Advertisement

Brain Structure and Function

, Volume 221, Issue 3, pp 1691–1717 | Cite as

Morphogenesis of the cerebellum and cerebellum-related structures in the shark Scyliorhinus canicula: insights on the ground pattern of the cerebellar ontogeny

  • Sol Pose-Méndez
  • Eva Candal
  • Sylvie Mazan
  • Isabel Rodríguez-Moldes
Original Article

Abstract

Because the cerebellum emerged at the agnathan-gnathostome transition and cartilaginous fishes are at the base of the gnathostome lineage, this group is crucial to determine the basic developmental pattern of the cerebellum and to gain insights into its origin. We have systematically analyzed key events in the development of cerebellum and cerebellum-related structures of the shark Scyliorhinus canicula. Three developmental periods are distinguished based on anatomical observations combined with molecular analysis. We present neurochemical and genoarchitectonic evidence on the onset of cerebellar development, the rostral and caudal cerebellar boundaries, the compartmentalization of the cerebellum, and correspondence of cerebellar domains to rhombomeric segmentation of the rostral hindbrain. Our observations, mainly based on the expression pattern of ScHoxA2, support the origin of both the upper and lower auricular leaves from r1 and exclude any cerebellar origin from r2. Correlation between subrhombomeres r1a/r1b and cerebellar domains is proposed based on the ScEn2 expression. The ScEn2 and ScOtx2 expression patterns revealed an antero-posterior cerebellar compartmentalization similar to that of mammals, and supported certain fissures (commonly used to define cerebellar domains) as reliable anatomical landmarks. At difference from mammals, the expression of ScEn2 along the cerebellar median-lateral axis does not reveal a multiple-banded pattern. The present study provides an atlas of cerebellar development in one of the most basal extant gnathostome lineages and emphasizes the importance of combining classic descriptive with modern molecular studies to gain knowledge on the ancestral condition of cerebellar developmental processes and the origins and evolution of the cerebellum.

Keywords

Chondrichthyans Development Auricles Compartmentalization Rhombomeres Engrailed-2 HoxA2 

