The CNS connectome of a tadpole larva of Ciona intestinalis (L.) highlights sidedness in the brain of a chordate sibling

eLife

Volumn 5, Issue DECEMBER2016, 2016, Pages

  Ryan, Kerrianne ^a   Lu, Zhiyuan ^a   Meinertzhagen, Ian A ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN ASYMMETRY; CHORDATA; CIONA INTESTINALIS; CONNECTOME; ELECTRON MICROSCOPY; GAP JUNCTION; INTERNEURON; LARVA; MOTONEURON; NONHUMAN; OTOLITH; SYNAPSE; ANIMAL; BRAIN; CELL ORGANELLE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HEMISPHERIC DOMINANCE; METABOLISM; NERVE CELL; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; BRAIN; CIONA INTESTINALIS; CONNECTOME; FUNCTIONAL LATERALITY; LARVA; MICROSCOPY, ELECTRON; NEURONS; ORGANELLES; SYNAPSES;

EID: 85005952170     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.16962     Document Type: Article

References (98)

1. Belloni E, Muenke M, Roessler E, Traverso G, Siegel-Bartelt J, Frumkin A, Mitchell HF, Donis-Keller H, Helms C, Hing AV, Heng HH, Koop B, Martindale D, Rommens JM, Tsui LC, Scherer SW. 1996. Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nature Genetics 14: 353-356. doi: 10.1038/ng1196-353, PMID: 8896571
2. Bennett MVL, Goodenough DM. 1978. Gap junctions, electrotonic coupling and intercellular communication. Neurosciences Research Program Bulletin 16: 373-486.
3. Blinkov SM, Glezer II. 1968. The Human Brain in Figures and Tables: A Quantitative Handbook Translated From the Russian by Basil Haigh. New York: Plenum Press. p 445-482.
4. Bone Q. 1992. On the locomotion of ascidian tadpole larvae. Journal of the Marine Biological Association of the United Kingdom 72: 161-186. doi: 10.1017/S0025315400048864
5. Boorman CJ, Shimeld SM. 2002a. Pitx homeobox genes in Ciona and amphioxus show left-right asymmetry is a conserved chordate character and define the ascidian adenohypophysis. Evolution and Development 4: 354-365. doi: 10.1046/j.1525-142X.2002.02021.x, PMID: 12356265
6. Boorman CJ, Shimeld SM. 2002b. The evolution of left-right asymmetry in chordates. BioEssays 24: 1004-1011. doi: 10.1002/bies.10171, PMID: 12386931
7. Brown NA, Wolpert L. 1990. The development of handedness in left/right asymmetry. Development 109: 1-9. PMID: 2209459
8. Brozovic M, Martin C, Dantec C, Dauga D, Mendez M, Simion P, Percher M, Laporte B, Scornavacca C, Di Gregorio A, Fujiwara S, Gineste M, Lowe EK, Piette J, Racioppi C, Ristoratore F, Sasakura Y, Takatori N, Brown TC, Delsuc F, et al. 2016. ANISEED 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acids Research 44: D808-D818. doi: 10.1093/nar/gkv966, PMID: 26420834
9. Cameron CB, Garey JR, Swalla BJ. 2000. Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proceedings of the National Academy of Sciences of the United States of America 97: 4469-4474. doi: 10.1073/pnas.97.9.4469
10. Carl M, Bianco IH, Bajoghli B, Aghaallaei N, Czerny T, Wilson SW. 2007. Wnt/Axin1/beta-catenin signaling regulates asymmetric nodal activation, elaboration, and concordance of CNS asymmetries. Neuron 55: 393-405. doi: 10.1016/j.neuron.2007.07.007, PMID: 17678853
11. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413. doi: 10.1038/383407a0, PMID: 8837770
