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Identifying Vertebrate Brain Prototypes in Deuterostomes

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Brain Evolution by Design

Part of the book series: Diversity and Commonality in Animals ((DCA))

Abstract

Vertebrates have a dorsal tubular central nervous system (CNS), the anterior part of which is a complex and highly organized brain. The invertebrate chordates (tunicates and cephalochordates) also have a CNS derived from the dorsal neural tube, but it is far simpler than the vertebrate CNS. The nervous system of ambulacrarians (hemichordates and echinoderms), the sister group of chordates, consists of a nerve net and multiple nerve cords with no discrete brain. Despite the poorly centralized organization of the ambulacrarian nervous system, genomics and molecular developmental biological studies have suggested that the major developmental programs that pattern the vertebrate brain already existed in the common ancestor of chordates and ambulacrarians. The CNS of cephalochordate amphioxus is a nerve cord with little anterior concentration, but has neuronal circuits with similarities to those of the vertebrate diencephalon-midbrain-hindbrain. The tadpole larva of the tunicate ascidian has a brain with sensory and motor control systems that shares many features with the vertebrate brain, including the retinal/hypothalamic territory, a locomotor central pattern generator, neural crests, and cranial placodes. Given the many shared characteristics among chordates, the CNS of invertebrate chordates should provide a unique platform to study the developmental and evolutionary bases underlying the emergence of the complex CNS of vertebrates.

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References

  • Abitua PB, Wagner E, Navarrete IA, Levine M (2012) Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492:104–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abitua PB, Gainous TB, Kaczmarczyk AN, Winchell CJ, Hudson C, Kamata K, Nakagawa M, Tsuda M, Kusakabe TG, Levine M (2015) The pre-vertebrate origins of neurogenic placodes. Nature 524:462–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams BA, Tello JA, Erchegyi J, Warby C, Hong DJ et al (2003) Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology 144:1907–1919

    Article  CAS  PubMed  Google Scholar 

  • Alford S, Schwartz E, Viana di Prisco G (2003) The pharmacology of vertebrate spinal central pattern generators. Neuroscientist 9:217–228

    Article  CAS  PubMed  Google Scholar 

  • Amemiya CT, Prohaska SJ, Hill-Force A, Cook A, Wasserscheid J, Ferrier DE, Pascual-Anaya J, Garcia-Fernandez J, Dewar K, Stadler PF (2008) The amphioxus Hox cluster: characterization, comparative genomics, and evolution. J Exp Zool B Mol Dev Evol 310:465–477

    Article  PubMed  CAS  Google Scholar 

  • Arendt D, Denes AS, Jékely G, Tessmar-Raible K (2008) The evolution of nervous system centralization. Philos Trans R Soc Lond B Biol Sci 363:1523–1528

    Article  PubMed  PubMed Central  Google Scholar 

  • Bateson W (1886) The ancestry of the chordata. Q J Microsc Sci 26:535–571

    Google Scholar 

  • Begbie J (2008) Migration of neuroblasts from neurogenic placodes. Dev Neurosci 30:33–35

    Article  CAS  PubMed  Google Scholar 

  • Bertrand S, Escriva H (2011) Evolutionary crossroads in developmental biology: amphioxus. Development 138:4819–4830

    Article  CAS  PubMed  Google Scholar 

  • Bisgrove BW, Burke RD (1986) Development of serotonergic neurons in embryos of the sea urchin Strongylocentrotus purpuratus. Dev Growth Differ 28:569–574

    Article  Google Scholar 

  • Bisgrove BW, Burke RD (1987) Development of the nervous system of the pluteus larva of Strongylocentrotus droebachiensis. Cell Tissue Res 248:335–343

    Article  Google Scholar 

  • Bohn JM, Heinzeller T (1999) Morphology of the bourgueticrinid and isocrinid aboral nervous system and its possible phylogenetic implications (Echinodermata, Crinoidea). Acta Zool 80:241–249

    Article  Google Scholar 

  • Bourlat SJ, Juliusdottir T, Lowe CJ, Freeman R, Aronowicz J, Kirschner M, Lander ES, Thorndyke M, Nakano H, Khon AB, Heyland A, Moroz LL, Copley RR, Telford MJ (2006) Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444:85–88

    Article  CAS  PubMed  Google Scholar 

  • Bronner ME, Le Douarin NM (2012) Evolution and development of the neural crest: an overview. Dev Biol 366:2–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown ER, Nishino A, Bone Q, Meinertzhagen IA, Okamura Y (2005) GABAergic synaptic transmission modulates swimming in the ascidian larva. Eur J Neurosci 22:2541–2548

    Article  CAS  PubMed  Google Scholar 

  • Brown FD, Prendergast A, Swalla BJ (2008) Man is but a worm: chordate origins. Genesis 46:605–613

    Article  PubMed  Google Scholar 

  • Buchanan JT (1999) Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord. J Neurophysiol 81:2037–2045

    CAS  PubMed  Google Scholar 

  • Bullock TH (1944) The giant nerve fiber system in balanoglossids. J Comp Neurol 80:355–367

    Article  Google Scholar 

  • Bullock TH (1965) The nervous system of hemichordates. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous systems of invertebrates. Freeman, San Francisco/London, pp 1567–1577

    Google Scholar 

  • Burke RD, Brand DG, Bisgrove BW (1986) Structure of the nervous system of the auricularia larva of Parasticopus californicus. Biol Bull 170:450–460

    Article  Google Scholar 

  • Burke RD, Angerer LM, Elphick MR, Humphrey GW, Yaguchi S, Kiyama T, Liang S, Mu X, Agca C, Klein WH, Brandhorst BP, Rowe M, Wilson K, Churcher AM, Taylor JS, Chen N, Murray G, Wang D, Mellott D, Olinski R, Hallböök F, Thorndyke MC (2006) A genomic view of the sea urchin nervous system. Dev Biol 300:434–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrne M, Nakajima Y, Chee FC, Burke RD (2007) Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria. Evol Dev 9:432–445