Abbreviations

AMV

Anterior medullary velum

Aur

Auricles

c

Sulcus c

Cb

Cerebellum

Cbcl

Caudal lobe of cerebellum

CbCr

Cerebellar crest

Cbdp

Dorsal part of the cerebellar body

Cbp

Cerebellar plate

Cbrl

Rostral lobe of cerebellum

Cbvp

Ventral part of the cerebellar body

ChP

Choroid plexus

CP

Cerebellar peduncle

CPp

Cerebellar peduncle primordium

Di

Diencephalon

DON

Dorsal octaval nucleus

e2

Sulcus e2

e2′

Subcerebellar sulcus e2′

FL

Fibrous layer

fmi

Inferior median fissure

GE

Granular eminence

GL

Cerebellar granular layer

IIIn

Oculomotor nerve

IS

Isthmus

Isfo

Isthmic fovea

IVv

Fourth ventricle

IVn

Trochlear nerve

IXn

Glossopharyngeal nerve

iz

Intermediate zone

LAL

Lower auricular leaf

Lf

Longitudinal fissure

LPost

Lobulus posticus

LR

Lateral recess

LRL

Lower rhombic lip

MedE

Median eminence

Mes

Mesencephalon

MHB

Midbrain-hindbrain boundary

MOL

Cerebellar molecular layer

MON

Medial octaval nucleus

Mrf

Meso-rhombencephalic fissure

Nlla

Anterior lateral line nerve

OLA

Octavolateral area

OT

Optic tectum

PL

Purkinje cell layer

plf

Posterolateral fissure

prf

Primary transverse fissure

Pros

Prosencephalon

r0-2

Rhombomeres 0–2

Ra

Raphe

Rh

Rombencephalon

sid

Intermediate dorsal sulcus

slH

His sulcus or sulcus limitans

sms

Median superior sulcus

UAL

Upper auricular leaf

UALp

Upper auricular leaf primordium

URL

Upper rhombic lip

vAP

Ventral area of the alar plate

VbCb

Vestibulocerebellum

VIIIm

Magnocellular octaval nucleus

VIIIn

Octaval nerve

VIIn

Facial nerve

Vn

Trigeminal nerve

Notes

Acknowledgments

We thank Prof. Dr. R. Anadón for the valuable comments made during the preparation of this paper and his critical reading of the manuscript. This work was supported by grants from the Spanish Dirección General de Investigación-FEDER (BFU2010- 15816), the Xunta de Galicia (10PXIB200051PR, CN 2012/237), and European Community-Research Infrastructure Action under the FP7 "Capacities" Specific Programme (ASSEMBLE 227799).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The manuscript does not contain clinical studies or patient data.

Supplementary material

429_2015_998_MOESM1_ESM.tif (2.6 mb)
Supplementary material 1 Transverse sections of the caudal hindbrain in Scyliorhinus canicula at late embryonic and juvenile stages, showing specific neurochemical features of the intermediate zone (indicated with the red dotted line) in between the lower auricular leaf and dorsal octaval nucleus. In this area, it was observed: granule cells with the hematoxylin–eosin staining (a), expression of ScHoxA2 (b), low density of 5-HT-ir fibers (c), and high density of CR-ir fibers (d). Scale bars 200 µm (c, d); 500 µm (a, b) (TIFF 2620 kb)
429_2015_998_MOESM2_ESM.tif (366 kb)
Supplementary material 2 Transverse section of the caudal hindbrain in Scyliorhinus canicula at stage 29, showing a reduction in the expression of proliferating cell nuclear marker (PCNA) in the zones where grooves are forming (indicated with arrowheads). Scale bar 300 µm (TIFF 366 kb)

