Skip to main content

Vision Made Easy: Cubozoans Can Advance Our Understanding of Systems-Level Visual Information Processing

  • Chapter
  • First Online:
Marine Organisms as Model Systems in Biology and Medicine

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 65))

Abstract

Animals relying on vision as their main sensory modality reserve a large part of their central nervous system to appropriately navigate their environment. In general, neural involvement correlates to the complexity of the visual system and behavioural repertoire. In humans, one third of the available neural capacity supports our single-chambered general-purpose eyes, whereas animals with less elaborate visual systems need less computational power, and generally have smaller brains, and thereby lack in visual behaviour. As a consequence, both traditional model animals (mice, zebrafish, and flies) and more experimentally tractable animals (Hydra, Planaria, and C. elegans) cannot contribute to our understanding of systems-level visual information processing—a Goldilocks case of too big and too small.

However, one animal, the box jellyfish Tripedalia cystophora, possesses a rather complex visual system, displays multiple visual behaviours, yet processes visual information by means of a relatively simple central nervous system. This—just right—model system could not only provide information on how visual stimuli are processed through distinct combinations of neural circuitry but also provide a processing algorithm for extracting specific information from a complex visual scene.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R (2012) Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485:471–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10:413–420

    Article  CAS  PubMed  Google Scholar 

  • Akemann W, Mutoh H, Perron A, Rossier J, Knöpfel T (2010) Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat Methods 7:643–649

    Article  CAS  PubMed  Google Scholar 

  • Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M, Tolö J, Gordus A, Orger MB, Severi KE, Macklin JJ, Patel R, Pulver SR, Wardill TJ, Fischer E, Schüler C, Chen TW, Sarkisyan KS, Marvin JS, Bargmann CI, Kim DS, Kügler S, Lagnado L, Hegemann P, Gottschalk A, Schreiter ER, Looger LL (2013) Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 6:2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alford SC, Wu J, Zhao Y, Campbell RE, Knöpfel T (2013) Optogenetic reporters. Biol Cell 105:14–29

    Article  CAS  PubMed  Google Scholar 

  • Anderson PA, Grünert U (1988) Three-dimensional structure of bidirectional, excitatory chemical synapses in the jellyfish Cyanea capillata. Synapse 2:606–613

    Article  CAS  PubMed  Google Scholar 

  • Bielecki J, Høeg JT, Garm A (2013a) Fixational eye movements in the earliest stage of metazoan evolution. PLoS One 8:e66442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielecki J, Nachman G, Garm A (2013b) Swim pacemaker response to bath applied neurotransmitters in the cubozoan Tripedalia cystophora. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199:785–797

    Article  CAS  PubMed  Google Scholar 

  • Bielecki J, Zaharoff AK, Leung NY, Garm A, Oakley TH (2014) Ocular and extraocular expression of opsins in the rhopalium of Tripedalia cystophora (Cnidaria: Cubozoa). PLoS One 9:e98870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briggman KL, Abarbanel HD, Kristan WB (2005) Optical imaging of neuronal populations during decision-making. Science 307:896–901

    Article  CAS  PubMed  Google Scholar 

  • Buskey E (2003) Behavioral adaptations of the cubozoan medusa Tripedalia cystophora for feeding on copepod (Dioithona oculata) swarms. Mar Biol 142:225–232

    Article  Google Scholar 

  • Coates MM, Garm A, Theobald JC, Thompson SH, Nilsson DE (2006) The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant). J Exp Biol 209:3758–3765

    Article  PubMed  Google Scholar 

  • De Pittà M, Volman V, Berry H, Parpura V, Volterra A, Ben-Jacob E (2012) Computational quest for understanding the role of astrocyte signaling in synaptic transmission and plasticity. Front Comput Neurosci 6:98

    Article  PubMed  PubMed Central  Google Scholar 

  • Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210:492–498

    Article  CAS  PubMed  Google Scholar 

  • Fain GL, Matthews HR, Cornwall MC, Koutalos Y (2001) Adaptation in vertebrate photoreceptors. Physiol Rev 81:117–151

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Vandenberghe LH, Wilson JM (2005) New recombinant serotypes of AAV vectors. Curr Gene Ther 5:285–297

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Bielecki J (2008) Swim pacemakers in box jellyfish are modulated by the visual input. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 194:641–651

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Ekström P (2010) Evidence for multiple photosystems in jellyfish. Int Rev Cell Mol Biol 280:41–78

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Mori S (2009) Multiple photoreceptor systems control the swim pacemaker activity in box jellyfish. J Exp Biol 212:3951–3960

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Ekström P, Boudes M, Nilsson DE (2006) Rhopalia are integrated parts of the central nervous system in box jellyfish. Cell Tissue Res 325:333–343

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Coates MM, Gad R, Seymour J, Nilsson DE (2007a) The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:547–557

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Poussart Y, Parkefelt L, Ekström P, Nilsson DE (2007b) The ring nerve of the box jellyfish Tripedalia cystophora. Cell Tissue Res 329:147–157