12. Cobb JL, Pentreath VW. 1978. Comparison of the morphology of synapses in invertebrate and vertebrate nervous systems: analysis of the significance of the anatomical differences and interpretation of the morphological specializations. Progress in Neurobiology 10: 231-252. doi: 10.1016/0301-0082(78)90004-7, PMID: 32579
13. Cole AG, Meinertzhagen IA. 2004. The central nervous system of the ascidian larva: mitotic history of cells forming the neural tube in late embryonic Ciona intestinalis. Developmental Biology 271: 239-262. doi: 10. 1016/j.ydbio.2004.04.001, PMID: 15223332
14. Concha ML, Wilson SW. 2001. Asymmetry in the epithalamus of vertebrates. Journal of Anatomy 199: 63-84. doi: 10.1046/j.1469-7580.2001.19910063.x, PMID: 11523830
15. Crocetta F, Marino R, Cirino P, Macina A, Staiano L, Esposito R, Pezzotti MR, Racioppi C, Toscano F, De Felice E, Locascio A, Ristoratore F, Spagnuolo A, Zanetti L, Branno M, Sordino P. 2015. Mutation studies in ascidians: a review. Genesis 53: 160-169. doi: 10.1002/dvg.22837, PMID: 25395385
16. Crowther RJ, Whittaker JR. 1994. Serial repetition of cilia pairs along the tail surface of an ascidian larva. Journal of Experimental Zoology 268: 9-16. doi: 10.1002/jez.1402680103, PMID: 8301249
17. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, et al. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157-2167. doi: 10.1126/science.1080049, PMID: 12481130
18. Dilly PN. 1962. Studies on the receptors in the cerebral vesicle of the ascidian tadpole. 1. the otolith. Quarterly Journal of Microscopical Science 103: 393-398.
19. Dilly PN. 1969. Studies on the receptors in Ciona intestinalis. Zeitschrift für Zellforschung und mikroskopische Anatomie 96: 63-65. doi: 10.1007/BF00321477
20. Dowling JE, Boycott BB. 1966. Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B: Biological Sciences 166: 80-111. doi: 10.1098/rspb.1966.0086
21. Duboc V, Dufourcq P, Blader P, Roussigné M. 2015. Asymmetry of the brain: development and implications. Annual Review of Genetics 49: 647-672. doi: 10.1146/annurev-genet-112414-055322, PMID: 26442849
22. Duboc V, Röttinger E, Lapraz F, Besnardeau L, Lepage T. 2005. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Developmental Cell 9: 147-158. doi: 10.1016/j.devcel.2005.05. 008, PMID: 15992548
23. Durbin RM 1987. Studies on the development and organisation of the nervous system of Caenorhabditis elegans. PhD thesis. University of Cambridge.
24. Eakin RM, Kuda A. 1971. Ultrastructure of sensory receptors in Ascidian tadpoles. Zeitschrift Für Zellforschung Und Mikroskopische Anatomie 112: 287-312. doi: 10.1007/BF02584045, PMID: 5542324
25. Fiala JC. 2005. Reconstruct: a free editor for serial section microscopy. Journal of Microscopy 218: 52-61. doi: 10. 1111/j.1365-2818.2005.01466.x, PMID: 15817063
26. Frasnelli E, Vallortigara G, Rogers LJ. 2012. Left-right asymmetries of behaviour and nervous system in invertebrates. Neuroscience & Biobehavioral Reviews 36: 1273-1291. doi: 10.1016/j.neubiorev.2012.02.006, PMID: 22353424
27. Galaburda AM, LeMay M, Kemper TL, Geschwind N. 1978. Right-left asymmetrics in the brain. Science 199: 852-856. doi: 10.1126/science.341314, PMID: 341314
28. Garstang W. 1928.Memoirs: The Morphology of the Tunicata, and its Bearings on the Phylogeny of the Chordata Journal of Cell Science 2: 51-187.
