722-30. Russian.

Maximova EM, Maximov VV. Detectors of the oriented lines in the visual system of the fish Carassius carassius. J Evol Biochem Phys. 1981;17:519-25. Russian.

Maximov VV, Maximova EM, Maximov PV. Classification of direction-selective units recorded in the goldfish tectum. Sensornye Sistemy. 2005b;19:322-35. Russian.

Barlow HB, Levick WR. The mechanism of directionally selective units in rabbit's retina. J Physiol. 1965;178:477-504. https://doi.org/10.1113/jphysiol.1965.sp007638

Borst A, Euler T. Seeing things in motion: models, circuits, and mechanisms. Neuron. 2011;71:974-94. https://doi.org/10.1016/j.neuron.2011.08.031

Vaney DI, Sivyer DI, Taylor WR. Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci. 2012;13:194-208. https://doi.org/10.1038/nrn3165

Oyster CW, Barlow HB. Direction-selective units in rabbit retina: Distribution of preferred directions. Science. 1967; 155:841-2. https://doi.org/10.1126/science.155.3764.841

Briggman KL, Helmstaedter M, Denk W. Wiring specificity in the direction-selectivity circuit of the retina. Nature. 2011;471:183-8. https://doi.org/10.1038/nature09818

Damjanović I, Maximova EM, Aliper AT, Maximov PV, Maximov VV. Opposing motion inhibits responses of direction-selective ganglion cells in the fish retina. J Integr Neurosci. 2015;14:53-72. https://doi.org/10.1142/S0219635215500077

Damjanović I, Maximova EM, Maximov VV. Receptive field sizes of direction-selective units in the fish tectum. J Integr Neurosci. 2009;8:77-93. https://doi.org/10.1142/S021963520900206X

Maximov VV, Maximova EM, Damjanović I, Maximov PV. Detection and resolution of drifting gratings by motion detectors in the fish retina. J Integr Neurosci. 2013;12:117-43. https://doi.org/10.1142/S0219635213500015

Maximova EM, Govardovskii VI, Maximov PV, Maximov VV. Spectral sensitivity of direction-selective ganglion cells in the fish retina. Ann NY Acad Sci. 2005;1048:433-4.

Maximova EM, Levichkina EV, Utina IA. Morphology of putative direction-selective ganglion cells traced with Dii in the fish retina. Senssornye Sistemy. 2006;20:279-87. Russian.

Oyster CW, Takahashi E, Collewijn H. Direction-selective retinal ganglion cells and control of optokinetic nystagmus in the rabbit. Vision Res. 1972; 12:183-93. https://doi.org/10.1016/0042-6989(72)90110-1

Wyatt HJ, Daw NW. Directionally sensitive ganglion cells in the rabbit retina: Specificity for stimulus direction, size, and speed. J Neurophysiol. 1975;38:613-26. https://doi.org/10.1152/jn.1975.38.3.613

Grzywacz NM, Amthor FR. Robust directional computation in on-off irectionally selective ganglion cells of rabbit retina. Vis Neurosci. 2007;24:647-61. https://doi.org/10.1017/S0952523807070666

Lee S, Kim K, Zhou ZJ. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron. 2010;68:1159-72. https://doi.org/10.1016/j.neuron.2010.11.031

Brandon C. Cholinergic amacrine neurons of the dogfish retina. Vis Neurosci. 1991;6:553-62. https://doi.org/10.1017/s0952523800002534

Yazulla S, Studholme KM. Neurochemical anatomy of the zebrafish retina as determined by immunocytochemistry. J Neurocyt. 2001;30:551-92. https://doi.org/10.1023/A:1016512617484

Arenzana FJ, Clemente D, Sánchez-González, R, Porteros A, Aijόn J, Arévalo, R. Development of the cholinergic system in the brain and retina of the zebrafish. Brain Res Bull. 2005;66:421-5. https://doi.org/10.1016/j.brainresbull.2005.03.006

Tauchi M, Masland RH. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc R Soc Lond B Biol Sci. 1984;223:101-19. http://doi.org/10.1098/rspb.1984.0085

Masland RH, Mills JW, Hayden SA. Acetylcholine-synthesizing amacrine cells: Identification and selective staining by using radioautography and fluorescent markers. Proc R Soc Lond B Biol Sci. 1984;223:79-100. https://doi.org/10.1098/rspb.1984.0084

Vaney DI, Young HM. GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res. 1988;438:369-73. https://doi.org/10.1016/0006-8993(88)91366-2

Masland RH. The neuronal organization of the retina. Neuron. 2012;76:266-80. https://doi.org/10.1016/j.neuron.2012.10.002

Matsumoto A, Agbariah W, Solveig Nolte S, Andrawos R, Levi H, Sabbah S, Yonehara K. Direction selectivity in retinal bipolar cell axon terminals. Neuron. 2021;109:1-15. https://doi.org/10.1016/j.neuron.2021.11.004

Maximov VV, Maximova EM, Maximov PV. Classification of orientation-selective units recorded in the goldfish tectum. Sensornye Sistemy. 2009;23:13-23. Russian.