    Article  PubMed  Google Scholar 

  • Cameron CB (2002) Particle retention and flow in the pharynx of the enteropneust worm Harrimania planktophilus: the filter-feeding pharynx may have evolved before the chordates. Biol Bull 202:192–200

    Article  PubMed  Google Scholar 

  • Cameron CB, Garey JR, Swalla BJ (2000) Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla. Proc Natl Acad Sci USA 97:4469–4474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cannon JT, Vellutini BC, Smith J III, Ronquist F, Jondelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530:89–93

    Article  CAS  PubMed  Google Scholar 

  • Castro LFC, Rasmussen SLK, Holland PWH, Holland ND, Holland LZ (2006) A Gbx homeobox gene in amphioxus: insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Dev Biol 295:40–51

    Article  CAS  PubMed  Google Scholar 

  • Chia FS, Burke RD (1978) Echinoderm metamorphosis: fate of larval structures. In: Chia FS, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier-North Holland, New York, pp 219–234

    Google Scholar 

  • Cisternas P, Byrne M (2009) Expression of Hox4 during development of the pentamerous juvenile sea star, Parvulastra exigua. Dev Genes Evol 219:613–618

    Article  CAS  PubMed  Google Scholar 

  • Cole AG, Meinertzhagen IA (2004) The central nervous system of the ascidian larva: mitotic history of cells forming the neural tube in the late embryonic Ciona intestinalis. Dev Biol 271:239–262

    Article  CAS  PubMed  Google Scholar 

  • Conway Morris S (1982) Atlas of the Burgess shale. Palaeontological Association, London

    Google Scholar 

  • Dale N (1985) Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord. J Physiol 363:61–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D’Aniello S, D’Aniello E, Locascio A, Memoli A, Corrado M, Russo MT, Aniello F, Fucci L, Brown ER, Branno M (2006) The ascidian homolog of the vertebrate homeobox gene Rx is essential for ocellus development and function. Differentiation 74:222–234

    Article  PubMed  CAS  Google Scholar 

  • Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B et al (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157–2167

    Article  CAS  PubMed  Google Scholar 

  • Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relative of vertebrates. Nature 439:965–968

    Article  CAS  PubMed  Google Scholar 

  • Denes AS, Jekely G, Steinmetz PR, Raible F, Snyman H, Prud’-homme B, Ferrier DE, Balavoine G, Arendt D (2007) Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in Bilateria. Cell 129:277–288

    Article  CAS  PubMed  Google Scholar 

  • Devlin CL (2001) The pharmacology of γ-aminobutyric acid and acetylcholine receptors at the echinoderm neuromuscular junction. J Exp Biol 204:887–896

    CAS  PubMed  Google Scholar 

  • Dilly N (1961) Electron microscope observations of the receptors in the sensory vesicle of the ascidian tadpole. Nature 191:786–787

    Article  Google Scholar 

  • Dilly N (1964) Studies on the receptors in the cerebral vesicle of the ascidian tadpole. 2. The ocellus. Q J Microsc Sci 105:13–20

    Google Scholar 

  • Dufour HD, Chettouh Z, Deyts C, de Rosa R, Goridis C, Joly JS, Brunet JF (2006) Precraniate origin of cranial motoneurons. Proc Natl Acad Sci USA 103:8727–8732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eakin RM, Kuda A (1971) Ultrastructure of sensory receptors in ascidian tadpoles. Z Zellforsch 112:287–312

    Article  CAS  PubMed  Google Scholar 

  • Echelard Y, Epstein DJ, St.-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417–1430

    Article  CAS  PubMed  Google Scholar 

  • Elphick MR, Egertova M (2001) The neurobiology and evolution of cannabinoid signalling. Philos Trans R Soc Lond B Biol Sci 356:381–408

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elphick MR, Egertova M (2005) The phylogenetic distribution and evolutionary origins of endocannabinoid signalling. Handb Exp Pharmacol 168:283–297

    Article  CAS  Google Scholar 

  • Elphick MR, Melarange R (2001) Neural control of muscle relaxation in echinoderms. J Exp Biol 204:875–885

    CAS  PubMed  Google Scholar 

  • Elphick MR, Price DA, Lee TD, Thorndyke MC (1991) The SALMFamides: a new family of neuropeptides isolated from an echinoderm. Philos Trans R Soc Lond B Biol Sci 243:121–127

    Article  CAS  Google Scholar 

  • Elphick MR, Satou Y, Satoh N (2003) The invertebrate ancestry of endocannabinoid signalling: an orthologue of vertebrate cannabinoid receptors in the urochordate Ciona intestinalis. Gene 302:95–101

    Article  CAS  PubMed  Google Scholar 

  • Ferrier DEK, Brooke NM, Panopoulou G, Holland PWH (2001) The Mnx homeobox gene class defined by HB9, MNR2 and amphioxus AmphiMnx. Dev Genes Evol 211:103–107

    Article  CAS  PubMed  Google Scholar 

  • Florey E, Cahill MA, Rathmayer M (1975) Excitatory actions of GABA and of acetylcholine in sea urchin tube feet. Comp Biochem Physiol 51C:5–12

    Google Scholar 

  • Garcia-Fernandez J, Holland PWH (1994) Archetypal organization of the amphioxus Hox gene cluster. Nature 370:563–566

    Article  CAS  PubMed  Google Scholar 

  • Garstang W (1894) Preliminary note on a new theory of the ancestry of the Chordata. Zool Anz 17:122–125

    Google Scholar 

  • Gorman AL, McReynolds JS, Barnes SN (1971) Photoreceptors in primitive chordates: fine structure, hyperpolarizing receptor potentials, and evolution. Science 172:1052–1054

