A comparative examination of neural circuit and brain patterning between the lamprey and amphioxus reveals the evolutionary origin of the vertebrate visual center

Journal of Comparative Neurology

Volumn 523, Issue 2, 2015, Pages 251-261

  Suzuki, Daichi G ^a   Murakami, Yasunori ^b   Escriva, Hector ^c   Wada, Hiroshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b EHIME UNIVERSITY   (Japan)

^c CNRS   (France)

Author keywords

Amphioxus; EvoDevo; Lamprey; RRID: AB_10566287; RRID: AB_258008; RRID: AB_261464; RRID: AB_261875; RRID: AB_477522; RRID: AB_477585; Vision

Indexed keywords

COMPLEMENTARY DNA; TRANSCRIPTION FACTOR PAX6; EYE PROTEIN; FISH PROTEIN; HOMEODOMAIN PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; REPRESSOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN PATTERNING; BRANCHIOSTOMA; COMPARATIVE STUDY; CONTROLLED STUDY; DNA ISOLATION; EMBRYO; EVOLUTION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LAMPREY; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; PRIORITY JOURNAL; VERTEBRATE; VISUAL CORTEX; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; METABOLISM; MORPHOGENESIS; RETINA; SPECIES DIFFERENCE; VISUAL SYSTEM;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; BRAIN; EYE PROTEINS; FISH PROTEINS; HOMEODOMAIN PROTEINS; IMMUNOBLOTTING; IN SITU HYBRIDIZATION; LAMPREYS; LANCELETS; OPTIC NERVE; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; RETINA; SPECIES SPECIFICITY; VISUAL PATHWAYS;

EID: 84918816463     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23679     Document Type: Article

References (55)

