Updated functional segregation of retinal ganglion cell projections in the tectum of a cyprinid fish—further elaboration based on microelectrode recordings

  • Alexey T. Aliper
  • Alisa A. Zaichikova
  • Ilija Damjanović
  • Paul V. Maximov
  • Anna A. Kasparson
  • Zoran GačićEmail author
  • Elena M. Maximova


Single-unit responses of retinal ganglion cells (GCs) were recorded extracellularly from their axonal terminals in the tectum opticum (TO) of the intact fish (goldfish, carp). The depths of retinal units consecutively recorded along the track of the microelectrode were measured. At the depth of around 50 μm, the responses of six types of direction-selective (DS) GCs were regularly recorded. Responses of two types of orientation-selective (OS) GCs and detectors of white and black spots occurred approximately 50 μm deeper. Responses of GCs with dark- and light-sustained activity were recorded deeper than all others, at about 200 μm. The receptive fields of consecutively recorded units overlap, so they analyze the same fragment of the visual scene, focused by eye optic on the photoreceptor raster. The responses of pairs of DS GCs (ON and OFF units that preferred same direction of stimulus movement) and OS GCs (detectors of vertical and horizontal lines) were often simultaneously recorded at one position of the microelectrode. (The paired recordings of certain units amounted about fourth part of all recordings.) This suggests that their axonal arborizations are located close to each other in the tectal retinorecipient layer. Electrophysiological method, thus, allows to indirectly clarify and make precise the morphology of the retino-tectal connections and to establish a morpho-physiological correspondence.


Goldfish Carp Extracellular recording Ganglion cells Retino-tectal projections Tectum opticum Tectal neurons 



Authors are grateful to Luka Gačić who provided improvements to our English grammar.

Funding information

This study was supported by the Russian Foundation for Basic Research (grant no. 16-04-00029).

Compliance with ethical standards

The experimental procedures were approved by the local ethical committee of the Institute for Information Transmission Problems of the Russian Academy of Sciences (Protocol No. 1 of April 24 2018).


