Direction selectivity of the retinotectal system of fish: findings based on microelectrode extracellular recordings of the tectum opticum
Keywords:tectum opticum, motion detectors, retinal direction-selective, direction-selective ganglion cells, direction-selective tectal neurons
- 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.
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.19126.96.36.1998
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.19188.8.131.523
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
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Copyright (c) 2023 Ilija Damjanović, Alexey Aliper, Paul Maximov, Alisa Zaichikova, Zoran Gačić, Elena Maximova
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