29. Grande C, Patel NH. 2009. Lophotrochozoa get into the game: the nodal pathway and left/right asymmetry in bilateria. Cold Spring Harbor Symposia on Quantitative Biology 74: 281-287. doi: 10.1101/sqb.2009.74.044, PMID: 20413706
30. Gray EG. 1959. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. Journal of Anatomy 93: 420-433. PMID: 13829103
31. Grillner S, Wallén P. 1999. On the cellular bases of vertebrate locomotion. Progress in Brain Research. 123: 297-309. doi: 10.1016/S0079-6123(08)62865-4
32. Halpern ME, Liang JO, Gamse JT. 2003. Leaning to the left: laterality in the zebrafish forebrain. Trends in Neurosciences 26: 308-313. doi: 10.1016/S0166-2236(03)00129-2, PMID: 12798600
33. Hamada H, Meno C, Watanabe D, Saijoh Y. 2002. Establishment of vertebrate left-right asymmetry. Nature Reviews Genetics 3: 103-113. doi: 10.1038/nrg732, PMID: 11836504
34. Hobert O, Johnston RJ, Chang S. 2002. Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nature Reviews Neuroscience 3: 629-640. doi: 10.1038/nrn897, PMID: 12154364
35. Horie T, Nakagawa M, Sasakura Y, Kusakabe TG, Tsuda M. 2010. Simple motor system of the ascidian larva: neuronal complex comprising putative cholinergic and GABAergic/glycinergic neurons. Zoological Science 27: 181-190. doi: 10.2108/zsj.27.181, PMID: 20141423
36. Horie T, Orii H, Nakagawa M. 2005. Structure of ocellus photoreceptors in the ascidian Ciona intestinalis larva as revealed by an anti-arrestin antibody. Journal of Neurobiology 65: 241-250. doi: 10.1002/neu.20197, PMID: 16118796
37. Horie T, Sakurai D, Ohtsuki H, Terakita A, Shichida Y, Usukura J, Kusakabe T, Tsuda M. 2008. Pigmented and nonpigmented ocelli in the brain vesicle of the ascidian larva. Journal of Comparative Neurology 509: 88-102. doi: 10.1002/cne.21733, PMID: 18421706
38. Horridge G, Mackay B, Chapman DM. 1962. Naked axons and symmetrical synapses in an elementary nervous system. Nature 193: 899-900. doi: 10.1038/193899a0, PMID: 14449017
39. Hudson C. 2016. The central nervous system of ascidian larvae. Wiley Interdisciplinary Reviews: Developmental Biology 5: 538-561. doi: 10.1002/wdev.239, PMID: 27328318
40. Imai JH, Meinertzhagen IA. 2007a. Neurons of the ascidian larval nervous system in Ciona intestinalis: I. Central nervous system. Journal of Comparative Neurology 501: 316-334. doi: 10.1002/cne.21246, PMID: 17245701
41. Imai JH, Meinertzhagen IA. 2007b. Neurons of the ascidian larval nervous system in Ciona intestinalis: II. Peripheral nervous system. Journal of Comparative Neurology 501: 335-352. doi: 10.1002/cne.21247, PMID: 17245709
42. Katsumoto S, Hatta K, Nakagawa M. 2013. Brief hypo-osmotic shock causes test cell death, prevents neurula rotation, and disrupts left-right asymmetry in Ciona intestinalis. Zoological Science 30: 352-359. doi: 10.2108/zsj.30.352, PMID: 23646939
43. Katz MJ. 1983. Comparative anatomy of the tunicate tadpole, Ciona intestinalis. Biological Bulletin 164: 1-27. doi: 10.2307/1541186
44. Lamb TD, Collin SP, Pugh EN. 2007. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nature Reviews Neuroscience 8: 960-976. doi: 10.1038/nrn2283, PMID: 18026166
45. Lamb TD. 2013. Evolution of phototransduction, vertebrate photoreceptors and retina. Progress in Retinal and Eye Research 36: 52-119. doi: 10.1016/j.preteyeres.2013.06.001, PMID: 23792002
46. Lichtman JW, Sanes JR. 2008. Ome sweet ome: what can the genome tell us about the connectome? Current Opinion in Neurobiology 18: 346-353. doi: 10.1016/j.conb.2008.08.010, PMID: 18801435
47. Lu J, Tapia JC, White OL, Lichtman JW. 2009. The interscutularis muscle connectome. PLoS Biology 7: e1000032. doi: 10.1371/journal.pbio.1000032