  1. Bowmaker JK (1999) The ecology of visual pigments. In: Takeuchi I, Bock G, Goode JA (eds) Novartis Foundation Symposium 224—rhodopsins and phototransduction. John Wiley & Sons, Chichester, pp 21–31Google Scholar
  2. Burrill JD, Easter SS Jr (1994) Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J Comp Neurol 346:583–600CrossRefGoogle Scholar
  3. Cronly-Dillon JR (1964) Units sensitive to direction of movement in goldfish tectum. Nature 203:214–215CrossRefGoogle Scholar
  4. Damjanović I (2015) Direction selective units in goldfish retina and tectum opticum—review and new aspects. J Integr Neurosci 14:535–556CrossRefGoogle Scholar
  5. Damjanović I, Maximova EM, Maximov VV (2009a) Receptive field sizes of direction-selective units in the fish tectum. J Integr Neurosci 8:77–93CrossRefGoogle Scholar
  6. Damjanović I, Maximova EM, Maximov VV (2009b) On the organization of receptive fields of orientation-selective units recorded in the fish tectum. J Integr Neurosci 8:323–344CrossRefGoogle Scholar
  7. Damjanović I, Maximova EM, Aliper AT, Maximov PV, Maximov VV (2015) Opposing motion inhibits responses of direction-selective ganglion cells in the fish retina. J Integr Neurosci 14:53–72CrossRefGoogle Scholar
  8. Gabriel JP, Triverdi CA, Maurer CM, Ryu C, Bollman JH (2012) Layer-specific targeting of direction-selective neurons in the zebrafish tectum opticum. Neuron 76:1147–1160CrossRefGoogle Scholar
  9. Gesteland RC, Howland B, Lettvin JY, Pitts WH (1959) Comments on microelectrodes. P IRE 47:1856–1862CrossRefGoogle Scholar
  10. Grama A, Engert F (2012) Direction selectivity in the larval zebrafish tectum is mediated by asymmetric inhibition. Front Neural Circuit 6:59Google Scholar
  11. Hong YK, Kim IJ, Sanes JR (2011) Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. J Comp Neurol 519:1691–1711CrossRefGoogle Scholar
  12. Hunter PR, Lowe AS, Thompson I, Meyer MP (2013) Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity. J Neurosci 33:13940–13945CrossRefGoogle Scholar
  13. Jacobson M, Gaze RM (1964) Types of visual response from single units in the optic tectum and optic nerve of the goldfish. Q J Exp Physiol 49:199–209CrossRefGoogle Scholar
  14. Kassing V, Engelman G, Kurtz R (2013) Monitoring of single-cell responses in the optic tectum of adult zebrafish with dextran-coupled calcium dyes delivered via local electroporation. PLoS One 8:1–10CrossRefGoogle Scholar
  15. Kinoshita M, Ito E (2006) Roles of periventricular neurons in retinotectal transmission in the optic tectum. Prog Neurobiol 79:112–121CrossRefGoogle Scholar
  16. Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8:960–976CrossRefGoogle Scholar
  17. Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What frog’s eye tells to the frog’s brain. P Ire 47:1940–1951CrossRefGoogle Scholar
  18. Liège B, Galand G (1971) Types of single-unit visual responses in the trout’s optic tectum. In: Gudikov A (ed) Visual information processing and control of motor activity. Publishing House of the Bulgarian Academy of Sciences, Sofia, pp 63–65Google Scholar
  19. Marc RE, Cameron D (2002) A molecular phenotype atlas of the zebrafish retina. J Neurocytol 30:593–654CrossRefGoogle Scholar
  20. Marc RE, Jones BW (2002) Molecular phenotyping of retinal ganglion cells. J Neurosci 22:413–427CrossRefGoogle Scholar
  21. Marc RE, Sperling HG (1976) Chromatic organization of the goldfish cone mosaic. Vis Res 16:1211–1224CrossRefGoogle Scholar
  22. Masland RH (2012) The neuronal organization of the retina. Neuron 76:266–280CrossRefGoogle Scholar
  23. Matthiessen L (1880) Untersuchungen uber den aplanatismus und die periscopie der krys-tallinsen des fischauges. Pfluger Arch Ges Physiol 21:287–307CrossRefGoogle Scholar
  24. Maturana HR, Lettvin JY, McCulloch WS, Pitts WH (1960) Anatomy and physiology of vision in the frog. J Gen Physiol 43:129–175CrossRefGoogle Scholar
  25. Maximov VV (2010) A model of receptive field of orientation-selective ganglion cells of the fish retina. Sensornye Sistemy 24:110–124 (in Russian)Google Scholar
  26. Maximov PV, Maximov VV (2010) A hardware-software complex for electrophysiological studies of the fish visual system. In: International Symposium “Ivan Djaja’s (Jaen Giaja) Belgrade School of Physiology”. Book of Abstracts 9–15 September, Belgrade, Serbia 151Google Scholar
  27. Maximov VV, Maximova EM, Maximov PV (2005a) Direction selectivity in the goldfish tectum revisited. Ann N Y Acad Sci 1048:198–205CrossRefGoogle Scholar
  28. Maximov VV, Maximova EM, Maximov PV (2005b) Classification of direction-selective units recorded in the goldfish tectum. Sensornye Sistemy 19:322–335 (in Russian)Google Scholar
  29. Maximov VV, Maximova EM, Maximov PV (2009) Classification of orientation-selective units recorded in the gold fish tectum. Sensornye Sistemy 23:13–23 (in Russian)Google Scholar
  30. Maximov VV, Maximova EM, Damjanović I, Maximov PV (2013) Detection and resolution of drifting gratings by motion detectors in the fish retina. J Integr Neurosci 12:117–143CrossRefGoogle Scholar