    Article  CAS  PubMed  Google Scholar 

  • Garm A, O’Connor M, Parkefelt L, Nilsson DE (2007c) Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol 210:3616–3623

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Andersson F, Nilsson Dan-E (2008) Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. Vision Research 48 (8):1061–1073

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Oskarsson M, Nilsson DE (2011) Box jellyfish use terrestrial visual cues for navigation. Curr Biol 21:798–803

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Bielecki J, Petie R, Nilsson DE (2012) Opposite patterns of diurnal activity in the box jellyfish Tripedalia cystophora and Copula sivickisi. Biol Bull 222:35–45

    Article  CAS  PubMed  Google Scholar 

  • Garm A, Hedal I, Islin M, Gurska D (2013) Pattern- and contrast-dependent visual response in the box jellyfish Tripedalia cystophora. J Exp Biol 216:4520–4529

    Article  PubMed  Google Scholar 

  • Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

    Article  CAS  PubMed  Google Scholar 

  • Gray GC, Martin VJ, Satterlie RA (2009) Ultrastructure of the retinal synapses in cubozoans. Biol Bull 217:35–49

    Article  PubMed  Google Scholar 

  • Ijspeert AJ (2008) 2008 Special issue: Central pattern generators for locomotion control in animals and robots: a review. Neural Netw 21:642–653

    Article  PubMed  Google Scholar 

  • Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4:147ra111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kass-Simon G, Pierobon P (2007) Cnidarian chemical neurotransmission, an updated overview. Comp Biochem Physiol A Mol Integr Physiol 146:9–25

    Article  CAS  PubMed  Google Scholar 

  • Koyanagi M, Takano K, Tsukamoto H, Ohtsu K, Tokunaga F, Terakita A (2008) Jellyfish vision starts with cAMP signaling mediated by opsin-G(s) cascade. Proc Natl Acad Sci U S A 105:15576–15580

    Article  PubMed  PubMed Central  Google Scholar 

  • Kozmik Z, Ruzickova J, Jonasova K, Matsumoto Y, Vopalensky P, Kozmikova I, Strnad H, Kawamura S, Piatigorsky J, Paces V, Vlcek C (2008) Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc Natl Acad Sci U S A 105:8989–8993

    Article  PubMed  PubMed Central  Google Scholar 

  • Land MF (1999) Motion and vision: why animals move their eyes. J Comp Physiol A 185:341–352

    Article  CAS  PubMed  Google Scholar 

  • Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press, New York

    Book  Google Scholar 

  • Levy O, Appelbaum L, Leggat W, Gothlif Y, Hayward DC, Miller DJ, Hoegh-Guldberg O (2007) Light-responsive cryptochromes from a simple multicellular animal, the coral Acropora millepora. Science 318:467–470

    Article  CAS  PubMed  Google Scholar 

  • Lin MZ, Schnitzer MJ (2016) Genetically encoded indicators of neuronal activity. Nat Neurosci 19:1142–1153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackie G, Meech R (1995a) Central circuitry in the jellyfish Aglantha. I: The relay system. J Exp Biol 198:2261–2270

    PubMed  CAS  Google Scholar 

  • Mackie G, Meech R (1995b) Central circuitry in the jellyfish Aglantha. II: The ring giant and carrier systems. J Exp Biol 198:2271–2278

    PubMed  CAS  Google Scholar 

  • Mackie GO, Anderson PAV, Ssingla CL (1984) Apparent absence of gap junctions in two classes of cnidaria. Biol Bull 167:120–123

    Article  Google Scholar 

  • Marder E, Bucher D, Schulz DJ, Taylor AL (2005) Invertebrate central pattern generation moves along. Curr Biol 15:R685–R699

    Article  CAS  PubMed  Google Scholar 

  • Matthews HR, Murphy RLW, Fain GL, Lamb TD (1988) Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature 334:67–69

    Article  CAS  PubMed  Google Scholar 

  • Morgan PT, Perrins R, Lloyd PE, Weiss KR (2000) Intrinsic and extrinsic modulation of a single central pattern generating circuit. J Neurophysiol 84:1186–1193

    Article  CAS  PubMed  Google Scholar 

  • Mundell NA, Beier KT, Pan YA, Lapan SW, Göz Aytürk D, Berezovskii VK, Wark AR, Drokhlyansky E, Bielecki J, Born RT, Schier AF, Cepko CL (2015) Vesicular stomatitis virus enables gene transfer and transsynaptic tracing in a wide range of organisms. J Comp Neurol 523:1639–1663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson DE (2004) Eye evolution: a question of genetic promiscuity. Curr Opin Neurobiol 14:407–414

    Article  CAS  PubMed  Google Scholar 

  • Nilsson DE, Gislén L, Coates MM, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201–205

    Article  CAS  PubMed  Google Scholar 

  • Nusbaum MP, Blitz DM (2012) Neuropeptide modulation of microcircuits. Curr Opin Neurobiol 22:592–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connor M, Nilsson DE, Garm A (2010) Temporal properties of the lens eyes of the box jellyfish Tripedalia cystophora. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196:213–220