    Article  CAS  PubMed  Google Scholar 

  • Green SA, Simoes-Costa M, Bronner ME (2015) Evolution of vertebrates as viewed from the crest. Nature 520:474–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grillner S, Deliagina T, Ekeberg O, El Manira A, Hill RH, Lansner A, Orlovsky GN, Wallen P (1995) Neural networks that co-ordinate locomotion and body orientation in lamprey. Trends Neurosci 18:270–279

    Article  CAS  PubMed  Google Scholar 

  • Halanych KM (1995) The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Mol Phylogenet Evol 4:72–76

    Article  CAS  PubMed  Google Scholar 

  • Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186–193

    Article  CAS  PubMed  Google Scholar 

  • Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond B 267:1071–1079

    Article  CAS  Google Scholar 

  • Heinzeller T, Welsch U (2001) The echinoderm nervous system and its phylogenetic interpretation. In: Roth G, Wulliman WF (eds) Brain evolution and cognition. Wiley-Spektrum, New York/Heidelberg, pp 41–75

    Google Scholar 

  • Hirokawa T, Komatsu M, Nakajima Y (2008) Development of the nervous system in the brittle star Amphipholis kochii. Dev Genes Evol 218:15–21

    Article  PubMed  Google Scholar 

  • Holland LZ (2009) Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat Rev Genet 10:736–746

    Article  CAS  Google Scholar 

  • Holland LZ (2015) Evolution of basal deuterostome nervous systems. J Exp Biol 218(pt 4):637–645

    Article  PubMed  Google Scholar 

  • Holland ND, Panganiban G, Henyey EL, Holland LZ (1996) Sequence and developmental expression of AmphiDll, an amphioxus distal-less gene transcribed in the ectoderm, epidermis and nervous system: insights into evolution of craniate forebrain and neural crest. Development 122:2911–2920

    CAS  PubMed  Google Scholar 

  • Holland LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK (2013) Evolution of bilaterian central nervous systems: a single origin? Evodevo 4:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Horie T, Orii H, Nakagawa M (2005) Structure of photoreceptors in the ascidian Ciona intestinalis larva revealed by an anti-arrestin antibody. J Neurobiol 65:241–250

    Article  CAS  PubMed  Google Scholar 

  • Horie T, Kusakabe T, Tsuda M (2008a) Glutamatergic networks in the Ciona intestinalis larva. J Comp Neurol 508:249–263

    Article  CAS  PubMed  Google Scholar 

  • Horie T, Sakurai D, Ohtsuki H, Terakita A, Shichida Y, Usukura J, Kusakabe T, Tsuda M (2008b) Pigmented and nonpigmented ocelli in the brain vesicle of the ascidian larva. J Comp Neurol 509:88–102

    Article  PubMed  Google Scholar 

  • Horie T, Nakagwa M, Sasakura Y, Kusakabe TG (2009) Cell type and function of neurons in the ascidian nervous system. Dev Growth Differ 51:207–220

    Article  CAS  PubMed  Google Scholar 

  • Horie T, Nakagawa M, Sasakura Y, Kusakabe TG, Tsuda M (2010) Simple motor system of the ascidian larva: neuronal complex comprising putative cholinergic neurons and GABAergic/glycinergic neurons. Zool Sci 27:181–190

    Article  CAS  PubMed  Google Scholar 

  • Horie T, Shinki R, Ogura Y, Kusakabe TG, Satoh N, Sasakura Y (2011) Ependymal cells of chordate larvae are stem-like cells that form the adult nervous system. Nature 469:525–528

    Article  CAS  PubMed  Google Scholar 

  • Hyman LH (1955) The invertebrates. Echinodermata: the coelomate Bilateria, vol 4. McGraw-Hill, New York

    Google Scholar 

  • Ikuta T, Saiga H (2007) Dynamic change in the expression of developmental genes in the ascidian central nervous system: revisit to the tripartite model and the origin of the midbrain-hindbrain boundary region. Dev Biol 312:631–643

    Article  CAS  PubMed  Google Scholar 

  • Imai JH, Meinertzhagen IA (2007) Neurons of the ascidian larval nervous system in Ciona intestinalis: I. Central nervous system. J Comp Neurol 501:316–334

    Article  CAS  PubMed  Google Scholar 

  • Imai KS, Satoh N, Satou Y (2002) Region specific gene expressions in the central nervous system of the ascidian embryo. Gene Expr Patterns 2:319–321

    Article  CAS  PubMed  Google Scholar 

  • Inada K, Horie T, Kusakabe T, Tsuda M (2003) Targeted knockdown of an opsin gene inhibits the swimming behaviour photoresponse of ascidian larvae. Neurosci Lett 347:167–170

    Article  CAS  PubMed  Google Scholar 

  • Irimia M, Piñeiro C, Maeso I, Gómez-Skarmeta JL, Casares F, Garcia-Fernàndez J (2010) Conserved developmental expression of fezf in chordates and Drosophila and the origin of the zona limitans intrathalamica (ZLI) brain organizer. Evodevo 1:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivashkin E, Adameyko I (2013) Progenitors of the protochordate ocellus as an evolutionary origin of the neural crest. Evodevo 4:12

    Article  PubMed  PubMed Central  Google Scholar 

  • Jefferies RPS (1991) In: Bock GR, Marsh J (eds) Biological asymmetry and handedness. Wiley, Chichester, pp 94–127

    Google Scholar 

  • Jeffery WR (2006) Ascidian neural crest-like cells: phylogenetic distribution, relationship to larval complexity, and pigment cell fate. J Exp Zool B Mol Dev Evol 306:470–480

    Article  PubMed  CAS  Google Scholar 

  • Jeffery WR, Strickler AG, Yamamoto Y (2004) Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431:696–699

