Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

On analogies in vertebrate and insect visual systems

Abstract

Despite the large evolutionary distance between vertebrates and insects, the visual systems of these two taxa bear remarkable similarities that have been noted repeatedly, including by pioneering neuroanatomists such as Ramón y Cajal. Fuelled by the advent of transgenic approaches in neuroscience, studies of visual system anatomy and function in both vertebrates and insects have made dramatic progress during the past two decades, revealing even deeper analogies between their visual systems than were noted by earlier observers. Such across-taxa comparisons have tended to focus on either elementary motion detection or relatively peripheral layers of the visual systems. By contrast, the aims of this Review are to expand the scope of this comparison to pathways outside visual motion detection, as well as to deeper visual structures. To achieve these aims, we primarily discuss examples from recent work in larval zebrafish (Danio rerio) and the fruitfly (Drosophila melanogaster), a pair of genetically tractable model organisms with comparatively sized, small brains. In particular, we argue that the brains of both vertebrates and insects are equipped with third-order visual structures that specialize in shared behavioural tasks, including postural and course stabilization, approach and avoidance, and some other behaviours. These wider analogies between the two distant taxa highlight shared behavioural goals and associated evolutionary constraints and suggest that studies on vertebrate and insect vision have a lot to inspire each other.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Overview of phylogeny and neuroanatomy.
Fig. 2: Analogies of peripheral visual processing between vertebrates and insects.
Fig. 3: Visual structures for stabilization behaviours in vertebrates and insects.
Fig. 4: Visual structures for approach and avoidance behaviours in vertebrates and insects.
Fig. 5: Visual structures for phototaxis and landmark-based navigation in vertebrates and insects.

Similar content being viewed by others

References

  1. Rádl, E. Untersuchungen über den bau des tractus opticus von squilla mantis und von aderen Arthropoden. Sitzungsberichte der königlichen Böhmischen Gesellschaft der Wissenschaften. Math.-naturwissenschaftliche Classe. 551–598 (1899).

  2. Cajal, S. R. Y. & Sánchez, D. Contribución al Conocimiento de los Centros Nerviosos de los Insectos (Imprenta de Hijos de Nicolás Moya, 1915).

  3. Randel, N. & Jékely, G. Phototaxis and the origin of visual eyes. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150042 (2016).

    Article  Google Scholar 

  4. Joly, J.-S., Recher, G., Brombin, A., Ngo, K. & Hartenstein, V. A conserved developmental mechanism builds complex visual systems in insects and vertebrates. Curr. Biol. 26, R1001–R1009 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Zipursky, S. L. & Sanes, J. R. Chemoaffinity revisited: Dscams, protocadherins, and neural circuit assembly. Cell 143, 343–353 (2010).

    Article  CAS  PubMed  Google Scholar 

  6. Borst, A. & Helmstaedter, M. Common circuit design in fly and mammalian motion vision. Nat. Neurosci. 18, 1067–1076 (2015).

    Article  CAS  PubMed  Google Scholar 

  7. Clark, D. A. & Demb, J. B. Parallel computations in insect and mammalian visual motion processing. Curr. Biol. 26, R1062–R1072 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sanes, J. R. & Zipursky, S. L. Design principles of insect and vertebrate visual systems. Neuron 66, 15–36 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Naumann, E. A., Kampff, A. R., Prober, D. A., Schier, A. F. & Engert, F. Monitoring neural activity with bioluminescence during natural behavior. Nat. Neurosci. 13, 513–520 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Raji, J. I. & Potter, C. J. The number of neurons in Drosophila and mosquito brains. PLoS ONE 16, 1–11 (2021).

    Article  Google Scholar 

  11. Baden, T., Euler, T. & Berens, P. Understanding the retinal basis of vision across species. Nat. Rev. Neurosci. 21, 5–20 (2020).

    Article  CAS  PubMed  Google Scholar 

  12. Kerschensteiner, D. Feature detection by retinal ganglion cells. Annu. Rev. Vis. Sci. 8, 135–169 (2022).

    Article  PubMed  Google Scholar 

  13. Masland, R. H. The neuronal organization of the retina. Neuron 76, 266–280 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Behnia, R. & Desplan, C. Visual circuits in flies: beginning to see the whole picture. Curr. Opin. Neurobiol. 34, 125–132 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Currier, T. A., Pang, M. M. & Clandinin, T. R. Visual processing in the fly, from photoreceptors to behavior. Genetics 224, iyad064 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Ryu, L., Kim, S. Y. & Kim, A. J. From photons to behaviors: neural implementations of visual behaviors in Drosophila. Front. Neurosci. 16, 883640 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Schnaitmann, C., Pagni, M. & Reiff, D. F. Color vision in insects: insights from Drosophila. J. Comp. Physiol. A 206, 183–198 (2020).

    Article  Google Scholar 

  18. Yang, H. H. & Clandinin, T. R. Elementary motion detection in Drosophila: algorithms and mechanisms. Annu. Rev. Vis. Sci. 4, 143–163 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Baden, T. Ancestral photoreceptor diversity as the basis of visual behaviour. Nat Ecol. Evol. https://doi.org/10.1038/s41559-023-02291-7 (2024).

  20. van der Kooi, C. J., Stavenga, D. G., Arikawa, K., Belušič, G. & Kelber, A. Evolution of insect color vision: from spectral sensitivity to visual ecology. Annu. Rev. Entomol. 66, 435–461 (2021).

    Article  PubMed  Google Scholar 

  21. Morshedian, A. & Fain, G. L. The evolution of rod photoreceptors. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160074 (2017).

    Article  Google Scholar 

  22. Friedrich, M., Wood, E. J. & Wu, M. Developmental evolution of the insect retina: insights from standardized numbering of homologous photoreceptors. J. Exp. Zool. B Mol. Dev. Evol. 316B, 484–499 (2011).

    Article  Google Scholar 

  23. Zimmermann, M. J. Y. et al. Zebrafish differentially process color across visual space to match natural scenes. Curr. Biol. 28, 2018–2032.e5 (2018).

    Article  CAS  PubMed  Google Scholar 

  24. Baden, T. et al. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron 80, 1206–1217 (2013).

    Article  CAS  PubMed  Google Scholar 

  25. Wernet, M. F., Perry, M. W. & Desplan, C. The evolutionary diversity of insect retinal mosaics: common design principles and emerging molecular logic. Trends Genet. 31, 316–328 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Meinertzhagen, I. A. & O’Neil, S. D. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305, 232–263 (1991).

    Article  CAS  PubMed  Google Scholar 

  27. Takemura, S., Lu, Z. & Meinertzhagen, I. A. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509, 493–513 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Shekhar, K. et al. Comprehensive classification of retinal bipolar neurons by single-cell transcriptomics. Cell 166, 1308–1323.e30 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hellevik, A. M. et al. Ancient origin of the rod bipolar cell pathway in the vertebrate retina. Nat. Ecol. Evol. 8, 1165–1179 (2024).

    Article  PubMed  Google Scholar 

  30. Li, Y. N., Tsujimura, T., Kawamura, S. & Dowling, J. E. Bipolar cell–photoreceptor connectivity in the zebrafish (Danio rerio) retina. J. Comp. Neurol. 520, 3786–3802 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Fischbach, K. F. & Dittrich, A. P. M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 258, 441–475 (1989).

    Article  Google Scholar 

  32. Hamanaka, Y., Shibasaki, H., Kinoshita, M. & Arikawa, K. Neurons innervating the lamina in the butterfly, Papilio xuthus. J. Comp. Physiol. A 199, 341–351 (2013).

    Article  CAS  Google Scholar 

  33. Chapot, C. A., Euler, T. & Schubert, T. How do horizontal cells ‘talk’ to cone photoreceptors? Different levels of complexity at the cone–horizontal cell synapse. J. Physiol. 595, 5495–5506 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Clark, D. A., Bursztyn, L., Horowitz, M. A., Schnitzer, M. J. & Clandinin, T. R. Defining the computational structure of the motion detector in Drosophila. Neuron 70, 1165–1177 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Franke, K. et al. Inhibition decorrelates visual feature representations in the inner retina. Nature 542, 439–444 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Silies, M. et al. Modular use of peripheral input channels tunes motion-detecting circuitry. Neuron 79, 111–127 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Freifeld, L., Clark, D. A., Schnitzer, M. J., Horowitz, M. A. & Clandinin, T. R. GABAergic lateral interactions tune the early stages of visual processing in Drosophila. Neuron 78, 1075–1089 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Strauss, S. et al. Center-surround interactions underlie bipolar cell motion sensitivity in the mouse retina. Nat. Commun. 13, 5574 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Baylor, D. A., Fuortes, M. G. F. & O’Bryan, P. M. Receptive fields of cones in the retina of the turtle. J. Physiol. 214, 265–294 (1971).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Hirasawa, H. & Kaneko, A. pH changes in the invaginating synaptic cleft mediate feedback from horizontal cells to cone photoreceptors by modulating Ca2+ channels. J. Gen. Physiol. 122, 657–671 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Seung, H. S. Interneuron diversity and normalization specificity in a visual system. Preprint at bioRxiv https://doi.org/10.1101/2024.04.03.587837 (2024).