1. Abalo XM, Villar-Cerviño V, Villar-Cheda B, Anadón R, Rodicio MC. 2008. Neurochemical differentiation of horizontal and amacrine cells during transformation of the sea lamprey retina. J Chem Neuroanat 35:225-232.
2. Barreiro-Iglesias A, Villar-Cheda B, Abalo XM, Anadón R, Rodicio MC. 2008. The early scaffold of axon tracts in the brain of a primitive vertebrate, the sea lamprey. Brain Res Bull 75:42-52.
3. Bone Q. 1960. The central nervous system in amphioxus. J Comp Neurol 115:27-64.
4. Burrill JD, Easter SS Jr. 1994. Development of the retinofugal projections in the embryonic and larval zebrafish (Brachydanio rerio). J Comp Neurol 346:583-600.
5. Candiani S, Moronti L, Ramoino P, Schubert M, Pestarino M. 2012. A neurochemical map of the developing amphioxus nervous system. BMC Neurosci 13:59.
6. Corinide-Petronio ME, Barreiro-Iglesias A, Anadón R, Rodicio MC. 2011. Retinotopy of visual projections to the optic tectum and pretectum in larval sea lamprey. Exp Eye Res 92:274-281.
7. Deguchi T, Suwa H, Yoshimoto M, Kondoh H, Yamamoto N. 2005. Central connection of the optic, oculomotor, trochlear and abducens nerves in medaka, Oryzias latipes. Zool Sci 22:321-332.
8. Deliagina TG, Fagerstedt P. 2000. Responses of reticulospinal neurons in intact lamprey to vestibular and visual inputs. J Neurophysiol 83:864-878.
9. De Miguel E, Rodicio, MC, Anadón R. 1989. Ganglion cells and retinopetal fibers of the larval lamprey retina: an HRP ultrastructual study. Neurosci Lett 106:1-6.
10. De Miguel E, Rodicio, MC, Anadon R. 1990. Organization of the visual system in larval lampreys: an HRP study. J Comp Neurol 302:529-542.
11. Fuentes M, Benito E, Bertrand S, Paris M, Mignardot A, Godoy L, Jimenez-Delgado S, Oliveri D, Candiani S, Hirsinger E, D'Aniello S, Pascual-Anaya J, Maeso I, Pestarino M, Vernier P, Nicolas JF, Schubert M, Laudet V, Geneviere AM, Albalat R, Garcia Fernandez J, Holland ND, Escriva H. 2007. Insights into spawning behavior and development of the European amphioxus (Branchiostoma lanceolatum). J Exp Zool B Mol Dev Evol 308:484-493.
12. Glardon S, Holland LZ, Gehring WJ, Holland ND. 1998. Isolation and developmental expression of the amphioxus Pax-6 gene (AmphiPax-6): insights into eye and photoreceptor evolution. Development 125:2701-2710.
13. Glover JC. 1995. Retrograde and anterograde axonal tracing with fluorescent dextran amines in the embryonic nervous system. Neurosci Protoc 30:1-13.
14. Gustafsson OSE, Collin SP, Kröger RHH. 2008. Early evolution of multifocal optics for well-focused colour vision in vertebrates. J Exp Biol 211:1559-1564.
15. Holland ND, Holland LZ. 1993. Serotonin-containing cells in the nervous system and other tissues during ontogeny of a lancelet, Branchiostoma floridae. Acta Zool 74:195-204.
16. Holland LZ, Carvalho J, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK. 2013. Evolution of bilaterian central nervous systems: a single origin? EvoDevo 4:27.
17. Imai JH, Meinertzhagen IA. 2007. Neurons of the ascidian larval nervous system in Ciona intestinalis: I. Central nervous system. J Comp Neurol 334:316-334.
18. Jones MR, Grillner S, Robertson B. 2009. Selective projection patterns from subtypes of retinal ganglion cells to tectum and pretectum: distribution and relation to behavior. J Comp Neurol 517:257-275.
19. Kaji T, Aizawa S, Uemura M, Yasui K. 2001. Establishment of left-right asymmetric innervation in the lancelet oral region. J Comp Neurol 435:394-405.
20. Kleerekoper H. 1972. The sense organ. In: Hardisty MW, Potter IC, eds. The biology of lampreys, vol. 2. London: Academic Press. p 373-404.
21. Kuratani S, Ueki T, Aizawa S, Hirano S. 1997. Peripheral development of cranial nerves in a cyclostome, Lampetra japonica: morphological distribution of nerve branches and the vertebrate body plan. J Comp Neurol 384:483-500.
22. Kuratani S, Horigome N, Ueki T, Aizawa S, Hirano S. 1998. Stereotyped axonal bundle formation and neuromeric patterns in embryos of a cyclostome, Lampetra japonica. J Comp Neurol 391:99-114.
23. Kusunoki T, Amemiya F. 1983. Retinal projections in the hagfish, Eptatretus burgeri. Brain Res 262:295-298.
24. Lacalli TC. 1996. Frontal eye circuitry, rostral sensory pathways and brain organization in amphioxus larvae: evidence from 3D reconstructions. Philos Trans R Soc Lond B 351:243-263.
25. Lacalli TC. 2001. New perspectives on the evolution of protochordate sonsory and locomotory systems, and the origin of brains and heads. Philos Trans R Soc Lond B 356:1565-1572.
26. Lacalli TC. 2002. Sensory pathways in amphioxus larvae I. Constituent fibres of the rostral and anterodorsal nerves, their targets and evolutionary significance. Acta Zool 83:149-166.
27. Lacalli TC. 2004. Sensory systems in amphioxus: a window on the ancestral chordate condition. Brain Behav Evol 64:148-162.