    Article  CAS  PubMed  Google Scholar 

  • Jeffery WR, Chiba T, Razy-Krajka F, Deyts C, Satoh N, Joly JS (2008) Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: insights into the ancestry and evolution of the neural crest. Dev Biol 324:152–160

    Article  CAS  PubMed  Google Scholar 

  • Joly JS, Osorio J, Alunni A, Auger H, Kano S, Retaux S (2007) Windows of the brain: towards a developmental biology of circumventricular and other neurohemal organs. Semin Cell Dev Biol 18:512–524

    Article  PubMed  Google Scholar 

  • Kajiwara S, Yoshida M (1985) Change in behavior and ocellar structure during the larval life of solitary ascidians. Biol Bull 169:565–577

    Article  Google Scholar 

  • Kaltenbach SL, Yu JK, Holland ND (2009) The origin and migration of the earliest-developing sensory neurons in the peripheral nervous system of amphioxus. Evol Dev 11:142–151

    Article  PubMed  Google Scholar 

  • Kamiya C, Ohta N, Ogura Y, Yoshida K, Horie T, Kusakabe TG, Satake H, Sasakura Y (2014) Nonreproductive role of gonadotropin-releasing hormone in the control of ascidian metamorphosis. Dev Dyn 243:1524–1535

    Article  CAS  PubMed  Google Scholar 

  • Kappers CUA (1929) The evolution of the nervous system in invertebrates, vertebrates and man. Bohn, Haarlem

    Google Scholar 

  • Katow H, Yaguchi S, Kyozuka K (2007) Serotonin stimulates [Ca2+]i elevation in ciliary ectodermal cells of echinoplutei through a serotonin receptor cell network in the blastocoel. J Exp Biol 210:403–412

    Article  CAS  PubMed  Google Scholar 

  • Katow H, Suyemitsu T, Ooka S, Yaguchi J, Jin-Nai T, Kuwahara I, Katow T, Yaguchi S, Abe H (2010) Development of a dopaminergic system in sea urchin embryos and larvae. J Exp Biol 213:2808–2819

    Article  CAS  PubMed  Google Scholar 

  • Katow H, Abe K, Katow T, Zamani A, Abe H (2013) Development of the GABA-ergic signaling system and its role in larval swimming in sea urchin. J Exp Biol 216:1704–1716

    Article  CAS  PubMed  Google Scholar 

  • Katz MJ (1983) Comparative anatomy of the tunicate tadpole Ciona intestinalis. Biol Bull 164:1–27

    Article  Google Scholar 

  • Kaul S, Stach T (2010) Ontogeny of the collar cord: neurulation in the hemichordate Saccoglossus kowalevskii. J Morphol 271:1240–1259

    Article  PubMed  Google Scholar 

  • Kon T, Nohara M, Yamanoue Y, Fujiwara Y, Nishida M, Nishikawa T (2007) Phylogenetic position of a whale-fall lancelet (Cephalochordata) inferred from whole mitochondrial genome sequences. BMC Evol Biol 7:127

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kusakabe T, Tsuda M (2007) Photoreceptive systems in ascidians. Photochem Photobiol 83:248–252

    Article  CAS  PubMed  Google Scholar 

  • Kusakabe T, Kusakabe R, Kawakami I, Satou Y, Satoh N, Tsuda M (2001) Ci-opsin1, a vertebrate-type opsin gene, expressed in the larval ocellus of the ascidian Ciona intestinalis. FEBS Lett 506:69–72

    Article  CAS  PubMed  Google Scholar 

  • Kusakabe T, Mishima S, Shimada I, Kitajima Y, Tsuda M (2003) Structure, expression, and cluster organization of genes encoding gonadotropin-releasing hormone receptors found in the neural complex of the ascidian Ciona intestinalis. Gene 322:77–84

    Article  CAS  PubMed  Google Scholar 

  • Kusakabe TG, Takimoto N, Jin M, Tsuda M (2009) Evolution and the origin of the visual retinoid cycle in vertebrates. Philos Trans R Soc Lond B Biol Sci 364:2897–2910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusakabe TG, Sakai T, Aoyama M, Kitajima Y, Miyamoto Y, Takigawa T, Daido Y, Fujiwara K, Terashima Y, Sugiuchi Y, Matassi G, Yagisawa H, Park MK, Satake H, Tsuda M (2012) A conserved non-reproductive GnRH system in chordates. PLoS One 7:e41955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacalli TC (2002) The dorsal compartment locomotory control system in amphioxus larvae. J Morphol 252:227–237

    Article  PubMed  Google Scholar 

  • Lacalli TC (2003) Ventral neurons in the anterior nerve cord of amphioxus larvae. II. Further data on the pacemaker circuit. J Morphol 257:212–218

    Article  PubMed  Google Scholar 

  • Lacalli TC (2006) Prospective protochordate homologs of vertebrate midbrain and MHB, with some thoughts on MHB origins. Int J Biol Sci 2:104–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacalli TC (2008) Basic features of the ancestral chordate brain: a protochordate perspective. Brain Res Bull 75:319–323

    Article  PubMed  Google Scholar 

  • Lacalli TC, Kelly SJ (2003) Ventral neurons in the anterior nerve cord of amphioxus larvae. I. An inventory of cell types and synaptic patterns. J Morphol 257:190–211

    Article  CAS  PubMed  Google Scholar 

  • Lacalli TC, West JE (1993) A distinctive nerve cell type common to diverse deuterostome larvae: comparative data from echinoderms, hemichordates and amphioxus. Acta Zool 74:1–8

    Article  Google Scholar 

  • Lacalli TC, Gilmour THJ, West JE (1990) Ciliary band innervation in the bipinnaria larva of Pisaster ochraceus. Philos Trans R Soc B Biol Sci 330:371–390