  42. Tachibana, M. & Kaneko, A. γ-Aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proc. Natl Acad. Sci. USA 84, 3501–3505 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tuthill, J. C., Nern, A., Holtz, S. L., Rubin, G. M. & Reiser, M. B. Contributions of the 12 neuron classes in the fly lamina to motion vision. Neuron 79, 128–140 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Pang, M. M. et al. A recurrent neural circuit in Drosophila temporally sharpens visual inputs. Curr. Biol. 35, 333–346.e6 (2025).

    Article  CAS  PubMed  Google Scholar 

  45. Matsumoto, A. et al. Direction selectivity in retinal bipolar cell axon terminals. Neuron 109, 2928–2942.e8 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Antinucci, P., Suleyman, O., Monfries, C. & Hindges, R. Neural mechanisms generating orientation selectivity in the retina. Curr. Biol. 26, 1802–1815 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kuffler, S. W. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16, 37–68 (1953).

    Article  CAS  PubMed  Google Scholar 

  48. Gjorgjieva, J., Sompolinsky, H. & Meister, M. Benefits of pathway splitting in sensory coding. J. Neurosci. 34, 12127–12144 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Wang, J. et al. Molecular characterization of the sea lamprey retina illuminates the evolutionary origin of retinal cell types. Nat. Commun. 15, 10761 (2024).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Davis, F. P. et al. A genetic, genomic, and computational resource for exploring neural circuit function. eLife 9, e50901 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Yoshimatsu, T. et al. Ancestral circuits for vertebrate color vision emerge at the first retinal synapse. Sci. Adv. 7, eabj6815 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Packer, O. S., Verweij, J., Li, P. H., Schnapf, J. L. & Dacey, D. M. Blue-yellow opponency in primate S cone photoreceptors. J. Neurosci. 30, 568–572 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Joesch, M. & Meister, M. A neuronal circuit for colour vision based on rod–cone opponency. Nature 532, 236–239 (2016).

    Article  CAS  PubMed  Google Scholar 

  54. Schnaitmann, C. et al. Color processing in the early visual system of Drosophila. Cell 172, 318–330.e18 (2018).

    Article  CAS  PubMed  Google Scholar 

  55. Heath, S. L. et al. Circuit mechanisms underlying chromatic encoding in Drosophila photoreceptors. Curr. Biol. 30, 264–275.e8 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Matsushita, A. et al. Connectome of the lamina reveals the circuit for early color processing in the visual pathway of a butterfly. Curr. Biol. 32, 2291–2299.e3 (2022).

    Article  CAS  PubMed  Google Scholar 

  57. Connaughton, V. P., Graham, D. & Nelson, R. Identification and morphological classification of horizontal, bipolar, and amacrine cells within the zebrafish retina. J. Comp. Neurol. 477, 371–385 (2004).

    Article  CAS  PubMed  Google Scholar 

  58. Ghosh, K. K., Bujan, S., Haverkamp, S., Feigenspan, A. & Wässle, H. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 469, 70–82 (2004).

    Article  PubMed  Google Scholar 

  59. Kölsch, Y. et al. Molecular classification of zebrafish retinal ganglion cells links genes to cell types to behavior. Neuron 109, 645–662.e9 (2021).

    Article  PubMed  Google Scholar 

  60. Rheaume, B. A. et al. Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes. Nat. Commun. 9, 2759 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Sanes, J. R. & Masland, R. H. The types of retinal ganglion cells: current status and implications for neuronal classification. Annu. Rev. Neurosci. 38, 221–246 (2015).

    Article  CAS  PubMed  Google Scholar 

  62. Helmstaedter, M. et al. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168–174 (2013).

    Article  CAS  PubMed  Google Scholar 

  63. Yan, W. et al. Mouse retinal cell atlas: molecular identification of over sixty amacrine cell types. J. Neurosci. 40, 5177–5195 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Garner, D. et al. Connectomic reconstruction predicts visual features used for navigation. Nature 634, 181–190 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Matsliah, A. et al. Neuronal parts list and wiring diagram for a visual system. Nature 634, 166–180 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Nern, A., Pfeiffer, B. D. & Rubin, G. M. Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc. Natl Acad. Sci. USA 112, E2967–E2976 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Fried, S. I., Münch, T. A. & Werblin, F. S. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414 (2002).

    Article  CAS  PubMed  Google Scholar 

  68. Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852 (2002).

    Article  CAS  PubMed  Google Scholar 

  69. Haverkamp, S., Albert, L., Balaji, V., Němec, P. & Dedek, K. Expression of cell markers and transcription factors in the avian retina compared with that in the marmoset retina. J. Comp. Neurol. 529, 3171–3193 (2021).

    Article  CAS  PubMed  Google Scholar 

  70. Li, Y., Yu, S., Jia, X., Qiu, X. & He, J. Defining morphologically and genetically distinct GABAergic/cholinergic amacrine cell subtypes in the vertebrate retina. PLoS Biol. 22, e3002506 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Wagner, H.-J., Wagner, E. & Boycott, B. B. Amacrine cells in the retina of a teleost fish, the roach (Rutilus rutilus): a Golgi study on differentiation and layering. Philos. Trans. R. Soc. Lond. B Biol. Sci. 321, 263–324 (1997).

    Google Scholar 

  72. Hausselt, S. E., Euler, T., Detwiler, P. B. & Denk, W. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol. 5, e185 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Kim, J. S. et al. Space–time wiring specificity supports direction selectivity in the retina. Nature 509, 331–336 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Vlasits, A. L. et al. A role for synaptic input distribution in a dendritic computation of motion direction in the retina. Neuron 89, 1317–1330 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lee, S. & Zhou, Z. J. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787–799 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Barlow, H. B. & Hill, R. M. Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139, 412–414 (1963).

    Article  CAS  PubMed  Google Scholar 

  77. Briggman, K. L., Helmstaedter, M. & Denk, W. Wiring specificity in the direction-selectivity circuit of the retina. Nature 471, 183–188 (2011).

    Article  CAS  PubMed  Google Scholar 

  78. Lee, S., Kim, K. & Zhou, Z. J. Role of ACh-GABA cotransmission in detecting image motion and motion direction. Neuron 68, 1159–1172 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Taylor, W. R., He, S., Levick, W. R. & Vaney, D. I. Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2347–2350 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Yoshida, K. et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780 (2001).

    Article  CAS  PubMed  Google Scholar 

  81. Maisak, M. S. et al. A directional tuning map of Drosophila elementary motion detectors. Nature 500, 212–216 (2013).

    Article  CAS  PubMed  Google Scholar 

  82. Shinomiya, K. et al. A common evolutionary origin for the ON- and OFF-edge motion detection pathways of the Drosophila visual system. Front. Neural Circuits 9, 1–12 (2015).

    Article  Google Scholar 

  83. Arenz, A., Drews, M. S., Richter, F. G., Ammer, G. & Borst, A. The temporal tuning of the Drosophila motion detectors is determined by the dynamics of their input elements. Curr. Biol. 82, 887–895 (2017).

    Google Scholar 

  84. Shinomiya, K. et al. Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain. eLife 8, 1–19 (2019).

    Article  Google Scholar 

  85. Strother, J. A. et al. The emergence of directional selectivity in the visual motion pathway of Drosophila. Neuron 94, 168–182.e10 (2017).

    Article  CAS  PubMed  Google Scholar 

  86. Takemura, S. et al. The comprehensive connectome of a neural substrate for ‘ON’ motion detection in Drosophila. eLife 6, e24394 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Strausfeld, N. J. The lobula plate is exclusive to insects. Arthropod Struct. Dev. 61, 101031 (2021).

    Article  PubMed  Google Scholar 

  88. Strausfeld, N. J. & Blest, A. D. Golgi studies on insects part I. The optic lobes of Lepidoptera. Philos. Trans. R. Soc. Lond. B Biol. Sci. 258, 81–134 (1970).

    Article  CAS  PubMed  Google Scholar 

  89. Semmelhack, J. L. et al. A dedicated visual pathway for prey detection in larval zebrafish. eLife 3, 1–19 (2014).

    Article  Google Scholar 

  90. Ölveczky, B. P., Baccus, S. A. & Meister, M. Segregation of object and background motion in the retina. Nature 423, 401–408 (2003).

    Article  PubMed  Google Scholar 

  91. Zhang, Y., Kim, I.-J., Sanes, J. R. & Meister, M. The most numerous ganglion cell type of the mouse retina is a selective feature detector. Proc. Natl Acad. Sci. USA 109, E2391–E2398 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Lee, S. et al. An unconventional glutamatergic circuit in the retina formed by vGluT3 amacrine cells. Neuron 84, 708–715 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kim, T., Soto, F. & Kerschensteiner, D. An excitatory amacrine cell detects object motion and provides feature-selective input to ganglion cells in the mouse retina. eLife 4, 1–15 (2015).