References

  1. Alexander T, Nolte C, Krumlauf R (2009) Hox genes and segmentation of the hindbrain and axial skeleton. Annu Rev Cell Dev Biol 25:431–456PubMedCrossRefGoogle Scholar
  2. Altman J, Bayer SA (1985) Embryonic development of the rat cerebellum. I. Delineation of the cerebellar primordium and early cell movements. J Comp Neurol 231:1–26PubMedCrossRefGoogle Scholar
  3. Álvarez R, Anadón R (1987) The cerebellum of the dogfish, Scyliorhinus canicula: a quantitative study. J Hirnforsch 28:133–137PubMedGoogle Scholar
  4. Álvarez-Otero R, Anadón R (1992) GOLGI cells of the cerebellum of the dogfish, Scyliorhinus canicula (elasmobranchs): a GOLGI and ultrastructural study. J Hirnforsch 33:321–327PubMedGoogle Scholar
  5. Álvarez-Otero R, Regueira SD, Anadón R (1993) New structural aspects of the synaptic contacts on Purkinje cells in an elasmobranch cerebellum. J Anat 182:13–21PubMedPubMedCentralGoogle Scholar
  6. Álvarez-Otero R, Pérez SE, Rodríguez MA, Adrio F, Anadón R (1995) GABAergic neuronal circuits in the cerebellum of the dogfish Scyliorhinus canicula (Elasmobranchs): an immunocytochemical study. Neurosci Lett 187:87–90PubMedCrossRefGoogle Scholar
  7. Anadón R, Molist P, Rodríguez-Moldes I, López JM, Quintela I, Cerviño MC, Barja P, González A (2000) Distribution of choline acetyltransferase immunoreactivity in the brain of an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula). J Comp Neurol 420:139–170PubMedCrossRefGoogle Scholar
  8. Anadón R, Ferreiro-Galve S, Sueiro C, Graña P, Carrera I, Yáñez J, Rodríguez-Moldes I (2009) Calretinin-immunoreactive systems in the cerebellum and cerebellum-related lateral-line medullary nuclei of an elasmobranch, Scyliorhinus canicula. J Chem Neuroanat 37:46–54PubMedCrossRefGoogle Scholar
  9. Aroca P, Puelles L (2005) Postulated boundaries and differential fate in the developing rostral hindbrain. Brain Res Rev 49:179–190PubMedCrossRefGoogle Scholar
  10. Aruga J, Inoue T, Hoshino J, Mikoshiba K (2002) Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22:218–225PubMedGoogle Scholar
  11. Ashwell KW (2012) Development of the cerebellum in the platypus (Ornithorhynchus anatinus) and short-beaked echidna (Tachyglossus aculeatus). Brain Behav Evol 79:237–251PubMedCrossRefGoogle Scholar
  12. Ballard WW, Mellinger J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336CrossRefGoogle Scholar
  13. Bell CC (2002) Evolution of cerebellum-like structures. Brain Behav Evol 59:312–326PubMedCrossRefGoogle Scholar
  14. Bell CC, Han V, Sawtell NB (2008) Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci 31:1–24PubMedCrossRefGoogle Scholar
  15. Berry M, Ibrahim M, Carlile J, Ruge F, Duncan A, Butt AM (1995) Axon-glial relationships in the anterior medullary velum of the adult rat. J Neurocytol 24:965–983PubMedCrossRefGoogle Scholar
  16. Bovolenta P (2005) Morphogen signaling at the vertebrate growth cone: a few cases or a general strategy? J Neurobiol 64:405–416PubMedCrossRefGoogle Scholar
  17. Buffo A, Rossi F (2013) Origin, lineage and function of cerebellar glia. Prog Neurobiol 109:42–63PubMedCrossRefGoogle Scholar
  18. Butler A, Hodos W (2005) Comparative vertebrate neuroanatomy. Evolution and adaption, 2nd edn. Wiley-Liss, Hoboken, NJ, pp 180–197Google Scholar
  19. Cambronero F, Puelles L (2000) Rostrocaudal nuclear relationships in the avian medula oblongata: a fate map with quail chick chimeras. J Comp Neurol 427:522–545PubMedCrossRefGoogle Scholar
  20. Candal E, Anadón R, Bourrat F, Rodríguez-Moldes I (2005) Cell proliferation in the developing and adult hindbrain and midbrain of trout and medaka (teleosts): a segmental approach. Brain Res 160:157–175CrossRefGoogle Scholar
  21. Carrera (2008) Desarrollo de los sistemas gabaérgico y aminérgicos en el sistema nervioso central de peces cartilaginosos. Dissertation, University of Santiago de CompostelaGoogle Scholar