    Article  Google Scholar 

  • Legendre P (2001) The glycinergic inhibitory synapse. Cell Mol Life Sci 58:760–793

    Article  CAS  PubMed  Google Scholar 

  • Lester S (1988) Settlement and metamorphosis of Rhabdopleura normani (Hemichordata: Pterobranchia). Acta Zool 69:111–120

    Article  Google Scholar 

  • Lowe CJ (2008) Molecular genetic insights into deuterostome evolution from the direct-developing hemichordate Saccoglossus kowalevskii. Philos Trans R Soc Lond B Biol Sci 363:1569–1578

    Article  PubMed  PubMed Central  Google Scholar 

  • Lowe CJ, Wu M, Salic A, Evans L, Lander E, Stange-Thomann N, Gruber CE, Gerhart J, Kirschner M (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113:853–865

    Article  CAS  PubMed  Google Scholar 

  • Luttrell S, Konikoff C, Byrne A, Bengtsson B, Swalla BJ (2012) Ptychoderid hemichordate neurulation without a notochord. Integr Comp Biol 52:829–834

    Article  PubMed  Google Scholar 

  • Mackie GO, Spencer AN, Strathmann R (1969) Electrical activity associated with ciliary reversal in an echinoderm larva. Nature 223:1384–1385

    Article  Google Scholar 

  • Manni L, Lane NJ, Gasparini F, Tiozzo S, Caicci F, Zaniolo G, Burighel P (2004a) Neurogenic and nonneurogenic placodes in ascidians. J Exp Zool B Mol Dev Evol 302:483–504

    Article  PubMed  Google Scholar 

  • Manni L, Caicci F, Gasparini F, Zaniolo G, Burighel P (2004b) Hair cells in ascidians and the evolution of lateral line placodes. Evol Dev 6:379–381

    Article  PubMed  Google Scholar 

  • Manni L, Agnoletto A, Zaniolo G, Burighel P (2005) Stomodeal and neurohypophysial placodes in Ciona intestinalis: insights into the origin of the pituitary gland. J Exp Zool B Mol Dev Evol 304:324–339

    Article  PubMed  Google Scholar 

  • Mazet F, Shimeld S (2005) Molecular evidence from ascidians for the evolutionary origin of vertebrate cranial sensory placodes. J Exp Zool B Mol Dev Evol 304:340–346

    Article  PubMed  CAS  Google Scholar 

  • Mazet F, Hutt JA, Milloz J, Millard J, Graham A, Shimeld SM (2005) Molecular evidence from Ciona intestinalis for the evolutionary origin of vertebrate cranial placodes. Dev Biol 282:494–508

    Article  CAS  PubMed  Google Scholar 

  • Metchnikoff E (1881) Ãœber die systematische Stellung von Balanoglossus. Zool Anz 4:153–157

    Google Scholar 

  • Meinertzhagen IA, Okamura Y (2001) The larval ascidian nervous system: the chordate brain from its small beginnings. Trends Neurosci 24:401–410

    Article  CAS  PubMed  Google Scholar 

  • Meinertzhagen IA, Lemaire P, Okamura Y (2004) The neurobiology of the ascidian tadpole larva: recent developments in an ancient chordate. Annu Rev Neurosci 27:453–485

    Article  CAS  PubMed  Google Scholar 

  • Moret F, Christiaen L, Deyts C, Blin M, Joly JS, Vernier P (2005a) 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. Eur J Neurosci 21:3043–3055

    Article  PubMed  Google Scholar 

  • Moret F, Christiaen L, Deyts C, Blin M, Vernier P, Joly JS (2005b) Regulatory gene expressions in the ascidian ventral sensory vesicle: evolutionary relationships with the vertebrate hypothalamus. Dev Biol 277:567–579

    Article  CAS  PubMed  Google Scholar 

  • Morgan TH (1891) The growth and development of tornaria. J Morphol 5:407–458

    Article  Google Scholar 

  • Morgan TH (1894) Development of Balanoglossus. J Morphol 9:1–86

    Article  Google Scholar 

  • Miyamoto N, Wada H (2013) Hemichordate neurulation and the origin of the neural tube. Nat Commun 4:2713

    PubMed  Google Scholar 

  • Miyamoto N, Nakajima Y, Wada H, Saito Y (2010) Development of the nervous system in the acorn worm Balanoglossus simodensis: insights into nervous system evolution. Evol Dev 12:416–424

    Article  PubMed  Google Scholar 

  • Nakagawa M, Miyamoto T, Ohkuma M, Tsuda M (1999) Action spectrum for the photophobic response of Ciona intestinalis (Ascidiacea, Urochordata) larvae implicates retinal protein. Photochem Photobiol 70:359–362

    Article  CAS  PubMed  Google Scholar 

  • Nakajima Y (1987) Localization of catecholaminergic nerves in larval echinoderms. Zool Sci 4:293–299

    Google Scholar 

  • Nakano H, Murabe N, Amemiya S, Nakajima Y (2006) Nervous system development of the sea cucumber Stichopus japonicus. Dev Biol 292:205–212

    Article  CAS  PubMed  Google Scholar 

  • Nakano H, Nakajima Y, Amemiya S (2009) Nervous system development of two crinoid species, the sea lily Metacrinus rotundus and the feather star Oxycomanthus japonicus. Dev Genes Evol 219:565–576

    Article  PubMed  Google Scholar 

  • Nicol D, Meinertzhagen IA (1988) Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. II. Neural plate morphogenesis and cell lineages during neurulation. Dev Biol 130:737–766

    Article  CAS  PubMed  Google Scholar 

  • Nicol D, Meinertzhagen IA (1991) Cell counts and maps in the larval central nervous system of the ascidian Ciona intestinalis (L.). J Comp Neurol 309:415–429

    Article  CAS  PubMed  Google Scholar 

  • Nielsen C (2006) Homology of echinoderm radial nerve cords and the chordate neural tube? Evol Dev 8:1–2