    Article  CAS  Google Scholar 

  94. Lee, S., Zhang, Y., Chen, M. & Zhou, Z. J. Segregated glycine-glutamate co-transmission from vGluT3 amacrine cells to contrast-suppressed and contrast-enhanced retinal circuits. Neuron 90, 27–34 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Tien, N. W., Kim, T. & Kerschensteiner, D. Target-specific glycinergic transmission from VGluT3-expressing amacrine cells shapes suppressive contrast responses in the retina. Cell Rep. 15, 1369–1375 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Keleş, M. F., Hardcastle, B. J., Städele, C., Qi, X. & Frye, M. A. Inhibitory interactions and columnar inputs to an object motion detector in Drosophila. Cell Rep. 30, 2115–2124 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Tanaka, R. & Clark, D. A. Object-displacement-sensitive visual neurons drive freezing in Drosophila. Curr. Biol. 30, 2532–2550.e8 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Osorio, D. Mechanisms of early visual processing in the medulla of the locust optic lobe: how self-inhibition, spatial-pooling, and signal rectification contribute to the properties of transient cells. Vis. Neurosci. 7, 345–355 (1991).

    Article  CAS  PubMed  Google Scholar 

  99. Bloomfield, S. A. Two types of orientation-sensitive responses of amacrine cells in the mammalian retina. Nature 350, 347–350 (1991).

    Article  CAS  PubMed  Google Scholar 

  100. Park, S. J. et al. Molecular identification of wide-field amacrine cells in mouse retina that encode stimulus orientation. Preprint at bioRxiv https://doi.org/10.1101/2023.12.28.573580 (2023).

  101. Seung, H. S. Predicting visual function by interpreting a neuronal wiring diagram. Nature 634, 113–123 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Famiglietti, E. V. & Kolb, H. Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195 (1976).

    Article  PubMed  Google Scholar 

  103. Wässle, H., Puller, C., Müller, F. & Haverkamp, S. Cone contacts, mosaics, and territories of bipolar cells in the mouse retina. J. Neurosci. 29, 106–117 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Bartel, P., Yoshimatsu, T., Janiak, F. K. & Baden, T. Spectral inference reveals principal cone-integration rules of the zebrafish inner retina. Curr. Biol. 31, 5214–5226.e4 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Seifert, M., Roberts, P. A., Kafetzis, G., Osorio, D. & Baden, T. Birds multiplex spectral and temporal visual information via retinal On- and Off-channels. Nat. Commun. 14, 5308 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Strother, J. A., Nern, A. & Reiser, M. B. Direct observation of on and off pathways in the Drosophila visual system. Curr. Biol. 24, 976–983 (2014).

    Article  CAS  PubMed  Google Scholar 

  107. Robles, E., Laurell, E. & Baier, H. The retinal projectome reveals brain-area-specific visual representations generated by ganglion cell diversity. Curr. Biol. 24, 2085–2096 (2014).

    Article  CAS  PubMed  Google Scholar 

  108. Kubo, F. et al. Functional architecture of an optic flow-responsive area that drives horizontal eye movements in zebrafish. Neuron 81, 1344–1359 (2014).

    Article  CAS  PubMed  Google Scholar 

  109. Zhou, M. et al. Zebrafish retinal ganglion cells asymmetrically encode spectral and temporal information across visual space. Curr. Biol. 30, 2927–2942.e7 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Longden, K. D., Rogers, E. M., Nern, A., Dionne, H. & Reiser, M. B. Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila. Nat. Commun. 14, 7693 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Gibson, J. J. The Senses Considered as Perceptual Systems (G. Allen & Unwin, 1966).

  112. Dodge, R. Five types of eye movement (in the horizontal meridian plane of the field of regard). Am. J. Physiol. VIII, 307–329 (1903).

    Article  Google Scholar 

  113. Fenk, L. M. et al. Muscles that move the retina augment compound eye vision in Drosophila. Nature https://doi.org/10.1038/s41586-022-05317-5 (2022).

  114. Gioanni, H., Rey, J., Villalobos, J., Bouyer, J. J. & Gioanni, Y. Optokinetic nystagmus in the pigeon (Columba livia) — I. Study in monocular and binocular vision. Exp. Brain Res. 44, 362–370 (1981).

    Article  CAS  PubMed  Google Scholar 

  115. Neuhauss, S. C. F. et al. Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J. Neurosci. 19, 8603–8615 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Götz, K. G. Optomotorische untersuchung des visuellen systems einiger augenmutanten der fruchtfliege Drosophila. Kybernetik 2, 77–92 (1964).

    Article  PubMed  Google Scholar 

  117. Harden Jones, F. R. The reaction of fish to moving backgrounds. J. Exp. Biol. 40, 437–446 (1963).

    Article  Google Scholar 

  118. Giolli, R. A., Blanks, R. H. I. & Lui, F. in Progress in Brain Research (ed. Büttner-Ennever, J. A.) vol. 151, 407–440 (Elsevier, 2006).

  119. Simpson, J. I. The accessory optic system. Annu. Rev. Neurosci. 7, 13–41 (1984).

    Article  CAS  PubMed  Google Scholar 

  120. Wullimann, M. F. & Northcutt, R. G. Connections of the corpus cerebelli in the green sunfish and the common goldfish. Brain Behav. Evol. https://doi.org/10.5282/ubm/epub.3303 (1988).

  121. Oyster, C. W., Simpson, J. I., Takahashi, E. S. & Soodak, R. E. Retinal ganglion cells projecting to the rabbit accessory optic system. J. Comp. Neurol. 190, 49–61 (1980).

    Article  CAS  PubMed  Google Scholar 

  122. Brecha, N., Karten, H. J. & Hunt, S. P. Projections of the nucleus of the basal optic root in the pigeon: an autoradiographic and horseradish peroxidase study. J. Comp. Neurol. 189, 615–670 (1980).

    Article  CAS  PubMed  Google Scholar 

  123. Mizuno, N., Mochizuki, K., Akimoto, C. & Matsushima, R. Pretectal projections to the inferior olive in the rabbit. Exp. Neurol. 39, 498–506 (1973).

    Article  CAS  PubMed  Google Scholar 

  124. Gioanni, H., Rey, J., Villalobos, J. & Dalbera, A. Single unit activity in the nucleus of the basal optic root (nBOR) during optokinetic, vestibular and visuo-vestibular stimulations in the alert pigeon (Columbia livia). Exp. Brain Res. 57, 49–60 (1984).

    Article  CAS  PubMed  Google Scholar 

  125. Walley, R. E. Receptive fields in the accessory optic system of the rabbit. Exp. Neurol. 17, 27–43 (1967).

    Article  CAS  PubMed  Google Scholar 

  126. Simpson, J. I., Soodak, R. E. & Hess, R. in Progress in Brain Research (eds Granit, R. & Pompeiano, O.) 50 715–724 (Elsevier, 1979).

  127. Lázár, G. Role of the accessory optic system in the optokinetic nystagmus of the frog. Brain Behav. Evol. 5, 443–460 (1973).

    Article  Google Scholar 

  128. Ito, K. et al. A systematic nomenclature for the insect brain. Neuron 81, 755–765 (2014).

    Article  CAS  PubMed  Google Scholar 

  129. Fabian, J. M., el Jundi, B., Wiederman, S. D. & O’Carroll, D. C. The complex optic lobe of dragonflies. Preprint at bioRxiv https://doi.org/10.1101/2020.05.10.087437 (2020).

  130. Buchner, E., Buchner, S. & Bülthoff, I. Deoxyglucose mapping of nervous activity induced in Drosophila brain by visual movement. J. Comp. Physiol. A 155, 471–483 (1984).

    Article  Google Scholar 

  131. Hausen, K. Motion sensitive interneurons in the optomotor system of the fly II. The horizontal cells: receptive field organization and response characteristics. Biol. Cybern. 46, 67–79 (1982).

    Article  Google Scholar 

  132. Hengstenberg, R. Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J. Comp. Physiol. 149, 179–193 (1982).

    Article  Google Scholar 

  133. Franz, M. O. & Krapp, H. G. Wide-field, motion-sensitive neurons and matched filters for optic flow fields. Biol. Cybern. 83, 185–197 (2000).

    Article  CAS  PubMed  Google Scholar 

  134. Krapp, H. G. & Hengstenberg, R. Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463–466 (1996).

    Article  CAS  PubMed  Google Scholar 

  135. Farrow, K., Haag, J. & Borst, A. Nonlinear, binocular interactions underlying flow field selectivity of a motion-sensitive neuron. Nat. Neurosci. 9, 1312–1320 (2006).

    Article  CAS  PubMed  Google Scholar 

  136. Blondeau, J. Electrically evoked course control in the fly Calliphora erythrocephala. J. Exp. Biol. 92, 143–153 (1981).

    Article  Google Scholar 

  137. Heisenberg, M., Wonneberger, R. & Wolf, R. Optomotor-blindH31 — a Drosophila mutant of the lobula plate giant neurons. J. Comp. Physiol. 124, 287–296 (1978).

    Article  Google Scholar 

  138. Kramer, A., Wu, Y., Baier, H. & Kubo, F. Neuronal architecture of a visual center that processes optic flow. Neuron 103, 118–132.e7 (2019).

    Article  CAS  PubMed  Google Scholar 

  139. Ahrens, M. B. et al. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471–477 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Portugues, R., Feierstein, C. E., Engert, F. & Orger, M. B. Whole-brain activity maps reveal stereotyped, distributed networks for visuomotor behavior. Neuron 81, 1328–1343 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Naumann, E. A. et al. From whole-brain data to functional circuit models: the zebrafish optomotor response. Cell 167, 947–960.e20 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Wang, K., Hinz, J., Zhang, Y., Thiele, T. R. & Arrenberg, A. B. Parallel channels for motion feature extraction in the pretectum and tectum of larval zebrafish. Cell Rep. 30, 442–453.e6 (2020).