  22. Carrera I, Anadón R, Rodríguez-Moldes I (2012) Development of tyrosine hydroxylase-immunoreactive cell populations and fiber pathways in the brain of the dogfish Scyliorhinus canicula: New perspectives on the evolution of the vertebrate catecholaminergic system. J Comp Neurol 520:3574–3603PubMedCrossRefGoogle Scholar
  23. Cerri S, Piccolini VM, Bernocchi G (2010) Postnatal development of the central nervous system: anomalies in the formation of cerebellum fissures. Anat Rec (Hoboken) 293:492–501CrossRefGoogle Scholar
  24. Chaplin N, Tendeng C, Wingate RJ (2010) Absence of an external germinal layer in zebrafish and shark reveals a distinct, anamniote ground plan of cerebellum development. J Neurosci 30:3048–3057PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cheng Y, Sudarov A, Szulc KU, Sgaier SK, Stephen D, Turnbull DH, Joyner AL (2010) The Engrailed homeobox genes determine the different foliation patterns in the vermis and hemispheres of the mammalian cerebellum. Development 137:519–529PubMedPubMedCentralCrossRefGoogle Scholar
  26. Compagnucci C, Debiais-Thibaud M, Coolen M, Fish J, Griffin JN, Bertocchini F, Minoux M, Rijli FM, Borday-Birraux V, Casane D, Mazan S, Depew MJ (2013) Pattern and polarity in the development and evolution of the gnathostome jaw: both conservation and heterotopy in the branchial arches of the shark, Scyliorhinus canicula. Dev Biol 377:428–448PubMedCrossRefGoogle Scholar
  27. Conley RA, Bodznick D (1994) The cerebellar dorsal granular ridge in an elasmobranch has proprioceptive and electroreceptive representations and projects homotopically to the medullary electrosensory nucleus. J Comp Physiol A 174:707–721PubMedCrossRefGoogle Scholar
  28. Coolen M, Sauka-Spengler T, Nicolle D, Le-Mentec C, Lallemand Y, Da Silva C, Plouhinec J-L, Robert B, Wincker P, Shi D-L, Mazan S (2007) Evolution of axis specification mechanisms in jawed vertebrates: insights from a chondrichthyan. PLoS One 2(4):e374. doi: 10.1371/journal.pone.0000374 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Coolen M, Menuet A, Chassoux D, Compagnucci C, Henry S, Lévèque L, Da Silva C, Gavory F, Samain S, Wincker P, Thermes C, D’Aubenton-Carafa Y, Rodriguez-Moldes I, Naylor G, Depew M, Sourdaine P, Mazan S (2009) The dogfish Scyliorhinus canicula, a reference in jawed vertebrates. In: Behringer RR, Johnson AD, Krumlauf RE (eds) Emerging model organisms. A laboratory manual, vol 1. Cold Spring Harbor, CSHL Press, NY, pp 431–446Google Scholar
  30. Davis CA, Joyner A (1988) Expression patterns of the homeo box-containing genes En-1 and En-2 and the proto-oncogene int-1 diverge during mouse development. Genes Dev 2:1736–1744PubMedCrossRefGoogle Scholar
  31. Davis CA, Noble-Topham SE, Rossant J, Joyner AL (1988) Expression of the homeo box-containing gene En-2 delineates a specific region of the developing mouse brain. Genes Dev 2:361–371PubMedCrossRefGoogle Scholar
  32. Devor A (2000) Is the cerebellum like cerebellar-like structures? Brain Res Rev 34:149–156PubMedCrossRefGoogle Scholar
  33. Dun XP (2012) Origin of climbing fiber neurons and the definition of rhombic lip. Int J Dev Neurosci 30:391–395PubMedCrossRefGoogle Scholar
  34. Ferreiro-Galve S (2010) Brain and retina regionalization in sharks: study based on the spatiotemporal expression pattern of Pax6 and other neurochemical markers. Dissertation, University of Santiago de CompostelaGoogle Scholar
  35. Ferreiro-Galve S, Candal E, Rodríguez-Moldes I (2012) Dynamic expression of Pax6 in the shark olfactory system: evidence for the presence of Pax6 cells along the olfactory nerve pathway. J Exp Zool B Mol Dev Evol 318:79–90PubMedCrossRefGoogle Scholar