    Article  PubMed  Google Scholar 

  • Nielsen C (2012) Animal evolution: interrelationships of the living phyla, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Nieuwenhuys R (2002) Deuterostome brains: synopsis and commentary. Brain Res Bull 57:257–270

    Article  PubMed  Google Scholar 

  • Nishino A, Satoh N (2001) The simple tail of chordates: phylogenetic significance of appendicularians. Genesis 29:36–45

    Article  CAS  PubMed  Google Scholar 

  • 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 Neurosci 11:6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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. Dev Growth Differ 54:177–186

    Article  CAS  PubMed  Google Scholar 

  • Nohara M, Nishida M, Miya M, Nishikawa T (2005) Evolution of the mitochondrial genome in Cephalochordata as inferred from complete nucleotide sequences from two Epigonichthys species. J Mol Evol 60:526–537

    Article  CAS  PubMed  Google Scholar 

  • Nomaksteinsky M, Röttinger E, Dufour HD, Chettouh Z, Lowe CJ, Martindale MQ, Brunet JF (2009) Centralization of the deuterostome nervous system predates chordates. Curr Biol 19:1264–1269

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG (2005) The new head hypothesis revisited. J Exp Zool B Mol Dev Evol 304B:274–297

    Article  Google Scholar 

  • Northcutt RG, Gans C (1983) The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q Rev Biol 58:1–28

    Article  CAS  PubMed  Google Scholar 

  • Ohkuma M, Katagiri Y, Nakagawa M, Tsuda M (2000) Possible involvement of light regulated gonadotropin-releasing hormone neurons in biological clock for reproduction in the cerebral ganglion of the ascidian, Halocynthia roretzi. Neurosci Lett 293:5–8

    Article  CAS  PubMed  Google Scholar 

  • Ohmori H, Sasaki S (1977) Development of neuromuscular transmission in a larval tunicate. J Physiol 269:221–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohtsuki H (1990) Statocyte and ocellar pigment cell in embryos and larvae of the ascidian, Styela plicata (Lesueur). Dev Growth Differ 32:85–90

    Article  Google Scholar 

  • Oka Y (1997) The gonadotropin-releasing hormone (GnRH) neuronal system of fish brain as a model system for the study of peptidergic neuromodulation. In: Parhar IS, Sakuma Y (eds) GnRH neurons: genes to behavior. Brain Shuppan, Tokyo, pp 245–276

    Google Scholar 

  • Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ (2012) Ancient deuterostome origins of vertebrate brain signalling centres. Nature 483:289–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul CRC, Smith AB (1984) The early radiation and phylogeny of echinoderms. Biol Rev 59:443–481

    Article  Google Scholar 

  • Pearce CM, Scheibling RE (1990) Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. Biol Bull 179:304–311

    Article  Google Scholar 

  • Pennati R, Groppelli S, Sotgia C, Candiani S, Pestarino M, De Bernardi F (2001) Serotonin localization in Phallusia mammillata larvae and effects of 5-HT antagonists during larval development. Dev Growth Differ 43:647–656

    Article  CAS  PubMed  Google Scholar 

  • Pennati R, Candiani S, Biggiogero M, Zega G, Groppelli S, Oliveri D, Parodi M, De Bernardi F, Pestarino M (2007) Developmental expression of tryptophan hydroxylase gene in Ciona intestinalis. Dev Genes Evol 217:307–313

    Article  CAS  PubMed  Google Scholar 

  • Perseke M, Golombek A, Schlegel M, Struck TH (2013) The impact of mitochondrial genome analyses on the understanding of deuterostome phylogeny. Mol Phylogenet Evol 66:898–905

    Article  PubMed  Google Scholar 

  • Philippe H, Brinkmann H, Martinez P, Riutort M, Baguñà J (2007) Acoel flatworms are not platyhelminthes: evidence from phylogenomics. PLoS ONE 2:e717

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Philippe H, Brinkmann H, Copley RR, Moroz LL, Nakano H, Poustka AJ, Wallberg A, Peterson KJ, Telford MJ (2011) Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 470:255–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Powell JFF, Reska-Skinner SM, Prakash MO, Fischer WH, Park M et al (1996) Two new forms of gonadotropin-releasing hormone in a protochordate and the evolutionary implications. Proc Natl Acad Sci USA 93:10461–10464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Protas LL, Muske GA (1980) The effects of some transmitter substances on the tube foot muscles of the starfish, Asterias amurensis (Lutken). Gen Pharmacol 11:113–118

    Article  CAS  PubMed  Google Scholar 

  • Quinlan KA, Kiehn O (2007) Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J Neurosci 27:6521–6530

    Article  CAS  PubMed  Google Scholar 

  • Raff RA (2008) Origin of the other metazoan body plans: the evolution of larval forms. Philos Trans R Soc Lond B Biol Sci 363:1473–1479

    Article  PubMed  PubMed Central  Google Scholar 

  • Razy-Krajka F, Brown ER, Horie T, Callebert J, Sasakura Y, Joly J-S, Kusakabe TG, Vernier P (2012) Monoaminergic modulation of photoreception in ascidian: evidence for a proto-hypothalamo-retinal territory. BMC Biol 10:45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rebelo S, Reguenga C, Osorio L, Pereira C, Lopes C, Lima D (2007) DRG11 immunohistochemical expression during embryonic development in the mouse. Dev Dyn 236:2653–2660

    Article  CAS  PubMed  Google Scholar 

  • Roberts A (2000) Early functional organization of spinal neurons in developing lower vertebrates. Brain Res Bull 53:585–593

    Article  CAS  PubMed  Google Scholar 

  • Roch GJ, Tello JA, Sherwood NM (2014) At the transition from invertebrates to vertebrates, a novel GnRH-like peptide emerges in amphioxus. Mol Biol Evol 31:765–778