    Article  CAS  PubMed  Google Scholar 

  143. Zhang, Y., Huang, R., Nörenberg, W. & Arrenberg, A. B. A robust receptive field code for optic flow detection and decomposition during self-motion. Curr. Biol. 32, 2505–2516.e8 (2022).

    Article  CAS  PubMed  Google Scholar 

  144. Dragomir, E. I., Štih, V. & Portugues, R. Evidence accumulation during a sensorimotor decision task revealed by whole-brain imaging. Nat. Neurosci. 23, 85–93 (2020).

    Article  CAS  PubMed  Google Scholar 

  145. Grasse, K. L. & Cynader, M. S. Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. J. Neurophysiol. 51, 276–293 (1984).

    Article  CAS  PubMed  Google Scholar 

  146. Collewijn, H. Direction-selective units in the rabbit’s nucleus of the optic tract. Brain Res. 100, 489–508 (1975).

    Article  CAS  PubMed  Google Scholar 

  147. Winterson, B. J. & Brauth, S. E. Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia). Exp. Brain Res. 60, 215–226 (1985).

    Article  CAS  PubMed  Google Scholar 

  148. Schnell, B., Raghu, S. V., Nern, A. & Borst, A. Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J. Comp. Physiol. A 198, 389–395 (2012).

    Article  Google Scholar 

  149. Shinomiya, K., Nern, A., Meinertzhagen, I. A., Plaza, S. M. & Reiser, M. B. Neuronal circuits integrating visual motion information in Drosophila melanogaster. Curr. Biol. 32, 3529–3544.e2 (2022).

    Article  CAS  PubMed  Google Scholar 

  150. Mauss, A. S. et al. Neural circuit to integrate opposing motions in the visual field. Cell 162, 351–362 (2015).

    Article  CAS  PubMed  Google Scholar 

  151. Schnell, B. et al. Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J. Neurophysiol. 103, 1646–1657 (2010).

    Article  CAS  PubMed  Google Scholar 

  152. Tanaka, R. et al. Neural mechanisms to incorporate visual counterevidence in self-movement estimation. Curr. Biol. 33, 4960–4979.e7 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Wasserman, S. M. et al. Olfactory neuromodulation of motion vision circuitry in Drosophila. Curr. Biol. 25, 467–472 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Chiappe, M. E., Seelig, J. D., Reiser, M. B. & Jayaraman, V. Walking modulates speed sensitivity in Drosophila motion vision. Curr. Biol. 20, 1470–1475 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Maimon, G., Straw, A. D. & Dickinson, M. H. Active flight increases the gain of visual motion processing in Drosophila. Nat. Neurosci. 13, 393–399 (2010).

    Article  CAS  PubMed  Google Scholar 

  156. Suver, M. P., Mamiya, A. & Dickinson, M. H. Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr. Biol. 22, 2294–2302 (2012).

    Article  CAS  PubMed  Google Scholar 

  157. Kim, A. J., Fitzgerald, J. K. & Maimon, G. Cellular evidence for efference copy in Drosophila visuomotor processing. Nat. Neurosci. 18, 1247–1255 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Kim, A. J., Fenk, L. M., Lyu, C. & Maimon, G. Quantitative predictions orchestrate visual signaling in Drosophila. Cell 168, 280–294.e12 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Fenk, L. M., Kim, A. J. & Maimon, G. Suppression of motion vision during course-changing, but not course-stabilizing, navigational turns. Curr. Biol. 31, 4608–4619.e3 (2021).

    Article  CAS  PubMed  Google Scholar 

  160. Fujiwara, T., Cruz, T. L., Bohnslav, J. P. & Chiappe, M. E. A faithful internal representation of walking movements in the Drosophila visual system. Nat. Neurosci. 20, 72–81 (2017).

    Article  CAS  PubMed  Google Scholar 

  161. Fujiwara, T., Brotas, M. & Chiappe, M. E. Walking strides direct rapid and flexible recruitment of visual circuits for course control in Drosophila. Neuron 110, 2124–2138.e8 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Boergens, K. M., Kapfer, C., Helmstaedter, M., Denk, W. & Borst, A. Full reconstruction of large lobula plate tangential cells in Drosophila from a 3D EM dataset. PLoS ONE 13, 1–15 (2018).

    Article  Google Scholar 

  163. Wei, H., Kyung, H. Y., Kim, P. J. & Desplan, C. The diversity of lobula plate tangential cells (LPTCs) in the Drosophila motion vision system. J. Comp. Physiol. A 206, 139–148 (2020).

    Article  Google Scholar 

  164. Zhao, A. et al. A comprehensive neuroanatomical survey of the Drosophila lobula plate tangential neurons with predictions for their optic flow sensitivity. eLife 13, RP93659 (2024).

    Google Scholar 

  165. Ammer, G. et al. Multilevel visual motion opponency in Drosophila. Nat. Neurosci. 26, 1894–1905 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Wu, M. et al. Visual projection neurons in the Drosophila lobula link feature detection to distinct behavioral programs. eLife 5, e21022 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  167. Isaacson, M. D. et al. Small-field visual projection neurons detect translational optic flow and support walking control. Preprint at bioRxiv https://doi.org/10.1101/2023.06.21.546024 (2023).

  168. Wu, Y., dal Maschio, M., Kubo, F. & Baier, H. An optical illusion pinpoints an essential circuit node for global motion processing. Neuron 108, 722–734.e5 (2020).

    Article  CAS  PubMed  Google Scholar 

  169. Busch, C., Borst, A. & Mauss, A. S. Bi-directional control of walking behavior by horizontal optic flow sensors. Curr. Biol. 28, 4037–4045.e5 (2018).

    Article  CAS  PubMed  Google Scholar 

  170. Haikala, V., Joesch, M., Borst, A. & Mauss, A. S. Optogenetic control of fly optomotor responses. J. Neurosci. 33, 13927–13934 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Creamer, M. S., Mano, O. & Clark, D. A. Visual control of walking speed in Drosophila. Neuron 100, 1460–1473.e6 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Knogler, L. D., Markov, D. A., Dragomir, E. I., Štih, V. & Portugues, R. Sensorimotor representations in cerebellar granule cells in larval zebrafish are dense, spatially organized, and non-temporally patterned. Curr. Biol. 27, 1288–1302 (2017).

    Article  CAS  PubMed  Google Scholar 

  173. Markov, D. A., Petrucco, L., Kist, A. M. & Portugues, R. A cerebellar internal model calibrates a feedback controller involved in sensorimotor control. Nat. Commun. 12, 6694 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Erginkaya, M. et al. A competitive disinhibitory network for robust optic flow processing in Drosophila. Nat. Neurosci. https://doi.org/10.1101/2023.08.06.552150 (2025).

  175. Suver, M. P., Huda, A., Iwasaki, N., Safarik, S. & Dickinson, M. H. An array of descending visual interneurons encoding self-motion in Drosophila. J. Neurosci. 36, 1–13 (2016).

    Article  Google Scholar 

  176. Hulse, B. K., Stanoev, A., Turner-Evans, D. B., Seelig, J. D. & Jayaraman, V. A rotational velocity estimate constructed through visuomotor competition updates the fly’s neural compass. Preprint at bioRxiv https://doi.org/10.1101/2023.09.25.559373 (2023).

  177. Lu, J. et al. Transforming representations of movement from body- to world-centric space. Nature 601, 98–104 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  178. Lyu, C., Abbott, L. F. & Maimon, G. Building an allocentric travelling direction signal via vector computation. Nature 601, 92–97 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  179. Cisek, P. Resynthesizing behavior through phylogenetic refinement. Atten. Percept. Psychophys. 81, 2265–2287 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  180. Bengtson, S. Origins and early evolution of predation. Paleontol. Soc. Pap. 8, 289–318 (2002).

    Article  Google Scholar 

  181. Erwin, D. H. et al. The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334, 1091–1097 (2011).

    Article  CAS  PubMed  Google Scholar 

  182. Paterson, J. R. et al. Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480, 237–240 (2011).

    Article  CAS  PubMed  Google Scholar 

  183. Braitenberg, V. Vehicles: Experiments in Synthetic Psychology (MIT Press, 1986).

  184. Remy, M. & Güntürkün, O. Retinal afferents to the tectum opticum and the nucleus opticus principalis thalami in the pigeon. J. Comp. Neurol. 305, 57–70 (1991).

    Article  CAS  PubMed  Google Scholar 

  185. Linden, R. & Perry, V. H. Massive retinotectal projection in rats. Brain Res. 272, 145–149 (1983).

    Article  CAS  PubMed  Google Scholar 

  186. Ellis, E. M., Gauvain, G., Sivyer, B. & Murphy, G. J. Shared and distinct retinal input to the mouse superior colliculus and dorsal lateral geniculate nucleus. J. Neurophysiol. 116, 602–610 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Robles, E., Filosa, A. & Baier, H. Precise lamination of retinal axons generates multiple parallel input pathways in the tectum. J. Neurosci. 33, 5027–5039 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Hong, Y. K., Kim, I. J. & Sanes, J. R. Stereotyped axonal arbors of retinal ganglion cell subsets in the mouse superior colliculus. J. Comp. Neurol. 519, 1691–1711 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Thompson, A. W., Vanwalleghem, G. C., Heap, L. A. & Scott, E. K. Functional profiles of visual-, auditory-, and water flow-responsive neurons in the zebrafish tectum. Curr. Biol. 26, 743–754 (2016).