Damjanović I, Maximova EM, Maximov VV. On the organization of receptive fields of orientation-selective units recorded in the fish tectum. J Integr Neurosci. 2009;8:323-44. https://doi.org/10.1142/S0219635209002174

Aliper AT, Zaichikova AA, Damjanović I, Maximov PV, Kasparson AA, Gačić Z, Maximova EM. Updated functional segregation of retinal ganglion cell projections in the tectum of a cyprinid fishFurther elaboration based on microelectrode recordings. Fish Physiol Biochem. 2019;45:773-92. https://doi.org/10.1007/s10695-018-0603-0

Maximova EM, Aliper AT, Damjanović I, Zaichikova AA, Maximov PV. 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. 2020;528:1423-35. https://doi.org/10.1002/cne.24824

Nevin LM, Robles E, Baier H, Scot EK. Focusing on optic tectum circuitry through the lens of genetics. BMC Biol. 2010;8:126. https://doi.org/10.1186/1741-7007-8-126

Robles E, Smith SJ, Baier H. Characterization of genetically targeted neuron types in the zebrafish optic tectum. Front Neural Circuit. 2011;5:1. https://doi.org/10.3389/fncir.2011.00001

Robles E, Filosa A, Baier H. Precise lamination of retinal axons generates multiple parallel input pathways in the tectum. J Neurosci. 2013; 33:5027-39. https://doi.org/10.1523/JNEUROSCI.4990-12.2013

Abbas F, Triplett MA, Goodhill GJ, Meyer MP. 2017. A three-layer network model of direction selective circuits in the optic tectum. Front Neural Circuits. 2017;11:88. https://doi.org/10.3389/fncir.2017.00088

Damjanović I. Direction selective units in goldfish retina and tectum opticum - review and new aspects. J Integr Neurosci. 2015;14:535-56. https://doi.org/10.1142/S0219635215300024

Damjanović I, Maximov PV, Aliper AT, Zaichikova AA, Gačić Z, Maximova EM. Putative targets of direction-selective retinal ganglion cells in the tectum opticum of cyprinid fish. Brain Res. 2019;1708:20-6. https://doi.org/10.1016/j.brainres.2018.12.006

Maximova EM, Pushchin II, Maximov PV, Maximov VV. Presynaptic and postsynaptic single-unit responses in the goldfish tectum as revealed by a reversible synaptic transmission blocker. J Integr Neurosci. 2012;11:183-91. https://doi.org/10.1142/S0219635212500136

O'Benar JD. Electrophysiology of neural units in goldfish optic tectum. Brain Res Bull. 1976:1:529-41. https://doi.org/10.1016/0361-9230(76)90080-0

Daw NW. Color coded units in the goldfish retina (PhD thesis). Baltimore: The Johns Hopkins University; 1967.

Bilotta J, Abramov I. Orientation and direction tuning of goldfish ganglion cells. Visual Neurosci. 1989;2:3-13. https://doi.org/10.1017/s0952523800004260

Tsvilling V, Donchin O, Shamir M, Segev R. Archer fish fast hunting maneuver may be guided by directionally selective retinal ganglion cells. Eur J Neurosci. 2012;35:436-44. https://doi.org/10.1111/j.1460-9568.2011.07971.x.

Zaichikova A, Damjanović I, Maximov P, Aliper A, Maximova E. Neurons in the optic tectum of fish: Electrical activity and selection of appropriate stimulation. Neurosci Behav Physiol. 2021;51:993-1001. https://doi.org/10.1007/s11055-021-01157-4

Grama A, Engert F. Direction selectivity in the larval zebrafish tectum is mediated by asymmetric inhibition. Front Neural Circuit. 2012;6:59. https://doi.org/10.3389/fncir.2012.00059

Gabriel JP, Triverdi CA, Maurer CM, Ryu C, Bollman JH. Layer-specific targeting of direction-selective neurons in the zebrafish tectum opticum. Neuron. 2012;76:1147-60. https://doi.org/10.1016/j.neuron.2012.12.003

Gebhardt C, Baier H, Del Bene F. Direction selectivity in the visual system of the zebrafish arva. Front. Neural Circuit. 2013;7:111. https://doi.org/10.3389/fncir.2013.00111

Hunter PR, Lowe AS, Thompson I, Meyer MP. Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity. J Neurosci. 2013;33:13940-5. https://doi.org/10.1523/JNEUROSCI.1493-13.2013

Barker AJ, Baier H. SINs and SOMs: neural microcircuits for size tuning in the zebrafish and mouse visual pathway. Front Neural Circuit. 2013;7:89. https://doi.org/10.3389/fncir.2013.00089

Downloads

Published

2023-04-03

How to Cite

1.
Damjanović I, Aliper A, Maximov P, Zaichikova A, Gačić Z, Maximova E. Direction selectivity of the retinotectal system of fish: findings based on microelectrode extracellular recordings of the tectum opticum. Arch Biol Sci [Internet]. 2023Apr.3 [cited 2024Jun.19];75(1):27-45. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/8241

Issue

Section

Articles