    Article  CAS  PubMed  Google Scholar 

  • Rouse GW, Wilson NG, Carvajal JI, Vrijenhoek RC (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature 530:94–97

    Article  CAS  PubMed  Google Scholar 

  • Saito T, Greenwood A, Sun Q, Anderson DJ (1995) Identification by differential RT-PCR of a novel paired homeodomain protein specifically expressed in sensory neurons and a subset of their CNS targets. Mol Cell Neurosci 6:280–292

    Article  CAS  PubMed  Google Scholar 

  • Sakurai D, Goda M, Kohmura Y, Horie T, Iwamoto H, Ohtsuki H, Tsuda M (2004) The role of pigment cells in the brain of ascidian larva. J Comp Neurol 475:70–82

    Article  PubMed  Google Scholar 

  • Satoh N (2009) An advanced filter-feeder hypothesis for urochordate evolution. Zool Sci 26:97–111

    Article  PubMed  Google Scholar 

  • Satoh N, Rokhsar D, Nishikawa T (2014) Chordate evolution and the three-phylum system. Proc R Soc B 281:20141729

    Article  PubMed  PubMed Central  Google Scholar 

  • Satterlie RA (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generation. Science 229:402–404

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G (2005) Evolutionary origins of vertebrate placodes: insights from developmental studies and from comparisons with other deuterostomes. J Exp Zool B Mol Dev Evol 304B:347–399

    Article  CAS  Google Scholar 

  • Schlosser G (2006) Induction and specification of cranial placodes. Dev Biol 294(2):303–351

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G (2008) Do vertebrate neural crest and cranial placodes have a common evolutionary origin? BioEssays 30:659–672

    Article  CAS  PubMed  Google Scholar 

  • Schlosser G (2010) Making senses development of vertebrate cranial placodes. Int Rev Cell Mol Biol 283:129–234

    Article  CAS  PubMed  Google Scholar 

  • Schuske K, Beg AA, Jorgensen EM (2004) The GABA nervous system in C. elegans. Trends Neurosci 27:407–414

    Article  CAS  PubMed  Google Scholar 

  • Shu DG, Conway Morris S, Zhang XL (1996) A Pikaia-like chordate from the Lower Cambrian of China. Nature 348:157–158

    Article  Google Scholar 

  • Sly BJ, Hazel JC, Popodi EM, Raff RA (2002) Patterns of gene expression in the developing adult sea urchin central nervous system reveal multiple domains and deep-seated neural pentamery. Evol Dev 4:189–204

    Article  CAS  PubMed  Google Scholar 

  • Smith JE (1965) Echinodermata. In: Bullock TH, Horridge GA (eds) Structure and function in the nervous systems of invertebrates. Freeman, London, pp 1519–1558

    Google Scholar 

  • Soffe SR, Clarke JDW, Roberts A (1984) Activity of commissural interneurons in the spinal cord of Xenopus embryos. J Neurophysiol 51:1257–1267

    CAS  PubMed  Google Scholar 

  • Stach T (2005) Comparison of the serotonergic nervous system among Tunicata: implications for its evolution within Chordata. Org Divers Evol 5:15–24

    Article  Google Scholar 

  • Stach T, Winter J, Bouquet JM, Chourrout D, Schnabel R (2008) Embryology of a planktonic tunicate reveals traces of sessility. Proc Natl Acad Sci USA 105:7229–7234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolfi A, Levine M (2011) Neuronal subtype specification in the spinal cord of a protovertebrate. Development 138:995–1004

    Article  CAS  PubMed  Google Scholar 

  • Stolfi A, Ryan K, Meinertzhagen IA, Christiaen L (2015) Migratory neuronal progenitors arise from the neural plate borders in tunicates. Nature 527:371–374

    Google Scholar 

  • Strathmann RR (1975) Larval feeding in echinoderms. Am Zool 15:717–730

    Article  Google Scholar 

  • Svane I, Young CM (1989) The ecology and behavior of ascidian larvae. Oceanogr Mar Biol Rev 27:45–90

    Google Scholar 

  • Swalla BJ, Cameron CB, Corley LS, Garey JR (2000) Urochordates are monophyletic within the deuterostomes. Syst Biol 49:122–134

    Google Scholar 

  • Takahashi T, Holland PWH (2004) Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origin of midbrain development. Development 131:3285–3294

    Article  CAS  PubMed  Google Scholar 

  • Takamura K (1998) Nervous network in larvae of the ascidian Ciona intestinalis. Dev Genes Evol 208:1–8

    Article  CAS  PubMed  Google Scholar 

  • Takamura K, Egawa T, Ohnishi S, Okada T, Fukuoka T (2002) Developmental expression of ascidian neurotransmitter synthesis genes. I. Choline acetyltransferase and acetylcholine transporter genes. Dev Genes Evol 212:50–53

    Article  CAS  PubMed  Google Scholar 

  • Takamura K, Minamida N, Okabe S (2010) Neural map of the larval central nervous system in the ascidian Ciona intestinalis. Zool Sci 27:191–203

    Article  CAS  PubMed  Google Scholar 

  • Tanabe Y, William C, Jessell TM (1998) Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95:67–80

    Article  CAS  PubMed  Google Scholar 

  • Tello JA, Sherwood NM (2009) Amphioxus: beginning of vertebrate and end of invertebrate type GnRH receptor lineage. Endocrinology 150:2847–2856

    Article  CAS  PubMed  Google Scholar 

  • Tello JA, Rivier JE, Sherwood NM (2005) Tunicate gonadotropin-releasing hormone (GnRH) peptides selectively activate Ciona intestinalis GnRH receptors and the green monkey type II GnRH receptor. Endocrinology 146:4061–4067