  36. Fiebig E (1988) Connections of the corpus cerebelli in the Thornback guitarfish, Platyrhinoidis triseriata (Elasmobranchii): a study with WGA-HRP and extracellular granule cell recording. J Comp Neurol 268:567–583PubMedCrossRefGoogle Scholar
  37. Frantz GD, Weimann JM, Levin ME, McConnell SK (1994) Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J Neurosci 14:5725–5740PubMedGoogle Scholar
  38. Fritzsch B, Sonntag R (1987) The trochlear nerve of amphibians and its relation to proprioceptive fibers: a qualitative and quantitative HRP study. Anat Embryol (Berl) 177:105–114CrossRefGoogle Scholar
  39. Fujita H, Sugihara I (2013) Branching patterns of olivocerebellar axons in relation to the compartmental organization of the cerebellum. Front Neural Circuits 7:3PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gardner CA, Barald KF (1992) Expression patterns of engrailed-like proteins in the chick embryo. Dev Dyn 193:370–388PubMedCrossRefGoogle Scholar
  41. Germot A, Lecointre G, Plouhinec JL, Le Mentec C, Girardot F, Mazan S (2001) Structural evolution of Otx genes in craniates. Mol Biol Evol 18:1668–1678PubMedCrossRefGoogle Scholar
  42. Gómez A, Durán E, Ocaña FM, Jiménez-Moya F, Broglio C, Domezain A, Salas C, Rodríguez F (2004) Observation on the brain development of the sturgeon Acipenser naccarii. In: Carmona R, Domezain A, García-Gallego M, Hernando JA, Rodríguez F, Ruiz-Rejón M (eds) Biology, conservation and sustainable development of sturgeons. Springer, Berlin, pp 155–174Google Scholar
  43. Herrup K, Kuemerle B (1997) The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61–90PubMedCrossRefGoogle Scholar
  44. Hidalgo-Sánchez M, Backer S, Puelles L, Bloch-Gallego E (2012) Origin and plasticity of the inferior olivary complex. Dev Biol 371:215–226PubMedCrossRefGoogle Scholar
  45. Ibrahim M, Menoud PA, Celio MR (2000) Neurones in the adult rat anterior medullary velum. J Comp Neurol 419:122–134PubMedCrossRefGoogle Scholar
  46. Irving C, Malhas A, Guthrie S, Mason I (2002) Establishing the trochlear motor axon trajectory: role of the isthmic organizer and Fgf8. Development 129:5389–5398PubMedCrossRefGoogle Scholar
  47. Joven A, Morona R, González A, Moreno N (2013) Spatiotemporal patterns of Pax3, Pax6 and Pax7 expression in the developing brain of a urodele amphibian, Pleurodeles waltl. J Comp Neurol 521:3913–3953PubMedGoogle Scholar
  48. Kaslin J, Ganz J, Geffarth M, Grandel H, Hans S, Brand M (2009) Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 29:6142–6153PubMedCrossRefGoogle Scholar
  49. Landsberg RL, Awatramani RB, Hunter NL, Farago AF, DiPietrantonio HJ, Rodríguez CI, Dymecki SM (2005) Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48:933–947PubMedCrossRefGoogle Scholar
  50. Larsell O (1925) The development of the cerebellum in the frog (Hyla regilla) in relation to the vestibular and lateral-line systems. J Comp Neurol 39:249–289CrossRefGoogle Scholar
  51. Larsell O (1934) Morphogenesis and evolution of the cerebellum. Arch Neurol 31:373–395CrossRefGoogle Scholar
  52. Larsell O (1967) The comparative anatomy and histology of the cerebellum from myxinoids through birds. University of Minnesota Press, MinneapolisGoogle Scholar
  53. Leclerc N, Doré L, Parent A, Hawkes R (1990) The compartmentalization of the monkey and rat cerebellar cortex: zebrin I and cytochrome oxidase. Brain Res 506:70–78PubMedCrossRefGoogle Scholar
  54. Ma S, Kwon HJ, Huang Z (2012) Ric-8a, a guanine nucleotide exchange factor for heterotrimeric G proteins, regulates Bergmann glia-basement membrane adhesion during cerebellar foliation. J Neurosci 32:14979–14993PubMedCrossRefGoogle Scholar
  55. Margotta V (2007) PCNA immunoreactivity revealing normal proliferative activity in the brain of an adult Elasmobranch, Torpedo marmorata. Ital J Anat Embryol 112:145–155PubMedGoogle Scholar
  56. Marín F, Puelles L (1995) Morphological fate of rhombomeres in quail/chick chimeras: a segmental analysis of hindbrain nuclei. Eur J Neurosci 7:1714–1738PubMedCrossRefGoogle Scholar
  57. Martínez S, Andreu A, Mecklenburg N, Echevarría D (2013) Cellular and molecular basis of cerebellar development. Front Neuroanat 7:18PubMedPubMedCentralCrossRefGoogle Scholar
  58. Marzban H, Chung SH, Pezhouh MK, Feirabend H, Watanabe M, Voogd J, Hawkes R (2010) Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticus). J Comp Neurol 518:2221–2239PubMedCrossRefGoogle Scholar
  59. Mazan S, Jaillard D, Baratte B, Janvier P (2000) Otx1 gene-controlled morphogenesis of the horizontal semicircular canal and the origin of the gnathostome characteristics. Evol Dev 2:186–193PubMedCrossRefGoogle Scholar
  60. Meek J, Hafmans TG, Maler L, Hawkes R (1992) Distribution of zebrin II in the gigantocerebellum of the mormyrid fish Gnathonemus petersii compared with other teleosts. J Comp Neurol 316:17–31PubMedCrossRefGoogle Scholar
  61. Millen KJ, Wurst W, Herrup K, Joyner A (1994) Abnormal embryonic cerebellar development and patterning of postnatal foliation in two mouse Engrailed-2 mutants. Development 120:695–706PubMedGoogle Scholar
  62. Millet S, Alvarado-Mallart RM (1995) Expression of the homeobox-containing gene En-2 during development of the chick central nervous system. Eur J Neurosci 7:777–791PubMedCrossRefGoogle Scholar
  63. Montgomery JC (1981) Origin of the Parallel fibers in the cerebellar crest overlying the intermediate nucleus of the elasmobranch hindbrain. J Comp Neurol 202:185–191PubMedCrossRefGoogle Scholar
  64. Montgomery JC, Bodznick D, Yopak KE (2012) The cerebellum and cerebellum-like structures of cartilaginous fishes. Brain Behav Evol 80:152–165PubMedCrossRefGoogle Scholar
  65. Moreno-Bravo JA, Perez-Balaguer A, Martinez-Lopez JE, Aroca P, Puelles L, Martinez S, Puelles E (2014) Role of Shh in the development of molecularly characterized tegmental nuclei in mouse rhombomere 1. Brain Struct Funct 219:777–792PubMedCrossRefGoogle Scholar
  66. Namba K, Sugihara I, Hashimoto M (2011) Close correlation between the birth date of Purkinje cells and the longitudinal compartmentalization of the mouse adult cerebellum. J Comp Neurol 519:2594–2614PubMedCrossRefGoogle Scholar
  67. New JG (2001) Comparative neurobiology of the elasmobranch cerebellum: theme and variations on a sensorimotor interface. Environ Biol Fish 60:93–108CrossRefGoogle Scholar
  68. Nieuwenhuys R (1967) Comparative anatomy of the cerebellum. Prog Brain Res 25:1–93PubMedCrossRefGoogle Scholar
  69. Northcutt RG (2002) Understanding vertebrate brain evolution. Integ Comp Biol 42:743–756CrossRefGoogle Scholar
  70. Orvis GD, Barraza LH, Wilson SL, Szulc KU, Turnbull DH, Joyner AL (2012) The engrailed homeobox genes are required in multiple cell lineages to coordinate sequential formation of fissures and growth of the cerebellum. Dev Biol 367:25–39PubMedPubMedCentralCrossRefGoogle Scholar
  71. Oulion S, Debiais-Thibaud M, d’Aubenton-Carafa Y, Thermes C, Da Silva C, Bernard-Samain S, Gavory F, Wincker P, Mazan S, Casane D (2010) Evolution of Hox gene clusters in gnathostomes: insights from a survey of a shark (Scyliorhinus canicula) transcriptome. Mol Biol Evol 27:2829–2838PubMedCrossRefGoogle Scholar
  72. Pakan JMP, Iwaniuk AN, Wylie DRW, Hawkes R, Marzban H (2007) Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia). J Comp Neurol 501:619–630PubMedCrossRefGoogle Scholar
  73. Palgrem A (1921) Embryological and morphological studies on the midbrain and cerebellum of vertebrates. Acta Zool 2:1–94CrossRefGoogle Scholar
  74. Paul DH, Roberts BL (1975) Responses of neurones in the cerebellar corpus of the dogfish (Scyliorhinus canicula). J Physiol 244:47P–49PPubMedGoogle Scholar
  75. Peña-Melián A, Puerta Fonolla J, Gil Loyzaga P (1986) The ontogeny of the cerebellar fissures in the chick embryo. Anat Embryol (Berl) 175:119–128CrossRefGoogle Scholar
  76. Plouhinec JL, Leconte L, Sauka-Spengler TS, Bovolenta P, Mazan S, Saule S (2005) Comparative analysis of gnathostome Otx gene expression patterns in the developing eye: implications for the functional evolution of the multigene family. Dev Biol 278:560–575PubMedCrossRefGoogle Scholar
  77. Pose-Méndez S (2013) Developmental study of the cerebellum in cartilaginous fishes: Towards the identification of primitive features of the cerebellar formation in gnathostomes. Dissertation, University of Santiago de CompostelaGoogle Scholar
  78. Pose-Méndez S, Candal E, Adrio F, Rodríguez-Moldes I (2014) Development of the cerebellar afferent system in the shark Scyliorhinus canicula: insights into the basal organization of precerebellar nuclei in gnathostomes. J Comp Neurol 522:131–168PubMedCrossRefGoogle Scholar
  79. Pose-Méndez S, Candal E, Mazan S, Rodríguez-Moldes I (2015) Genoarchitecture of the rostral hindbrain of a shark: basis for understanding the emergence of the cerebellum at the agnathan-gnathostome transition. Brain Struct Funct. doi: 10.1007/s00429-014-0973-8 Google Scholar
  80. Pouwels E (1978) On the development of the cerebellum of the trout, Salmo gairdneri. I. Patterns of cell migration. Anat Embryol (Berl) 152:291–308CrossRefGoogle Scholar
  81. Prayer D, Kasprian G, Krampl E, Ulm B, Witzani L, Prayer L, Brugger PC (2006) MRI of normal fetal brain development. Eur J Radiol 57:199–216PubMedCrossRefGoogle Scholar
  82. Puelles L, Ferrán JL (2012) Concept of neural genoarchitecture and its genomic fundament. Front Neuroanat 6:47PubMedPubMedCentralCrossRefGoogle Scholar
  83. Puelles L, Harrison M, Paxinos G, Watson C (2013) A developmental ontology for the mammalian brain based on the prosomeric model. Trends Neurosci 36:570–578PubMedCrossRefGoogle Scholar
  84. Puzdrowski RL (1997) Anti-Zebrin II immunopositivity in the cerebellum and octavolateral nuclei in two species of stingrays. Brain Behav Evol 50:358–368PubMedCrossRefGoogle Scholar
  85. Quintana-Urzainqui I, Rodríguez-Moldes I, Candal E (2014) Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve. Brain Struct Funct 219:85–104PubMedPubMedCentralCrossRefGoogle Scholar
  86. Rodríguez-Moldes I, Manso MJ, Becerra M, Molist P, Anadón R (1993) Distribution of substance P-like immunoreactivity in the brain of the elasmobranch Scyliorhinus canicula. J Comp Neurol 335:228–244PubMedCrossRefGoogle Scholar
  87. Rodríguez-Moldes I, Ferreiro-Galve S, Carrera I, Sueiro C, Candal E, Manzan S, Anadón R (2008) Development of the cerebellar body in sharks: spatiotemporal relations of Pax6-expression, cell proliferation and differentiation. Neurosci Lett 432:105–110PubMedCrossRefGoogle Scholar
  88. Rodríguez-Moldes I, Carrera I, Pose-Méndez S, Quintana-Urzainqui I, Candal E, Anadón R, Mazan S, Ferreiro-Galve S (2011) Regionalization of the shark hindbrain: a survey of an ancestral organization. Front Neuroanat 5:16PubMedPubMedCentralCrossRefGoogle Scholar
  89. Rüdeberg S (1961) Morphogenetic studies on the cerebellar nuclei and their homologization in different vertebrates including man. Dissertation, Univ of LundGoogle Scholar
  90. Sgaier SK, Millet S, Villanueva MP, Berenshteyn F, Song C, Joyner AL (2005) Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45:27–40PubMedGoogle Scholar
  91. Sgaier SK, Lao Z, Villanueva MP, Berenshteyn F, Stephen D, Turnbull RK, Joyner AL (2007) Genetic subdivision of the tectum and cerebellum into functionally related regions based on differential sensitivity to engrailed proteins. Development 134:2325–2335PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sillitoe RV, Stephen D, Lao Z, Joyner A (2008) Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. J Neurosci 28:12150–12162PubMedPubMedCentralCrossRefGoogle Scholar
  93. Sillitoe RV, Vogel MW, Joyner AL (2010) Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J Neurosci 30:10015–10024PubMedPubMedCentralCrossRefGoogle Scholar
  94. Smeets WJAJ (1998) Cartilaginous fish. In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C (eds) The central nervous system of vertebrates, vol 1. Springer, Berlin, pp 551–654CrossRefGoogle Scholar
  95. Smeets WJ, Nieuwenhuys R (1976) Topological analysis of the brain stem of the sharks Squalus acanthias and Scyliorhinus canicula. J Comp Neurol 165:333–368PubMedCrossRefGoogle Scholar
  96. Smeets WJAJ, Nieuwenhuys R, Roberts BL (1983) The central nervous system of cartilaginous fishes. Structure and functional correlations. Springer, BerlinCrossRefGoogle Scholar
  97. Sterzi G (1912) Il sistema nervoso centrale dei vertebrate Pesci, vol II. Draghi, PadovaGoogle Scholar
  98. Sudarov A, Joyner AL (2007) Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev 2:26PubMedPubMedCentralCrossRefGoogle Scholar
  99. ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen HO, Renier WO (2003) Development and developmental disorders of the human cerebellum. J Neurol 250:1025–1036PubMedCrossRefGoogle Scholar
  100. Triulzi F, Parazzini C, Righini A (2005) MRI of fetal and neonatal cerebellar development. Semin Fetal Neonatal Med 10:411–420PubMedCrossRefGoogle Scholar
  101. Tubbs RS, Wellons JC 3rd, Salter G, Oakes WJ (2004) Fenestration of the superior medullary velum as treatment for a trapped fourth ventricle: a feasibility study. Clin Anat 17:82–87PubMedCrossRefGoogle Scholar
  102. Tümpel S, Cambronero F, Sims C, Krumlauf R, Wiedemann LM (2008) A regulatory module embedded in the coding region of Hoxa2 controls expression in rhombomere 2. Proc Natl Acad Sci USA 105:20077–20082PubMedPubMedCentralCrossRefGoogle Scholar
  103. Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313–318PubMedCrossRefGoogle Scholar
  104. Vecino E, Ekström P (1991) Expression of the homeobox engrailed gene during the embryonic development of the nervous system of the trout (Salmo fario L.). Neurosci Lett 129:311–314PubMedCrossRefGoogle Scholar
  105. Vogel-Höpker A, Rohrer H (2002) The specification of noradrenergic locus coeruleus (LC) neurones depends on bone morphogenetic proteins (BMPs). Development 129:983–991PubMedGoogle Scholar
  106. von Kupffer C (1906) “Die Morphogenie des Zentral nerven systems”. In: O. Hertwig (Jena: Fischer) (ed) Handbuch der vergleichenden und experimentellen Entwicklungslehre der Wirbeltiere. Vol. 2, Part 3 pp 1–272Google Scholar
  107. Watanabe Y, Toyoda R, Nakamura H (2004) Navigation of trochlear motor axons along the midbrain-hindbrain boundary by neuropilin 2. Development 131:681–692PubMedCrossRefGoogle Scholar
  108. White JJ, Reeber SL, Hawkes R, Sillitoe RV (2012) Wholemount immunohistochemistry for revealing complex brain topography. J Vis Exp 62:e4042PubMedGoogle Scholar
  109. Wilson SL, Kalinovsky A, Orvis GD, Joyner A (2011) Spatially restricted and developmentally dynamic expression of engrailed genes in multiple cerebellar cell types. Cerebellum 10:356–372PubMedPubMedCentralCrossRefGoogle Scholar
  110. Wingate RJ, Hatten ME (1999) The role of the rhombic lip in avian cerebellum development. Development 126:4395–4404PubMedGoogle Scholar
  111. Zupanc GK, Hinsch K, Gage FH (2005) Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol 488:290–319PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sol Pose-Méndez
    • 1
  • Eva Candal
    • 1
  • Sylvie Mazan
    • 2
  • Isabel Rodríguez-Moldes
    • 1
  1. 1.Department of Cell Biology and Ecology, CIBUS Bldg, Avda. Lope Gómez de MarzoaUniversity of Santiago de CompostelaSantiago de CompostelaSpain
  2. 2.UPMC Université Paris 6, CNRS, Université Européenne de Bretagne, UMR 7150, SBRRoscoffFrance

Personalised recommendations