48. Ludwig W. 1932. Das Rechts-Links-Problem Im Tierreich Und Beim Menschen. Berlin: Julius Springer.
49. McCarrager G, Chase R. 1985. Quantification of ultrastructural symmetry at molluscan chemical synapses. Journal of Neurobiology 16: 69-74. doi: 10.1002/neu.480160107, PMID: 2985746
50. McHenry M, Strother J. 2003. The kinematics of phototaxis in larvae of the ascidian Aplidium constellatum. Marine Biology 142: 173-184. doi: 10.1007/s00227-002-0929-z
51. McHenry MJ. 2005. The morphology, behavior, and biomechanics of swimming in ascidian larvae. Canadian Journal of Zoology 83: 62-74. doi: 10.1139/z04-157
52. Meinertzhagen IA. 2010. The organisation of invertebrate brains: cells, synapses and circuits. Acta Zoologica 91: 64-71. doi: 10.1111/j.1463-6395.2009.00425.x
53. Meinertzhagen IA. 2016. Morphology of invertebrate neurons and synapses. In: Byrne J. H (Ed). Handbook of Invertebrate Neurobiology. Oxford University Press. In press.
54. Meinertzhagen IA, Lemaire P, Okamura Y. 2004. The neurobiology of the ascidian tadpole larva: recent developments in an ancient chordate. Annual Review of Neuroscience 27: 453-485. doi: 10.1146/annurev.neuro.27.070203.144255, PMID: 15217340
55. Meinertzhagen IA, Okamura Y. 2001. The larval ascidian nervous system: the chordate brain from its small beginnings. Trends in Neurosciences 24: 401-410. doi: 10.1016/S0166-2236(00)01851-8, PMID: 11410271
56. Meinertzhagen IA, Sorra KE. 2001. Synaptic organisation in the fly’s optic lamina: few cells, many synapses and divergent microcircuits. In: Kolb H, Ripps H, Wu S (Eds). Concepts and challenges in retinal biology: a tribute to John E. Dowling Volume 131 of Progress in brain research. p 53-69.
57. Moret F, Christiaen L, Deyts C, Blin M, Joly JS, Vernier P. 2005. The dopamine-synthesizing cells in the swimming larva of the tunicate Ciona intestinalis are located only in the hypothalamus-related domain of the sensory vesicle. European Journal of Neuroscience 21: 3043-3055. doi: 10.1111/j.1460-9568.2005.04147.x, PMID: 1597 8015
58. Neville AC. 1976. Animal Asymmetry. London: Edward Arnold.
59. Nicol D, Meinertzhagen IA. 1991. Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L.). Journal of Comparative Neurology 309: 415-429. doi: 10.1002/cne.903090402, PMID: 1918443
60. Nieuwenhuys R. 1998. Chapter 16, Lungfishes. In: Nieuwenhuys R, Ten Donkelaar H. J, Nicholson C (Eds). The Central Nervous System of Vertebrates, Volume 3. Berlin Heidelberg: Springer-Verlag. doi: 10.1007/978-3-642-18262-4_16
61. Nishide K, Mugitani M, Kumano G, Nishida H. 2012. Neurula rotation determines left-right asymmetry in ascidian tadpole larvae. Development 139: 1467-1475. doi: 10.1242/dev.076083, PMID: 22399684
62. Nishino A, Okamura Y, Piscopo S, Brown ER. 2010. A glycine receptor is involved in the organization of swimming movements in an invertebrate chordate. BMC Neuroscience 11: 6. doi: 10.1186/1471-2202-11-6, PMID: 20085645
63. Nishitsuji K, Horie T, Ichinose A, Sasakura Y, Yasuo H, Kusakabe TG. 2012. Cell lineage and cis-regulation for a unique GABAergic/glycinergic neuron type in the larval nerve cord of the ascidian Ciona intestinalis. Development, Growth & Differentiation 54: 177-186. doi: 10.1111/j.1440-169X.2011.01319.x, PMID: 22470937