  31. Maximova EM, Maximov VV (1981) Detectors of the oriented lines in the visual system of the fish Carassius carassius. J Evol Biochem Phys 17:519–525 (in Russian)Google Scholar
  32. Maximova EM, Orlov OY, Dimentman AM (1971) Investigation of visual system of some marine fishes. Voprocy Ichtiologii 11:893–899 (in Russian)Google Scholar
  33. Maximova EM, Dimentman AM, Maximov VV, Nikolayev PP, Orlov OY (1975) The physiological mechanisms of colour constancy. Neirofiziologiya 7:21–26 (in Russian)Google Scholar
  34. Maximova EM, Levichkina EV, Utina IA (2006) Morphology of putative direction-selective ganglion cells traced with Dii in the fish retina. Sensornye Sistemy 20:279–287 (in Russian)Google Scholar
  35. Maximova EM, Pushchin II, Maximov PV, Maximov VV (2012) Presynaptic and postsynaptic single-unit responses in the goldfish tectum as revealed by a reversible synaptic transmission blocker. J Integr Neurosci 11:183–191CrossRefGoogle Scholar
  36. Montgomery SH, Mundy NI, Burton RA (2017) Brain evolution and development: adaptation, allometry and constraint. Proc R Soc Lond B 283:1–9Google Scholar
  37. Nevin LM, Robles E, Baier H, Scot EK (2010) Focusing on optic tectum circuitry through the lens of genetics. BMC Biol 8:126CrossRefGoogle Scholar
  38. Nikolaou N, Lowe AS, Walker AS, Abbas F, Hunter PR, Thompson ID, Meyer MP (2012) Parametric functional maps of visual inputs to the tectum. Neuron 76:317–324CrossRefGoogle Scholar
  39. Northmore DPM (2011) The optic tectum. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment. Elsevier, Publisher, pp 131–142CrossRefGoogle Scholar
  40. Peichl L (2005) Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol 287A:1001–1012CrossRefGoogle Scholar
  41. Preuss SJ, Triverdi CA, Berg-Maurer CM, Ryu S, Bollman JH (2014) Classification of object size in retinotectal microcircuits. Curr Biol 24:2376–2385CrossRefGoogle Scholar
  42. Ramón y Cajal S (1892) Le retine des vertebres. Cellule 9:119–257Google Scholar
  43. Robles E, Smith SJ, Baier H (2011) Characterization of genetically targeted neuron types in the zebrafish optic tectum. Front Neural Circuit 5:1, 1–14Google Scholar
  44. Robles E, Filosa A, Baier H (2013) Precise lamination of retinal axons generates multiple parallel input pathways in the tectum. J Neurosci 33:5027–5039CrossRefGoogle Scholar
  45. Robles E, Laurell E, Baier H (2014) The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity. Curr Biol 24:2085–2096CrossRefGoogle Scholar
  46. Roska B, Meister M (2014) The retina dissects the visual scene into distinct features. In: Werner JH, Chalupa LM (eds) The new visual neurosciences. MIT Press, Cambridge, MA, pp 163–183Google Scholar
  47. Schwassmann HO, Kruger L (1965) Organization of the visual projection upon the optic tectum of some freshwater fish. J Comp Neurol 124:113–126CrossRefGoogle Scholar
  48. Springer AD, Easter SS, Agranoff BW (1977) The role of the optic tectum in various visually mediated behaviors of goldfish. Brain Res 128:393–404CrossRefGoogle Scholar
  49. Stell WK, Kock JH (1984) Structure, development and visual acuity in the goldfish retina. In: Hilfer SR et al (eds) Molecular and cellular basis of visual acuity. Springer-Verlag New York Inc., New York, pp 79–105CrossRefGoogle Scholar
  50. Tsvilling V, Donchin O, Shamir M, Segev R (2012) Archer fish fast hunting maneuver may be guided by directionally selective retinal ganglion cells. Eur J Neurosci 35:436–444CrossRefGoogle Scholar
  51. van Wyk M, Taylor WR, Vaney DI (2006) Local edge detectors: a substrate for fine spatial vision at low temporal frequencies in rabbit retina. J Neurosci 26:13250–13263CrossRefGoogle Scholar
  52. Vanegas H, Ito H (1983) Morphological aspects of the teleostean visual system: a review. Brain Res Rev 6:117–137CrossRefGoogle Scholar
  53. Wagner HJ, Kröger RH (2005) Adaptive plasticity during the development of colour vision. Prog Retin Eye Res 24:521–536CrossRefGoogle Scholar
  54. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield HillsGoogle Scholar
  55. Wartzok D, Marks WB (1973) Directionally selective visual units recorded in optic tectum of the goldfish. J Neurophysiol 36:588–604CrossRefGoogle Scholar
  56. Zenkin GM, Pigarev IN (1969) Detector properties of the ganglion cells of the pike retina. Biofizika 14:763–772 (in Russian)Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Alexey T. Aliper
    • 1
  • Alisa A. Zaichikova
    • 1
    • 2
  • Ilija Damjanović
    • 1
  • Paul V. Maximov
    • 1
  • Anna A. Kasparson
    • 1
  • Zoran Gačić
    • 3
    • 4
    Email author
  • Elena M. Maximova
    • 1
  1. 1.Institute for Information Transmission Problems of the Russian Academy of Sciences (Kharkevich Institute)MoscowRussia
  2. 2.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia
  3. 3.Institute for Multidisciplinary Research,University of BelgradeBelgradeSerbia
  4. 4.BelgradeSerbia

Personalised recommendations