    Article  CAS  PubMed  Google Scholar 

  190. Heap, L. A., Vanwalleghem, G., Thompson, A. W., Favre-Bulle, I. A. & Scott, E. K. Luminance changes drive directional startle through a thalamic pathway. Neuron 99, 293–301.e4 (2018).

    Article  CAS  PubMed  Google Scholar 

  191. Heap, L. A. et al. Hypothalamic projections to the optic tectum in larval zebrafish. Front. Neuroanat. 11, 135 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  192. Benavidez, N. L. et al. Organization of the inputs and outputs of the mouse superior colliculus. Nat. Commun. 12, 4004 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Meek, J. & Schellart, N. A. M. A Golgi study of goldfish optic tectum. J. Comp. Neurol. 182, 89–121 (1978).

    Article  CAS  PubMed  Google Scholar 

  194. Robles, E., Smith, S. & Baier, H. Characterization of genetically targeted neuron types in the zebrafish optic tectum. Front. Neural Circuits 5, 1 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Scott, E. & Baier, H. The cellular architecture of the larval zebrafish tectum, as revealed by Gal4 enhancer trap lines. Front. Neural Circuits 3, 13 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  196. Gale, S. D. & Murphy, G. J. Distinct representation and distribution of visual information by specific cell types in mouse superficial superior colliculus. J. Neurosci. 34, 13458–13471 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Isa, T., Marquez-Legorreta, E., Grillner, S. & Scott, E. K. The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action. Curr. Biol. 31, R741–R762 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Langer, T. P. & Lund, R. D. The upper layers of the superior colliculus of the rat: a Golgi study. J. Comp. Neurol. 158, 405–435 (1974).

    Article  Google Scholar 

  199. Basso, M. A., Bickford, M. E. & Cang, J. Unraveling circuits of visual perception and cognition through the superior colliculus. Neuron 109, 918–937 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Strausfeld, N. J. & Olea-Rowe, B. Convergent evolution of optic lobe neuropil in Pancrustacea. Arthropod Struct. Dev. 61, 101040 (2021).

    Article  PubMed  Google Scholar 

  201. Otsuna, H. & Ito, K. Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J. Comp. Neurol. 497, 928–958 (2006).

    Article  PubMed  Google Scholar 

  202. Panser, K. et al. Automatic segmentation of Drosophila neural compartments using GAL4 expression data reveals novel visual pathways. Curr. Biol. 26, 1943–1954 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  203. Sterling, P. & Wickelgren, B. G. Visual receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 1–15 (1969).

    Article  CAS  PubMed  Google Scholar 

  204. Lettvin, J. Y., Maturana, H. R., McCulloh, W. S. & Pitts, W. H. in Sensory Communications 757–776 (MIT Press, 1961).

  205. Hatsopoulos, N., Gabbiani, F. & Laurent, G. Elementary computation of object approach by a wide-field visual neuron. Science 270, 1000–1003 (1995).

    Article  CAS  PubMed  Google Scholar 

  206. O’Shea, M. & Williams, J. L. D. The anatomy and output connection of a locust visual interneurone; the lobular giant movement detector (LGMD) neurone. J. Comp. Physiol. 91, 257–266 (1974).

    Article  Google Scholar 

  207. O’Carroll, D. Feature-detecting neurons in dragonflies. Nature 362, 541–543 (1993).

    Article  Google Scholar 

  208. Gilbert, C. & Strausfeld, N. J. The functional organization of male-specific visual neurons in flies. J. Comp. Physiol. A 169, 395–411 (1991).

    Article  CAS  PubMed  Google Scholar 

  209. Nordström, K. & O’Carroll, D. C. Small object detection neurons in female hoverflies. Proc. R. Soc. B Biol. Sci. 273, 1211–1216 (2006).

    Article  Google Scholar 

  210. Niell, C. M. & Smith, S. J. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941–951 (2005).

    Article  CAS  PubMed  Google Scholar 

  211. Bianco, I. H. & Engert, F. Visuomotor transformations underlying hunting behavior in zebrafish. Curr. Biol. 25, 831–846 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  212. Förster, D. et al. Retinotectal circuitry of larval zebrafish is adapted to detection and pursuit of prey. eLife 9, 1–26 (2020).

    Article  Google Scholar 

  213. Barker, A. J. & Baier, H. Sensorimotor decision making in the zebrafish tectum. Curr. Biol. 25, 2804–2814 (2015).

    Article  CAS  PubMed  Google Scholar 

  214. Del Bene, F. et al. Filtering of visual information in the tectum by an identified neural circuit. Science 330, 669–673 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  215. Preuss, S. J., Trivedi, C. A., vom Berg-Maurer, C. M., Ryu, S. & Bollmann, J. H. Classification of object size in retinotectal microcircuits. Curr. Biol. 24, 2376–2385 (2014).

    Article  CAS  PubMed  Google Scholar 

  216. Gabriel, J. P., Trivedi, C. A., Maurer, C. M., Ryu, S. & Bollmann, J. H. Layer-specific targeting of direction-selective neurons in the zebrafish optic tectum. Neuron 76, 1147–1160 (2012).

    Article  CAS  PubMed  Google Scholar 

  217. Hunter, P. R., Lowe, A. S., Thompson, I. D. & Meyer, M. P. Emergent properties of the optic tectum revealed by population analysis of direction and orientation selectivity. J. Neurosci. 33, 13940–13945 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Temizer, I., Donovan, J. C., Baier, H. & Semmelhack, J. L. A visual pathway for looming-evoked escape in larval zebrafish. Curr. Biol. 25, 1823–1834 (2015).

    Article  CAS  PubMed  Google Scholar 

  219. Dunn, T. W. et al. Neural circuits underlying visually evoked escapes in larval zebrafish. Neuron 89, 613–628 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. Helmbrecht, T. O., dal Maschio, M., Donovan, J. C., Koutsouli, S. & Baier, H. Topography of a visuomotor transformation. Neuron 100, 1429–1445.e4 (2018).

    Article  CAS  PubMed  Google Scholar 

  221. Fornetto, C., Tiso, N., Pavone, F. S. & Vanzi, F. Colored visual stimuli evoke spectrally tuned neuronal responses across the central nervous system of zebrafish larvae. BMC Biol. 18, 172 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Guggiana Nilo, D. A., Riegler, C., Hübener, M. & Engert, F. Distributed chromatic processing at the interface between retina and brain in the larval zebrafish. Curr. Biol. 31, 1945–1953.e5 (2021).

    Article  CAS  PubMed  Google Scholar 

  223. Li, Y. & Meister, M. Functional cell types in the mouse superior colliculus. eLife 12, e82367 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. De Franceschi, G. & Solomon, S. G. Visual response properties of neurons in the superficial layers of the superior colliculus of awake mouse. J. Physiol. 596, 6307–6332 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  225. Liu, Y. et al. Mapping visual functions onto molecular cell types in the mouse superior colliculus. Neuron 111, 1876–1886.e5 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Wang, L., Sarnaik, R., Rangarajan, K., Liu, X. & Cang, J. Visual receptive field properties of neurons in the superficial superior colliculus of the mouse. J. Neurosci. 30, 16573–16584 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Zhao, X., Liu, M. & Cang, J. Visual cortex modulates the magnitude but not the selectivity of looming-evoked responses in the superior colliculus of awake mice. Neuron 84, 202–213 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Shainer, I. et al. Transcriptomic neuron types vary topographically in function and morphology. Nature 638, 1023–1033 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  229. von Reyn, C. R. et al. Feature integration drives probabilistic behavior in the Drosophila escape response. Neuron 94, 1190–1204.e6 (2017).

    Article  Google Scholar 

  230. Ache, J. M. et al. Neural basis for looming size and velocity encoding in the Drosophila giant fiber escape pathway. Curr. Biol. 29, 1073–1081.e4 (2019).

    Article  CAS  PubMed  Google Scholar 

  231. Klapoetke, N. C. et al. Ultra-selective looming detection from radial motion opponency. Nature 551, 237–241 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  232. Morimoto, M. M. et al. Spatial readout of visual looming in the central brain of Drosophila. eLife 9, e57685 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  233. Tanaka, R. & Clark, D. A. Neural mechanisms to exploit positional geometry for collision avoidance. Curr. Biol. 32, 2357–2374.e6 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Keleş, M. F. & Frye, M. A. Object-detecting neurons in Drosophila. Curr. Biol. 27, 1–8 (2017).

    Article  Google Scholar 

  235. Klapoetke, N. C. et al. A functionally ordered visual feature map in the Drosophila brain. Neuron https://doi.org/10.1016/j.neuron.2022.02.013 (2022).