64. Ohyama T, Schneider-Mizell CM, Fetter RD, Aleman JV, Franconville R, Rivera-Alba M, Mensh BD, Branson KM, Simpson JH, Truman JW, Cardona A, Zlatic M. 2015. A multilevel multimodal circuit enhances action selection in Drosophila. Nature 520: 633-639. doi: 10.1038/nature14297, PMID: 25896325
65. Oonuma K, Tanaka M, Nishitsuji K, Kato Y, Shimai K, Kusakabe TG. 2016. Revised lineage of larval photoreceptor cells in Ciona reveals archetypal collaboration between neural tube and neural crest in sensory organ formation. Developmental Biology. In press. doi: 10.1016/j.ydbio.2016.10.014, PMID: 27789227
66. Palmer AR. 2009. Animal asymmetry. Current Biology 19: R473-R477. doi: 10.1016/j.cub.2009.04.006, PMID: 1 9549490
67. Pascual A, Huang KL, Neveu J, Préat T. 2004. Neuroanatomy: brain asymmetry and long-term memory. Nature 427: 605-606. doi: 10.1038/427605a, PMID: 14961111
68. Peters A, Palay SL. 1996. The morphology of synapses. Journal of Neurocytology 25: 687-700. doi: 10.1007/BF02284835, PMID: 9023718
69. Petersen JK, Svane I. 1995. Larval dispersal in the ascidian Ciona intestinalis (L.). Evidence for a closed population. Journal of Experimental Marine Biology and Ecology 186: 89-102. doi: 10.1016/0022-0981(94) 00157-9
70. Randel N, Asadulina A, Bezares-Calderón LA, Verasztó C, Williams EA, Conzelmann M, Shahidi R, Jékely G. 2014. Neuronal connectome of a sensory-motor circuit for visual navigation. eLife 3: e02730. doi: 10.7554/eLife. 02730, PMID: 24867217
71. Randel N, Jékely G. 2016. Phototaxis and the origin of visual eyes. Philosophical Transactions of the Royal Society B: Biological Sciences 371: 20150042. doi: 10.1098/rstb.2015.0042
72. Randel N, Shahidi R, Verasztó C, Bezares-Calderón LA, Schmidt S, Jékely G. 2015. Inter-individual stereotypy of the Platynereis larval visual connectome. eLife 4: e08069. doi: 10.7554/eLife.08069, PMID: 26061864
73. Rodriguez-Moldes MI, Anadón R. 1988. Ultrastructural study of the evolution of globules in coronet cells of the saccus vasculosus of an elasmobranch (Scyliorhinus canicula L.), with some observations on cerebrospinal fluid-contacting neurons. Acta Zoologica 69: 217-224. doi: 10.1111/j.1463-6395.1988.tb00918.x
74. Rogers LJ, Andrew RJ (Eds). 2002. Comparative Vertebrate Lateralization. Cambridge: Cambridge University Press.
75. Sanes JR, Marshall LM, McMahan UJ. 1978. Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. Journal of Cell Biology 78: 176-198. doi: 10.1083/jcb.78.1.176, PMID: 307554
76. Sasakura Y, Mita K, Ogura Y, Horie T. 2012. Ascidians as excellent chordate models for studying the development of the nervous system during embryogenesis and metamorphosis. Development, Growth & Differentiation 54: 420-437. doi: 10.1111/j.1440-169X.2012.01343.x, PMID: 22524611
77. Satoh N, Rokhsar D, Nishikawa T. 2014. Chordate evolution and the three-phylum system. Proceedings of the Royal Society B: Biological Sciences 281: 20141729. doi: 10.1098/rspb.2014.1729
