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Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications

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Abstract

Tangential neuronal migration occurs along different axes from the axis demarcated by radial glia and it is thought to have evolved as a mechanism to increase the diversity of cell types in brain areas, which in turn resulted in increased complexity of functional networks. In the telencephalon of amniotes, different embryonic tangential pathways have been characterized. However, little is known about the exact routes of migrations in basal vertebrates. Cartilaginous fishes occupy a key phylogenetic position to assess the ancestral condition of vertebrate brain organization. In order to identify putative subpallial-derived tangential migratory pathways in the telencephalon of sharks, we performed a detailed analysis of the distribution pattern of GAD and Dlx2, two reliable markers of tangentially migrating interneurons of subpallial origin in the developing forebrain. We propose the existence of five tangential routes directed toward different telencephalic regions. We conclude that four of the five routes might have emerged in the common ancestor of jawed vertebrates. We have paid special attention to the characterization of the proposed migratory pathway directed towards the olfactory bulbs. Our results suggest that it may be equivalent to the “rostral migratory stream” of mammals and led us to propose a hypothesis about its evolution. The analysis of the final destinations of two other streams allowed us to identify the putative dorsal and medial pallium of sharks, the regions from which the neocortex and hippocampus might have, respectively, evolved. Derived features were also reported and served to explain some distinctive traits in the morphology of the telencephalon of cartilaginous fishes.

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Abbreviations

Cb:

Cerebellum

Di:

Diencephalon

Glom:

Glomerulus

LGE-h:

Lateral ganglionic eminence homolog

LS:

Lateral stream

Mes:

Mesencephalon

MGE-h:

Medial ganglionic eminence homolog

MS:

Medial stream

MP:

Medial pallium

OB:

Olfactory bulb

OT:

Optic tectum

P:

Pallium

Rh:

Rhombencephalon

RS:

Rostral stream

Sp:

Subpallium

Tel:

Telencephalon

V:

Ventricle

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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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Authors and Affiliations

  1. Departamento de Biología Celular y Ecología, Edificio CIBUS, Campus Vida, University of Santiago de Compostela, 15782, Santiago de Compostela, Spain

    Idoia Quintana-Urzainqui, Isabel Rodríguez-Moldes & Eva Candal

  2. UMR7150, UPMC Université Paris 6, CNRS, Université Européenne de Bretagne, UMR 7150, SBR, Roscoff, France

    Sylvie Mazan

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  1. Idoia Quintana-Urzainqui
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  2. Isabel Rodríguez-Moldes
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  3. Sylvie Mazan
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  4. Eva Candal
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Corresponding author

Correspondence to Eva Candal.

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Online Resource 1 Video showing a three-dimensional reconstruction of the telencephalon and the distribution of the different streams at stage 31 of development. The rostral-most sections were not included in the reconstruction process and, as a result, the rostral-end of the lateral ventricles appears opened in the final reconstruction.

Online Resource 2 Video showing a three-dimensional reconstruction of the telencephalon and the distribution of the different streams at stage 32 of development.

Supplementary material 1 (MP4 3308 kb)

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Quintana-Urzainqui, I., Rodríguez-Moldes, I., Mazan, S. et al. Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications. Brain Struct Funct 220, 2905–2926 (2015). https://doi.org/10.1007/s00429-014-0834-5

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  • DOI: https://doi.org/10.1007/s00429-014-0834-5

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