  236. Städele, C., Keleş, M. F., Mongeau, J.-M. M. & Frye, M. A. Non-canonical receptive field properties and neuromodulation of feature-detecting neurons in flies. Curr. Biol. 30, 2508–2519.e6 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  237. Turner, M. H., Krieger, A., Pang, M. M. & Clandinin, T. R. Visual and motor signatures of locomotion dynamically shape a population code for feature detection in Drosophila. eLife 11, e82587 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Fotowat, H. & Engert, F. Neural circuits underlying habituation of visually evoked escape behaviors in larval zebrafish. eLife 12, e82916 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  239. Lee, K. H., Tran, A., Turan, Z. & Meister, M. The sifting of visual information in the superior colliculus. eLife 9, e50678 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  240. O’Shea, M. & Rowell, C. H. F. Protection from habituation by lateral inhibition. Nature 254, 53–55 (1975).

    Article  PubMed  Google Scholar 

  241. Fabian, J. M., Dunbier, J. R., O’Carroll, D. C. & Wiederman, S. D. Properties of predictive gain modulation in a dragonfly visual neuron. J. Exp. Biol. 222, jeb207316 (2019).

    Article  PubMed  Google Scholar 

  242. Barnett, P. D., Nordström, K. & O’Carroll, D. C. Retinotopic organization of small-field-target-detecting neurons in the insect visual system. Curr. Biol. 17, 569–578 (2007).

    Article  CAS  PubMed  Google Scholar 

  243. Nordström, K., Barnett, P. D. & O’Carroll, D. C. Insect detection of small targets moving in visual clutter. PLoS Biol. 4, e54 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  244. Yamawaki, Y. Unraveling the functional organization of lobula complex in the mantis brain by identification of visual interneurons. J. Comp. Neurol. 527, 1161–1178 (2019).

    Article  PubMed  Google Scholar 

  245. de Malmazet, D., Kühn, N. K. & Farrow, K. Retinotopic separation of nasal and temporal motion selectivity in the mouse superior colliculus. Curr. Biol. 28, 2961–2969.e4 (2018).

    Article  PubMed  Google Scholar 

  246. Xiao, T. & Baier, H. Lamina-specific axonal projections in the zebrafish tectum require the type IV collagen dragnet. Nat. Neurosci. 10, 1529–1537 (2007).

    Article  CAS  PubMed  Google Scholar 

  247. Yamagata, M., Weiner, J. A., Dulac, C., Roth, K. A. & Sanes, J. R. Labeled lines in the retinotectal system: markers for retinorecipient sublaminae and the retinal ganglion cell subsets that innervate them. Mol. Cell. Neurosci. 33, 296–310 (2006).

    Article  CAS  PubMed  Google Scholar 

  248. Kim, I. J., Zhang, Y., Meister, M. & Sanes, J. R. Laminar restriction of retinal ganglion cell dendrites and axons: subtype-specific developmental patterns revealed with transgenic markers. J. Neurosci. 30, 1452–1462 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Nikolaou, N. et al. Parametric functional maps of visual inputs to the tectum. Neuron 76, 317–324 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Zhang, B., Yao, Y., Zhang, H., Kawakami, K. & Du, J. L. Left habenula mediates light-preference behavior in zebrafish via an asymmetrical visual pathway. Neuron 93, 914–928.e4 (2017).

    Article  CAS  PubMed  Google Scholar 

  251. Molotkov, D., Ferrarese, L., Boissonnet, T. & Asari, H. Topographic axonal projection at single-cell precision supports local retinotopy in the mouse superior colliculus. Nat. Commun. 14, 7418 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  252. Shi, X. et al. Retinal origin of direction selectivity in the superior colliculus. Nat. Neurosci. 20, 550–558 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Gale, S. D. & Murphy, G. J. Active dendritic properties and local inhibitory input enable selectivity for object motion in mouse superior colliculus neurons. J. Neurosci. 36, 9111–9123 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  254. Ribi, W. A. & Scheel, M. The second and third optic ganglia of the worker bee. Cell Tissue Res. 221, 17–43 (1981).

    Article  CAS  PubMed  Google Scholar 

  255. Tanaka, R. & Clark, D. A. Identifying Inputs to visual projection neurons in Drosophila lobula by analyzing connectomic data. eNeuro 9, ENEURO.0053-22.2022 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  256. Donders, F. C. Ueber angeborene und erworbene association. Albrecht von Graefes Arch. Ophthalmol. 18, 153–164 (1872).

    Article  Google Scholar 

  257. Apter, J. T. Projection of the retina on superior colliculus of cats. J. Neurophysiol. 8, 123–134 (1945).

    Article  Google Scholar 

  258. Robinson, D. A. Eye movements evoked by collicular stimulation in the alert monkey. Vis. Res. 12, 1795–1808 (1972).

    Article  CAS  PubMed  Google Scholar 

  259. Straschill, M. & Rieger, P. Eye movements evoked by focal stimulation of the cats superior colliculus. Brain Res. 59, 211–227 (1973).

    Article  CAS  PubMed  Google Scholar 

  260. Olds, M. E. & Olds, J. Approach-escape interactions in rat brain. Am. J. Physiol. 203, 803–810 (1962).

    Article  CAS  PubMed  Google Scholar 

  261. Olds, M. E. & Olds, J. Approach-avoidance analysis of rat diencephalon. J. Comp. Neurol. 120, 259–295 (1963).

    Article  CAS  PubMed  Google Scholar 

  262. Sahibzada, N., Dean, P. & Redgrave, P. Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J. Neurosci. 6, 723–733 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  263. Fajardo, O., Zhu, P. & Friedrich, R. Control of a specific motor program by a small brain area in zebrafish. Front. Neural Circuits 7, 67 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  264. Campagner, D. et al. A cortico-collicular circuit for orienting to shelter during escape. Nature 613, 111–119 (2023).

    Article  CAS  PubMed  Google Scholar 

  265. Shang, C. et al. Divergent midbrain circuits orchestrate escape and freezing responses to looming stimuli in mice. Nat. Commun. 9, 1232 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  266. Hoy, J. L., Bishop, H. I. & Niell, C. M. Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse. Curr. Biol. 29, 4130–4138.e5 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  267. Shang, C. et al. A subcortical excitatory circuit for sensory-triggered predatory hunting in mice. Nat. Neurosci. 22, 909–920 (2019).

    Article  CAS  PubMed  Google Scholar 

  268. De Franceschi, G., Vivattanasarn, T., Saleem, A. B. & Solomon, S. G. Vision guides selection of freeze or flight defense strategies in mice. Curr. Biol. 26, 2150–2154 (2016).

    Article  PubMed  Google Scholar 

  269. Ribeiro, I. M. A. et al. Visual projection neurons mediating directed courtship in Drosophila. Cell 174, 607–621.e18 (2018).

    Article  CAS  PubMed  Google Scholar 

  270. Sten, T. H., Li, R., Otopalik, A. & Ruta, V. Sexual arousal gates visual processing during Drosophila courtship. Nature 595, 549–553 (2021).

    Article  Google Scholar 

  271. Cowley, B. R. et al. Mapping model units to visual neurons reveals population code for social behaviour. Nature https://doi.org/10.1038/s41586-024-07451-8 (2024).

  272. Dean, P., Redgrave, P. & Westby, G. W. M. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci. 12, 137–147 (1989).

    Article  CAS  PubMed  Google Scholar 

  273. Zottoli, S. J., Hordes, A. R. & Faber, D. S. Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res. 401, 113–121 (1987).

    Article  CAS  PubMed  Google Scholar 

  274. Nissanov, J., Eaton, R. C. & DiDomenico, R. The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res. 517, 88–98 (1990).

    Article  CAS  PubMed  Google Scholar 

  275. Frye, M. A. & Olberg, R. M. Visual receptive field properties of feature detecting neurons in the dragonfly. J. Comp. Physiol. A 177, 569–576 (1995).

    Article  Google Scholar 

  276. Gronenberg, W. & Strausfeld, N. J. Premotor descending neurons responding selectively to local visual stimuli in flies. J. Comp. Neurol. 316, 87–103 (1992).

    Article  CAS  PubMed  Google Scholar 

  277. Rind, F. C. A chemical synapse between two motion detecting neurones in the locust brain. J. Exp. Biol. 110, 143–167 (1984).

    Article  CAS  PubMed  Google Scholar 

  278. Henriques, P. M., Rahman, N., Jackson, S. E. & Bianco, I. H. Nucleus isthmi is required to sustain target pursuit during visually guided prey-catching. Curr. Biol. 29, 1771–1786.e5 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Fernandes, A. M. et al. Neural circuitry for stimulus selection in the zebrafish visual system. Neuron 109, 805–822.e6 (2021).

    Article  CAS  PubMed  Google Scholar 

  280. Kappel, J. M. et al. Visual recognition of social signals by a tectothalamic neural circuit. Nature 608, 146–152 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Strausfeld, N. J., Sinkaevitch, I. & Okamura, J.-Y. Organization of local interneurons in optic glomeruli of the dipterous visual system and comparisons with the antennal lobes. Dev. Neurobiol. 67, 1267–1288 (2007).

    Article  PubMed  Google Scholar 

  282. Namiki, S., Dickinson, M. H., Wong, A. M., Korff, W. & Card, G. M. The functional organization of descending sensory-motor pathways in Drosophila. eLife 7, e34272 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  283. Gahtan, E., Tanger, P. & Baier, H. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J. Neurosci. 25, 9294–9303 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  284. Tanouye, M. A. & Wyman, R. J. Motor outputs of giant nerve fiber in Drosophila. J. Neurophysiol. 44, 405–421 (1980).