    Article  PubMed  PubMed Central  Google Scholar 

  • Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508:207–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parkefelt L, Ekström P (2009) Prominent system of RFamide immunoreactive neurons in the rhopalia of box jellyfish (Cnidaria: Cubozoa). J Comp Neurol 516:157–165

    Article  PubMed  Google Scholar 

  • Petie R, Garm A, Nilsson DE (2011) Visual control of steering in the box jellyfish Tripedalia cystophora. J Exp Biol 214:2809–2815

    Article  PubMed  Google Scholar 

  • Petie R, Garm A, Nilsson D-E (2013) Contrast and rate of light intensity decrease control directional swimming in the box jellyfish Tripedalia cystophora (Cnidaria, Cubomedusae). Hydrobiologia 703:69–77

    Article  Google Scholar 

  • Plachetzki DC, Degnan BM, Oakley TH (2007) The origins of novel protein interactions during animal opsin evolution. PLoS One 2:e1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plickert G, Schneider B (2004) Neuropeptides and photic behavior in Cnidaria. Hydrobiologia 530–531:49–57

    Google Scholar 

  • Satterlie RA (1979) Central control of swimming in the cubomedusan jellyfish Carybdea rastonii. J Comp Physiol 133:357–367

    Article  Google Scholar 

  • Satterlie RA (2002) Neuronal control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669

    Article  Google Scholar 

  • Satterlie RA (2011) Do jellyfish have central nervous systems? J Exp Biol 214:1215–1223

    Article  PubMed  Google Scholar 

  • Schall JD (2001) Neural basis of deciding, choosing and acting. Nat Rev Neurosci 2:33–42

    Article  CAS  PubMed  Google Scholar 

  • Shorten M, Seymour JE, Cross MC, Carette TJ, Woodward G, Cross TF (2005) J Zool 267:371–381

    Article  Google Scholar 

  • Skogh C, Garm A, Nilsson DE, Ekström P (2006) Bilaterally symmetrical rhopalial nervous system of the box jellyfish Tripedalia cystophora. J Morphol 267:1391–1405

    Article  CAS  PubMed  Google Scholar 

  • Stöckl AL, Petie R, Nilsson DE (2011) Setting the pace: new insights into central pattern generator interactions in box jellyfish swimming. PLoS One 6:e27201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St-Pierre F, Marshall JD, Yang Y, Gong Y, Schnitzer MJ, Lin MZ (2014) High-fidelity optical reporting of neuronal electrical activity with an ultrafast fluorescent voltage sensor. Nat Neurosci 17:884–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suga H, Schmid V, Gehring WJ (2008) Evolution and functional diversity of jellyfish opsins. Curr Biol 18:51–55

    Article  CAS  PubMed  Google Scholar 

  • Takano T, Han X, Deane R, Zlokovic B, Nedergaard M (2007) Two-photon imaging of astrocytic Ca2+ signaling and the microvasculature in experimental mice models of Alzheimer’s disease. Ann N Y Acad Sci 1097:40–50

    Article  CAS  PubMed  Google Scholar 

  • Terakita A (2005) The opsins. Genome Biol 6:213

    Article  PubMed  PubMed Central  Google Scholar 

  • Volterra A, Liaudet N, Savtchouk I (2014) Astrocyte Ca2+ signalling: an unexpected complexity. Nat Rev Neurosci 15:327–335

    Article  CAS  PubMed  Google Scholar 

  • Wehner R (1987) ‘Matched filters’ – neural models of the external world. J Comp Physiol A: Neuroethol Sens Neural Behav Physiol 161:511–531

    Article  Google Scholar 

  • Yamasu T, Yoshida M (1976) Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria Haeckel. Cell Tissue Res 170:325–339

    Article  CAS  PubMed  Google Scholar 

  • Yang HH, St-Pierre F, Sun X, Ding X, Lin MZ, Clandinin TR (2016) Subcellular imaging of voltage and calcium signals reveals neural processing in vivo. Cell 166:245–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsu N (1917) Notes on the physiology of Carybdea rastonii. J Coll Sci Tokyo Imp Univ 40:1–12

    Google Scholar 

Download references

Acknowledgements

The authors are indebted to Dan-Eric Nilsson for helping with the figures and continuous scientific insights.

This project was funded by the Cluster of Excellence ‘The Future Ocean’. ‘The Future Ocean’ is funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments. JB acknowledges Danish Independent Research Grant no. DFF—1325-00146. AG acknowledges DFF—4181-00398.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan Bielecki .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bielecki, J., Garm, A. (2018). Vision Made Easy: Cubozoans Can Advance Our Understanding of Systems-Level Visual Information Processing. In: Kloc, M., Kubiak, J. (eds) Marine Organisms as Model Systems in Biology and Medicine. Results and Problems in Cell Differentiation, vol 65. Springer, Cham. https://doi.org/10.1007/978-3-319-92486-1_27

Download citation

Publish with us

Policies and ethics