28. Lacalli TC, Kelly SJ. 1999. Somatic motoneurones in amphioxus larvae: cell types, cell position and innervation patterns. Acta Zool 80:113-124.
29. Lacalli TC, Holland ND, West JE. 1994. Landmarks in the anterior central nervous system of amphioxus larvae. Philos Trans R Soc Lond B 344:165-185.
30. Marlow H, Tosches MA, Tomer R, Steinmets P, Lauri A, Larsson T, Arendt D. 2014. Larval body patterning and apical organs are conserved in animal evolution. BMC Biol 12:7.
31. Mazet F, Hutt J, Millard J, Shimeld S. 2003. Pax gene expression in the developing central nervous system of Ciona intestinalis. Gene Expr Patterns 3:743-745.
32. Melendez-Ferro M, Villar-Cheda B, Abalo XM, Perez-Costas E, Rodriguez-Munoz R., Degrip WJ, Yanez J, Rodicio MC, Anadón R. 2002. Early development of the retina and pineal complex in the sea lamprey: comparative immunocytochemical study. J Comp Neurol 442:250-265.
33. 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.
34. Murakami Y, Ogasawara M, Sugahara F, Hirano S, Satoh N, Kuratani S. 2001. Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates. Development 128:3521-3531.
35. Nakajima Y, Humphreys T, Kaneko H, Tagawa K. 2004. Development and neural organization of the tornaria larva of the Hawaiian hemichordate, Ptychodera flava. Zool Sci 21:69-78.
36. Nielsen C, Hay-Schmidt A. 2007. Development of the Enteropneust Ptychodera flava: ciliary bands and nervous system. J Morphol 570:551-570.
37. Ogasawara M, Shigetani Y, Hirano S, Satoh N, Kuratani S. 2000. Pax1/Pax9-related genes in an agnathan vertebrate, Lampetra japonica: expression pattern of LjPax9 implies sequential evolutionary events toward the gnathostome body plan. Dev Biol 223:399-410.
38. Pani AM, Mullarkey EE, Aronowicz J, Assimacopoulos S, Grove EA, Lowe CJ. 2012. Ancient deuterostome origins of vertebrate brain signaling centres. Nature 483:289-294.
39. Potter IC, Welsch U. 1992. Arrangement, histochemistry and fine structure of the connective tissue architecture of lampreys. J Zool 225:1-30.
40. Richardson MK, Admiraal J, Wright GM. 2010. Developmental anatomy of lampreys. Biol Rev 85:1-33.
41. Tahara Y. 1988. Normal stages of development in the lamprey, Lampetra reissneri (Dybowski). Zool Sci 5:109-118.
42. Takahashi T, Holland PWH. 2004. Amphioxus and ascidian Dmbx homeobox genes give clues to the vertebrate origins of midbrain development. Development 131:3285-3294.
43. Trejo LJ, Cicerone CM. 1984. Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Res 300:49-62.
44. Ullén F, Orlovsky GN, Deliagina TG, Grillner S. 1993. Role of dermal photoreceptors and lateral eyes in initiation and orientation of locomotion in lamprey. Behav Brain Res 54:107-110.
45. Ullén F, Deliagina TG, Orlovsky GN, Grillner S. 1997. Visual pathways for postural control and negative phototaxis in lamprey. J Neurophysiol 78:960-976.
46. Villar-Cerviño V, Abalo XM, Villar-Cheda B, Meléndez-Ferro M, Pérez-Costas E, Holstein GR, Martinelli GP, Rodicio MC, Anadón R. 2006. Presence of glutamate, glycine, and γ-aminobutyric acid in the retina of the larval sea lamprey: comparative immunohistochemical study of classical neurotransmitters in larval and postmetamorphic retinas. J Comp Neurol 499:810-827.
47. Villar-Cheda B, Abalo XM, Villar-Cerviňo V, Barreiro-Iglesias A, Anadón R, Rodicio MC. 2008. Late proliferation and photoreceptor differentiation in the transforming lamprey retina. Brain Res 1201:60-67.
48. 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 U S A 109:15383-15388.
49. Voneida TJ, Sligar CM. 1976. A comparative neuroanatomic study of retinal projections in two fishes: Astyanax hubbsi (the blind cave fish), and Astyanax mexicanus. J Neurosci 165:89-105.
50. Wada H, Garcia-Fernàndez J, Holland PWH. 1999. Colinear and segmental expression of amphioxus Hox genes. Dev Biol 213:131-141.
51. Wicht H, Northcutt RG. 1990. Retinofugal and retinopetal projections in the Pacific hagfish, Eptatretus stouti (Myxinoidea). Brain Behav Evol 36:315-328.
52. Wright GM, Filisa MF, Youson JH. 1980. Immunocytochemical localization of thyroglobulin in the transforming endostyle of anadromous sea lampreys, Petromyzon marinus L., during metamorphosis. Gen Comp Endocr 42:187-194.
53. Yasui K, Tabata S, Ueki T, Uemura M, Zhang SC. 1998. Early development of the peripheral nervous system in a lancelet species. J Comp Neurol 393:415-425.
54. Yoda H, Hirose Y, Yasuoka A, Sasado T, Morinaga C, Deguchi T, Henrich T, Iwanami N, Watanabe T, Osakada M, Kunimatsu S, Wittbrodt J, Suwa H, Niwa K, Okamoto Y, Yamanaka T, Kondoh H, Furutani-Seiki M. 2004. Mutations affecting retinotectal axonal pathfinding in Medaka, Oryzias latipes. Mech Dev 121:725-728.
55. 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.