    Article  CAS  PubMed  Google Scholar 

  285. von Reyn, C. R. et al. A spike-timing mechanism for action selection. Nat. Neurosci. 17, 962–970 (2014).

    Article  Google Scholar 

  286. Dombrovski, M. et al. Synaptic gradients transform object location to action. Nature 613, 534–542 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. Baier, H. & Wullimann, M. F. Anatomy and function of retinorecipient arborization fields in zebrafish. J. Comp. Neurol. 529, 3454–3476 (2021).

    Article  PubMed  Google Scholar 

  288. Morin, L. P. & Studholme, K. M. Retinofugal projections in the mouse. J. Comp. Neurol. 522, 3733–3753 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  289. Santana, N. N. M. et al. Retinorecipient areas in the common marmoset (Callithrix jacchus): an image-forming and non-image forming circuitry. Front. Neural Circuits 17, 1088686 (2023).

    Article  PubMed  PubMed Central  Google Scholar 

  290. Helfrich-Förster, C. The circadian clock in the brain: a structural and functional comparison between mammals and insects. J. Comp. Physiol. A 190, 601–613 (2004).

    Article  Google Scholar 

  291. Omoto, J. J. et al. Visual input to the Drosophila central complex by developmentally and functionally distinct neuronal populations. Curr. Biol. 27, 1098–1110 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  292. Vogt, K. et al. Direct neural pathways convey distinct visual information to Drosophila mushroom bodies. eLife 5, 1–13 (2016).

    Article  Google Scholar 

  293. Ganguly, I., Heckman, E. L., Litwin-Kumar, A., Clowney, E. J. & Behnia, R. Diversity of visual inputs to Kenyon cells of the Drosophila mushroom body. Nat. Commun. 15, 5698 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  294. Bhadra, U., Thakkar, N., Das, P. & Pal Bhadra, M. Evolution of circadian rhythms: from bacteria to human. Sleep Med. 35, 49–61 (2017).

    Article  PubMed  Google Scholar 

  295. Berson, D. M., Dunn, F. A. & Takao, M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070–1073 (2002).

    Article  CAS  PubMed  Google Scholar 

  296. Hattar, S., Liao, H.-W., Takao, M., Berson, D. M. & Yau, K.-W. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295, 1065–1070 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  297. Aranda, M. L. & Schmidt, T. M. Diversity of intrinsically photosensitive retinal ganglion cells: circuits and functions. Cell. Mol. Life Sci. 78, 889–907 (2021).

    Article  CAS  PubMed  Google Scholar 

  298. Beier, C., Zhang, Z., Yurgel, M. & Hattar, S. Projections of ipRGCs and conventional RGCs to retinorecipient brain nuclei. J. Comp. Neurol. 529, 1863–1875 (2021).

    Article  PubMed  Google Scholar 

  299. Ecker, J. L. et al. Melanopsin-expressing retinal ganglion-cell photoreceptors: cellular diversity and role in pattern vision. Neuron 67, 49–60 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  300. Helfrich-Förster, C. The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 92, 612–616 (1995).

    Article  PubMed  PubMed Central  Google Scholar 

  301. Grima, B., Chélot, E., Xia, R. & Rouyer, F. Morning and evening peaks of activity rely on different clock neurons of the Drosophila brain. Nature 431, 869–873 (2004).

    Article  CAS  PubMed  Google Scholar 

  302. Reinhard, N. et al. Synaptic connectome of the Drosophila circadian clock. Nat. Commun. 15, 10392 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  303. Shafer, O. T. et al. Connectomic analysis of the Drosophila lateral neuron clock cells reveals the synaptic basis of functional pacemaker classes. eLife 11, e79139 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  304. Jékely, G. Evolution of phototaxis. Philos. Trans. R. Soc. B Biol. Sci. 364, 2795–2808 (2009).

    Article  Google Scholar 

  305. Burgess, H. A., Schoch, H. & Granato, M. Distinct retinal pathways drive spatial orientation behaviors in zebrafish navigation. Curr. Biol. 20, 381–386 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  306. Orger, M. B. & Baier, H. Channeling of red and green cone inputs to the zebrafish optomotor response. Vis. Neurosci. 22, 275–281 (2005).

    Article  PubMed  Google Scholar 

  307. Benzer, S. Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc. Natl Acad. Sci. USA 58, 1112–1119 (1967).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  308. Chen, X. & Engert, F. Navigational strategies underlying phototaxis in larval zebrafish. Front. Syst. Neurosci. 8, 1–13 (2014).

    Article  Google Scholar 

  309. Karpenko, S. et al. From behavior to circuit modeling of light-seeking navigation in zebrafish larvae. eLife 9, e52882 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  310. Guggiana Nilo, D. A. & Engert, F. Properties of the visible light phototaxis and UV avoidance behaviors in the larval zebrafish. Front. Behav. Neurosci. 10, 160 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  311. Chen, X. et al. Brain-wide organization of neuronal activity and convergent sensorimotor transformations in larval zebrafish. Neuron 100, 876–890.e5 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  312. Hikosaka, O. The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 11, 503–513 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  313. Okamoto, H., Cherng, B.-W., Nakajo, H., Chou, M.-Y. & Kinoshita, M. Habenula as the experience-dependent controlling switchboard of behavior and attention in social conflict and learning. Curr. Opin. Neurobiol. 68, 36–43 (2021).

    Article  CAS  PubMed  Google Scholar 

  314. Cheng, R.-K., Krishnan, S., Lin, Q., Kibat, C. & Jesuthasan, S. Characterization of a thalamic nucleus mediating habenula responses to changes in ambient illumination. BMC Biol. 15, 104 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  315. Dreosti, E., Vendrell Llopis, N., Carl, M., Yaksi, E. & Wilson, S. W. Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Curr. Biol. 24, 440–445 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  316. Lin, Q. & Jesuthasan, S. Masking of a circadian behavior in larval zebrafish involves the thalamo-habenula pathway. Sci. Rep. 7, 4104 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  317. Huang, L. et al. A visual circuit related to habenula underlies the antidepressive effects of light therapy. Neuron 102, 128–142.e8 (2019).

    Article  CAS  PubMed  Google Scholar 

  318. Zhu, Y., Nern, A., Zipursky, S. L. & Frye, M. A. Peripheral visual circuits functionally segregate motion and phototaxis behaviors in the fly. Curr. Biol. 19, 613–619 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  319. Otsuna, H., Shinomiya, K. & Ito, K. Parallel neural pathways in higher visual centers of the Drosophila brain that mediate wavelength-specific behavior. Front. Neural Circuits 8, 1–12 (2014).

    Article  Google Scholar 

  320. Lin, T. Y. et al. Mapping chromatic pathways in the Drosophila visual system. J. Comp. Neurol. 524, 213–227 (2016).

    Article  CAS  PubMed  Google Scholar 

  321. Kind, E. et al. Synaptic targets of photoreceptors specialized to detect color and skylight polarization in Drosophila. eLife 10, e71858 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  322. Timaeus, L., Geid, L., Sancer, G., Wernet, M. F. & Hummel, T. Parallel visual pathways with topographic versus nontopographic organization connect the Drosophila eyes to the central brain. iScience 23, 101590 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  323. Seelig, J. D. & Jayaraman, V. Feature detection and orientation tuning in the Drosophila central complex. Nature 503, 262–266 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  324. Hanesch, U., Fischbach, K.-F. & Heisenberg, M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257, 343–366 (1989).

    Article  Google Scholar 

  325. Artiushin, G. & Sehgal, A. The Drosophila circuitry of sleep–wake regulation. Curr. Opin. Neurobiol. 44, 243–250 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  326. Heinze, S. Variations on an ancient theme — the central complex across insects. Curr. Opin. Behav. Sci. 57, 101390 (2024).

    Article  Google Scholar 

  327. Seelig, J. D. & Jayaraman, V. Neural dynamics for landmark orientation and angular path integration. Nature 521, 186–191 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  328. Fisher, Y. E., Lu, J., D’Alessandro, I. & Wilson, R. I. Sensorimotor experience remaps visual input to a heading-direction network. Nature https://doi.org/10.1038/s41586-019-1772-4 (2019).

  329. Kim, S. S., Hermundstad, A. M., Romani, S., Abbott, L. F. & Jayaraman, V. Generation of stable heading representations in diverse visual scenes. Nature https://doi.org/10.1038/s41586-019-1767-1 (2019).

  330. Shiozaki, H. M. & Kazama, H. Parallel encoding of recent visual experience and self-motion during navigation in Drosophila. Nat. Neurosci. 20, 1395–1403 (2017).

    Article  CAS  PubMed  Google Scholar 

  331. Sun, Y. et al. Neural signatures of dynamic stimulus selection in Drosophila. Nat. Neurosci. 20, 1104–1113 (2017).

    Article  CAS  PubMed  Google Scholar 

  332. Hardcastle, B. J. et al. A visual pathway for skylight polarization processing in Drosophila. eLife 10, 1–46 (2021).

    Article  Google Scholar 

  333. Hardie, R. C. Properties of photoreceptors R7 and R8 in dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J. Comp. Physiol. A 154, 157–165 (1984).