    Article  CAS  PubMed  Google Scholar 

  • Terakado K (2001) Induction of gamete release by gonadotropin-releasing hormone in a protochordate, Ciona intestinalis. Gen Comp Endocrinol 124:277–284

    Article  CAS  PubMed  Google Scholar 

  • Thor S, Thomas JB (2002) Motor neuron specification in worms, flies and mice: conserved and ‘lost’ mechanisms. Curr Opin Genet Dev 12:558–564

    Article  CAS  PubMed  Google Scholar 

  • Tsuda M (1987) Photoreception and phototransduction in invertebrate photoreceptors. Photochem Photobiol 45:915–931

    Article  CAS  Google Scholar 

  • Tsuda M, Kawakami I, Shiraishi S (2003a) Sensitization and habituation of the swimming behavior in ascidian larvae to light. Zool Sci 20:13–22

    Article  PubMed  Google Scholar 

  • Tsuda M, Sakurai D, Goda M (2003b) Direct evidence for the role of pigment cells in the brain of ascidian larvae by laser ablation. J Exp Biol 206:1409–1417

    Article  PubMed  Google Scholar 

  • Tsutsui H, Yamamoto N, Ito H, Oka Y (1998) GnRH-immunoreactive neuronal system in the presumptive ancestral chordate, Ciona intestinalis (ascidian). Gen Comp Endocrinol 112:426–432

    Article  CAS  PubMed  Google Scholar 

  • Varju P, Katarova Z, Madarasz E, Szabo G (2001) GABA signaling during development: new data and old questions. Cell Tissue Res 305:239–246

    Article  CAS  PubMed  Google Scholar 

  • Vigh B, Manzano MJ, Zadori A, Frank CL, Lukats A, Rohlich P, Szel A, David C (2002) Non visual photoreceptors of the deep brain, pineal organs and retina. Histol Histopathol 17:555–590

    CAS  PubMed  Google Scholar 

  • Vopalensky P, Pergner J, Liegertova M, Benito-Gutierrez E, Arendt D, Kozmik Z (2012) Molecular analysis of the amphioxus frontal eye unravels the evolutionary origin of the retina and pigment cells of the vertebrate eye. Proc Natl Acad Sci USA 109:15383–15388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wada H, Satoh N (1994) Details of the evolutionary history from invertebrates to vertebrates, as deduced from the sequences of 18S rDNA. Proc Natl Acad Sci USA 91:1801–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wada H, Saiga H, Satoh N, Holland PWH (1998) Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development 125:1113–1122

    CAS  PubMed  Google Scholar 

  • Wada H, Garcia-Fernàndez J, Holland PWH (1999) Colinear and segmental expression of amphioxus Hox genes. Dev Biol 213:131–141

    Article  CAS  PubMed  Google Scholar 

  • Whittaker JR (1973) Segregation during ascidian embryogenesis of egg cytoplasmic information for tissue-specific enzyme development. Proc Natl Acad Sci USA 70:2096–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wicht H, Lacalli TC (2005) The nervous system of amphioxus: structure, development, and evolutionary significance. Can J Zool 83:122–150

    Article  Google Scholar 

  • Wickstead JH, Bone Q (1959) Ecology of acraniate larvae. Nature 184:1849–1851

    Article  Google Scholar 

  • Wilson DM (1961) The central nervous control of flight in a locust. J Exp Biol 38:471–479

    Google Scholar 

  • Wilson JM, Hartley R, Maxwell DJ, Todd AJ, Lieberam I, Kaltschmidt JA, Yoshida Y, Jessell TM, Brownstone RM (2005) Conditional rhythmicity of ventral spinal interneurons defined by expression of the Hb9 homeodomain protein. J Neurosci 25:5710–5719

    Article  CAS  PubMed  Google Scholar 

  • Yoshida R, Sakurai D, Horie T, Kawakami I, Tsuda M, Kusakabe T (2004) Identification of neuron-specific promoters in Ciona intestinalis. Genesis 39:130–140

    Article  CAS  PubMed  Google Scholar 

  • Yu JK, Satou Y, Holland ND, Shin-i T, Kohara Y, Satoh N, Bronner-Fraser M, Holland LZ (2007) Axial patterning in cephalochordates and the evolution of the organizer. Nature 445:613–617

    Article  CAS  PubMed  Google Scholar 

  • Zega G, Penatti R, Groppelli S, Sotgia C, De Bernardi F (2005) Dopamine and serotonin modulate the onset of metamorphosis in the ascidian Phallusia mammillata. Dev Biol 282:246–256

    Article  CAS  PubMed  Google Scholar 

  • Zega G, Thorndyke MC, Brown ER (2006) Development of swimming behavior in the larva of the ascidian Ciona intestinalis. J Exp Biol 209:3405–3412

    Article  PubMed  Google Scholar 

  • Zega G, Biggiogero M, Groppelli S, Candiani S, Oliveri D, Parodi M, Prestarino M, Bernardi F, Pennati R (2008) Delopmental expression of glutamic acid decarboxylase and of γ-aminnobutyric acid type B receptors in the ascidian Ciona intestinalis. J Comp Neurol 506:489–505

    Article  CAS  PubMed  Google Scholar 

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  1. Institute for Integrative Neurobiology & Department of Biology, Faculty of Science and Engineering, Konan University, 8-9-1 Okamoto, Higashinada-ku, Kobe, 658-8501, Japan

    Takehiro G. Kusakabe

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    Shuichi Shigeno

  2. Ehime University, Matsuyama, Japan

    Yasunori Murakami

  3. Kyoto Prefectural University of Medicine, Kyoto, Japan

    Tadashi Nomura

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Kusakabe, T.G. (2017). Identifying Vertebrate Brain Prototypes in Deuterostomes. In: Shigeno, S., Murakami, Y., Nomura, T. (eds) Brain Evolution by Design. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56469-0_7

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