78. Satoh N. 1994. Developmental Biology of Ascidians. Cambridge: Cambridge University Press.
79. Satoh N. 1999. Cell fate determination in the ascidian embryo. In: Moody SA. Cell-Lineage and Fate Determination London: Academic Press. p 59-74. doi: 10.1016/B978-012505255-9/50006-7
80. Satoh N. 2003. The ascidian tadpole larva: comparative molecular development and genomics. Nature Reviews Genetics 4: 285-295. doi: 10.1038/nrg1042, PMID: 12671659
81. Schier AF. 2009. Nodal morphogens. Cold Spring Harbor Perspectives in Biology 1: a003459 doi: 10.1101/cshperspect.a003459, PMID: 20066122
82. Schüz A, Palm G. 1989. Density of neurons and synapses in the cerebral cortex of the mouse. Journal of Comparative Neurology 286: 442-455. doi: 10.1002/cne.902860404, PMID: 2778101
83. Shimeld SM, Levin M. 2006. Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Developmental Dynamics 235: 1543-1553. doi: 10.1002/dvdy.20792, PMID: 16586445
84. Smeets W, Nieuwenhuys R, Roberts BL. 1983. The Central Nervous System of Cartilaginous Fishes: Structure and Functional Correlations. Berlin Heidelerg and New York: Springer-Verlag. doi: 10.1007/978-3-642-68923-9
85. Stolfi A, Ryan K, Meinertzhagen IA, Christiaen L. 2015. Migratory neuronal progenitors arise from the neural plate borders in tunicates. Nature 527: 371-374. doi: 10.1038/nature15758, PMID: 26524532
86. Svane I, Havenhand JN. 1993. Spawning and dispersal in Ciona intestinalis (L.). Marine Ecology 14: 53-66. doi: 10.1111/j.1439-0485.1993.tb00364.x
87. Svane I, Young CM. 1989. The ecology and behavior of ascidian larvae. Oceanography and Marine Biology Annual Review 27: 45-90.
88. Takemura Shin-ya, Xu CS, Lu Z, Rivlin PK, Parag T, Olbris DJ, Plaza S, Zhao T, Katz WT, Umayam L, Weaver C, Hess HF, Horne JA, Nunez-Iglesias J, Aniceto R, Chang L-A, Lauchie S, Nasca A, Ogundeyi O, Sigmund C, et al. 2015. Synaptic circuits and their variations within different columns in the visual system of Drosophila. Proceedings of the National Academy of Sciences of the United States of America 112: 13711-13716. doi: 10. 1073/pnas.1509820112
89. Takemura SY, Lu Z, Meinertzhagen IA. 2008. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. Journal of Comparative Neurology 509: 493-513. doi: 10.1002/cne.21757, PMID: 18537121
90. Thompson H, Shaw MK, Dawe HR, Shimeld SM. 2012. The formation and positioning of cilia in Ciona intestinalis embryos in relation to the generation and evolution of chordate left-right asymmetry. Developmental Biology 364: 214-223. doi: 10.1016/j.ydbio.2012.02.002, PMID: 22342242
91. Torrence SA. 1986. Sensory endings of the ascidian static organ (Chordata, Ascidiacea). Zoomorphology 106: 61-66. doi: 10.1007/BF00312108
92. Tsuda M, Sakurai D, Goda M. 2003. Direct evidence for the role of pigment cells in the brain of ascidian larvae by laser ablation. Journal of Experimental Biology 206: 1409-1417. doi: 10.1242/jeb.00235, PMID: 12624175
93. Varshney LR, Chen BL, Paniagua E, Hall DH, Chklovskii DB. 2011. Structural properties of the Caenorhabditis elegans neuronal network. PLoS Computational Biology 7: e1001066. doi: 10.1371/journal.pcbi.1001066, PMID: 21304930
94. Westfall IA. 1996. Ultrastructure of synapses in the first-evolved nervous systems. Journal of Neurocytology 25: 735-746. doi: 10.1007/BF02284838, PMID: 9023721
95. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society B: Biological Sciences 314: 1-340. doi: 10.1098/rstb.1986.0056
96. Yoshida K, Saiga H. 2008. Left-right asymmetric expression of Pitx is regulated by the asymmetric Nodal signaling through an intronic enhancer in Ciona intestinalis. Development Genes and Evolution 218: 353-360. doi: 10.1007/s00427-008-0230-3, PMID: 18546017
97. Yoshida K, Saiga H. 2011. Repression of Rx gene on the left side of the sensory vesicle by Nodal signaling is crucial for right-sided formation of the ocellus photoreceptor in the development of Ciona intestinalis. Developmental Biology 354: 144-150. doi: 10.1016/j.ydbio.2011.03.006, PMID: 21402066
98. Zega G, Thorndyke MC, Brown ER. 2006. Development of swimming behaviour in the larva of the ascidian Ciona intestinalis. Journal of Experimental Biology 209: 3405-3412. doi: 10.1242/jeb.02421, PMID: 16916975