    Article  Google Scholar 

  334. Weir, P. T. et al. Anatomical reconstruction and functional imaging reveal an ordered array of skylight polarization detectors in Drosophila. J. Neurosci. 36, 5397–5404 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  335. Wernet, M. F. et al. Genetic dissection reveals two separate retinal substrates for polarization vision in Drosophila. Curr. Biol. 22, 12–20 (2012).

    Article  CAS  PubMed  Google Scholar 

  336. Heinze, S., Florman, J., Asokaraj, S., el Jundi, B. & Reppert, S. M. Anatomical basis of sun compass navigation II: the neuronal composition of the central complex of the monarch butterfly. J. Comp. Neurol. 521, 267–298 (2013).

    Article  PubMed  Google Scholar 

  337. Pfeiffer, K. & Kinoshita, M. Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus). J. Comp. Neurol. 520, 212–229 (2012).

    Article  PubMed  Google Scholar 

  338. Träger, U., Wagner, R., Bausenwein, B. & Homberg, U. A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J. Comp. Neurol. 506, 288–300 (2008).

    Article  PubMed  Google Scholar 

  339. Heinze, S. & Reppert, S. M. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69, 345–358 (2011).

    Article  CAS  PubMed  Google Scholar 

  340. el Jundi, B., Pfeiffer, K. & Homberg, U. A distinct layer of the medulla integrates sky compass signals in the brain of an insect. PLoS ONE 6, e27855 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  341. Aizawa, H. et al. Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr. Biol. 15, 238–243 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  342. Bianco, I. H., Carl, M., Russell, C., Clarke, J. D. & Wilson, S. W. Brain asymmetry is encoded at the level of axon terminal morphology. Neural Dev. 3, 1–20 (2008).

    Article  Google Scholar 

  343. McLaughlin, I., Dani, J. A. & De Biasi, M. The medial habenula and interpeduncular nucleus circuitry is critical in addiction, anxiety, and mood regulation. J. Neurochem. 142, 130–143 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  344. Petrucco, L. et al. Neural dynamics and architecture of the heading direction circuit in zebrafish. Nat. Neurosci. 26, 765–773 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  345. Lavian, H., Prat, O., Petrucco, L., Štih, V. & Portugues, R. The representation of visual motion and landmark position aligns with heading direction in the zebrafish interpeduncular nucleus. Preprint at bioRxiv https://doi.org/10.1101/2024.09.25.614953 (2024).

  346. Tanaka, R. & Portugues, R. Mechanisms for plastic landmark anchoring in zebrafish compass neurons. Preprint at bioRxiv https://doi.org/10.1101/2024.12.13.628331 (2024).

  347. Briscoe, S. D. & Ragsdale, C. W. Evolution of the chordate telencephalon. Curr. Biol. 29, R647–R662 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  348. Suryanarayana, S. M., Pérez-Fernández, J., Robertson, B. & Grillner, S. The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nat. Ecol. Evol. 4, 639–651 (2020).

    Article  PubMed  Google Scholar 

  349. Bloch, S. et al. Non-thalamic origin of zebrafish sensory nuclei implies convergent evolution of visual pathways in amniotes and teleosts. eLife 9, e54945 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  350. Kaas, J. H., Qi, H. & Stepniewska, I. Escaping the nocturnal bottleneck, and the evolution of the dorsal and ventral streams of visual processing in primates. Philos. Trans. R. Soc. B Biol. Sci. 377, 20210293 (2021).

    Article  Google Scholar 

  351. Modi, M. N., Shuai, Y. & Turner, G. C. The Drosophila mushroom body: from architecture to algorithm in a learning circuit. Annu. Rev. Neurosci. 43, 465–484 (2020).

    Article  CAS  PubMed  Google Scholar 

  352. Paulk, A. C. & Gronenberg, W. Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Struct. Dev. 37, 443–458 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  353. Srinivasan, M. V. Honey bees as a model for vision, perception, and cognition. Annu. Rev. Entomol. 55, 267–284 (2010).

    Article  CAS  PubMed  Google Scholar 

  354. Zhang, S. Visually guided decision making in foraging honeybees. Front. Neurosci. 6, 88 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  355. Baden, T. From water to land: evolution of photoreceptor circuits for vision in air. PLoS Biol. 22, e3002422 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  356. Gabbiani, F., Krapp, H. G. & Laurent, G. Computation of object approach by a wide-field, motion-sensitive neuron. J. Neurosci. 19, 1122–1141 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  357. Burkhardt, P. & Jékely, G. Evolution of synapses and neurotransmitter systems: the divide-and-conquer model for early neural cell-type evolution. Curr. Opin. Neurobiol. 71, 127–138 (2021).

    Article  CAS  PubMed  Google Scholar 

  358. Pungor, J. R. & Niell, C. M. The neural basis of visual processing and behavior in cephalopods. Curr. Biol. 33, R1106–R1118 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  359. Bok, M. J., Macali, A. & Garm, A. High-resolution vision in pelagic polychaetes. Curr. Biol. 34, R269–R270 (2024).

    Article  CAS  PubMed  Google Scholar 

  360. Misof, B. et al. Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767 (2014).

    Article  CAS  PubMed  Google Scholar 

  361. Wu, Y. K., Petrucco, L. & Portugues, R. Anatomical and functional organization of the interpeduncular nucleus in larval zebrafish. Preprint at bioRxiv https://doi.org/10.1101/2024.10.09.617353 (2024).

  362. Puelles, L. & Medina, L. Field homology as a way to reconcile genetic and developmental variability with adult homology. Brain Res. Bull. 57, 243–255 (2002).

    Article  PubMed  Google Scholar 

  363. Brostek, L., Büttner, U., Mustari, M. J. & Glasauer, S. Eye velocity gain fields in MSTd during optokinetic stimulation. Cereb. Cortex 25, 2181–2190 (2015).

    Article  PubMed  Google Scholar 

  364. El-Danaf, R. N. et al. Morphological and functional convergence of visual projection neurons from diverse neurogenic origins in Drosophila. Nat. Commun. 16, 698 (2025).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  365. Ahrens, M. B., Orger, M. B., Robson, D. N., Li, J. M. & Keller, P. J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10, 413–420 (2013).

    Article  CAS  PubMed  Google Scholar 

  366. Panier, T. et al. Fast functional imaging of multiple brain regions in intact zebrafish larvae using selective plane illumination microscopy. Front. Neural Circuits 7, 65 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  367. Vladimirov, N. et al. Light-sheet functional imaging in fictively behaving zebrafish. Nat. Methods 11, 883–884 (2014).

    Article  CAS  PubMed  Google Scholar 

  368. Smarandache-Wellmann, C. R. Arthropod neurons and nervous system. Curr. Biol. 26, R960–R965 (2016).

    Article  CAS  PubMed  Google Scholar 

  369. Dionne, H., Hibbard, K. L., Cavallaro, A., Kao, J. C. & Rubin, G. M. Genetic reagents for making split-GAL4 lines in Drosophila. Genetics 209, 31–35 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  370. Meissner, G. W. et al. A searchable image resource of Drosophila GAL4 driver expression patterns with single neuron resolution. eLife 12, e80660 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  371. Dorkenwald, S. et al. Neuronal wiring diagram of an adult brain. Nature 634, 124–138 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  372. Scheffer, L. K. et al. A connectome and analysis of the adult Drosophila central brain. eLife 9, 1–74 (2020).

    Article  Google Scholar 

  373. Aimon, S., Cheng, K. Y., Gjorgjieva, J. & Grunwald Kadow, I. C. Global change in brain state during spontaneous and forced walk in Drosophila is composed of combined activity patterns of different neuron classes. eLife 12, e85202 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  374. Schaffer, E. S. et al. The spatial and temporal structure of neural activity across the fly brain. Nat. Commun. 14, 5572 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  375. Shainer, I. et al. A single-cell resolution gene expression atlas of the larval zebrafish brain. Sci. Adv. 9, eade9909 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  376. Svara, F. et al. Automated synapse-level reconstruction of neural circuits in the larval zebrafish brain. Nat. Methods 19, 1357–1366 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the members of the Portugues laboratory for helpful comments and discussions. R.T. was supported by EMBO Postdoctoral Fellowship (ALTF732-2022) and HFSP Postdoctoral Fellowship (LT0027/2023-L). R.P. was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) as part of the SPP 2205 — project 430156228. In addition, R.P. was supported by the DFG under the Excellence Strategy of Germany within the framework of the Munich Cluster for Systems Neurology (EXC 2145 SyNergy, identifier 390857198).

Author information

Authors and Affiliations

Authors

Contributions

Both authors contributed to all aspects of the preparation of the manuscript.

Corresponding authors

Correspondence to Ryosuke Tanaka  (田中涼介) or Ruben Portugues.

Ethics declarations

Competing interests

The authors declare no completing interests.

Peer review

Peer review information

Nature Reviews Neuroscience thanks Tom Baden, Ethan Scott and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tanaka, R., Portugues, R. On analogies in vertebrate and insect visual systems. Nat. Rev. Neurosci. 26, 456–475 (2025). https://doi.org/10.1038/s41583-025-00932-3

Download citation

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41583-025-00932-3

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing