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

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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.

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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

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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).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Cell Biology and Ecology, CIBUS Bldg, Avda. Lope Gómez de Marzoa, University of Santiago de Compostela, 15782, Santiago de Compostela, Spain

    Sol Pose-Méndez, Eva Candal & Isabel Rodríguez-Moldes

  2. UPMC Université Paris 6, CNRS, Université Européenne de Bretagne, UMR 7150, SBR, Roscoff, France

    Sylvie Mazan

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  1. Sol Pose-Méndez
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  2. Eva Candal
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  3. Sylvie Mazan
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  4. Isabel Rodríguez-Moldes
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Correspondence to Isabel Rodríguez-Moldes.

Electronic supplementary material

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429_2015_998_MOESM1_ESM.tif

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

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)

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Pose-Méndez, S., Candal, E., Mazan, S. et al. Morphogenesis of the cerebellum and cerebellum-related structures in the shark Scyliorhinus canicula: insights on the ground pattern of the cerebellar ontogeny. Brain Struct Funct 221, 1691–1717 (2016). https://doi.org/10.1007/s00429-015-0998-7

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  • DOI: https://doi.org/10.1007/s00429-015-0998-7

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