Isabel Rodríguez‐Moldes

Universidade de Santiago de Compostela

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Ramón Anadón

Universidade de Santiago de Compostela

Eva Candal

Universidade de Santiago de Compostela

Susana Ferreiro‐Galve

Universidade de Santiago de Compostela

Sylvie Mazan

Centre National de la Recherche Scientifique

Iván Carrera

EuroEspes Biomedical Research Center

Fátima Adrio

Universidade de Santiago de Compostela

Pilar Molíst

Universidade de Vigo

Catalina Sueiro

Universidade de Santiago de Compostela

Idoia Quintana‐Urzainqui

University of Edinburgh

Sol Pose‐Méndez

Technische Universität Braunschweig

Cooperative Institutions

Universidade de Santiago de Compostela

Centre National de la Recherche Scientifique

Sorbonne Université

University of California, San Diego

Université Paris Cité

Universidade da Coruña

Station Biologique de Roscoff

Inserm

Scripps Institution of Oceanography

Université Paris-Saclay

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Prosomeric organization of the hypothalamus in an elasmobranch, the catshark Scyliorhinus canicula

Frontiers in Neuroanatomy (2015)

Gabriel N. Santos-Durán Arnaud Menuet Ronan Lagadec Hélène Mayeur Susana Ferreiro‐Galve

The hypothalamus has been a central topic in neuroanatomy because of its important physiological functions, but its mature organization remains elusive. Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain. Here we studied the molecular organization of the hypothalamus and neighboring telencephalic domains in a cartilaginous fish, the catshark, Scyliorhinus canicula, focusing on ScFoxg1a, ScShh, ScNkx2.1, ScDlx2/5, ScOtp, and ScTbr1 expression profiles and on the identification α-acetylated-tubulin-immunoreactive (ir), TH-ir, 5-HT-ir, and GFAP-ir structures by means of immunohistochemistry. Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates. These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

Scyliorhinus canicula

Forebrain

Medial forebrain bundle

Hagfish

Neuroanatomy

10.3389/fnana.2015.00037

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Citations (22)

Ontogeny of somatostatin-immunoreactive systems in the brain of the brown trout (Teleostei)

Anatomy and Embryology (1995)

Manuela Becerra M. Jesús Manso Isabel Rodríguez‐Moldes Ram�n Anad�n

Diencephalon

Pretectal area

Interpeduncular nucleus

10.1007/bf00186784

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Citations (25)

Temporal and spatial organization of tyrosine hydroxylase-immunoreactive cell groups in the embryonic brain of an elasmobranch, the lesser-spotted dogfish Scyliorhinus canicula

Brain Research Bulletin (2005)

Iván Carrera Catalina Sueiro Pilar Molíst Susana Ferreiro Fátima Adrio

Scyliorhinus canicula

Tegmentum

Pretectal area

Pars compacta

10.1016/j.brainresbull.2005.02.010

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Citations (19)

Subject Index, Vol. 137, 1990

Cells Tissues Organs (1990)

Isabel Rodríguez‐Moldes Jean‐Pierre Timmermans Dirk Adriaensen M.H.A. de Groodt-Lasseel D.W. Scheuermann

gene-related peptide 278 Casting 109

10.1159/000146913

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Citations (0)

A Developmental Approach to Forebrain Organization in Elasmobranchs: New Perspectives on the Regionalization of the Telencephalon

Brain Behavior and Evolution (2009)

Isabel Rodríguez‐Moldes

It is essential to consider chondrichthyans (cartilaginous fishes) in analyzing ancestral brain organization because this radiation represents the out-group to all other living gnathostomes (jawed vertebrates). It is particularly crucial to understand the evolution of the telencephalon in chondrichthyans, as this structure develops by evagination (as in most other vertebrates), whereas in most osteichthyans (bony fishes), it develops by eversion, a markedly different process. Among chondrichthyans, the Lesser Spotted Dogfish Scyliorhinus canicula (Elasmobranchii) appears to offer the most potential as a model species for study. Developmental studies of Scyliorhinus have revealed a segmentary pattern in the developing forebrain, similar to that described in other vertebrates, as well as the occurrence of tangential cell migration within the telencephalon, especially in relation to the pallial-subpallial boundary. These observations indicate that major morphogenetic processes thought to be a hallmark of mammalian brains actually existed much earlier in vertebrate phylogeny. In addition, analysis of telencephalic development in Scyliorhinus indicates the existence of telencephalic structures that are probably related to the ganglionic eminences of mammals.

Scyliorhinus canicula

Forebrain

Elasmobranchii

Skate

10.1159/000229010

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Citations (38)

The segmental organization of the developing shark brain based on neurochemical markers, with special attention to the prosencephalon

Brain Research Bulletin (2007)

Susana Ferreiro‐Galve Iván Carrera Eva Candal Begoña Villar‐Cheda Ramón Anadón

Calretinin

Neurochemical

10.1016/j.brainresbull.2007.10.048

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Citations (37)

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 Structure and Function (2012)

Idoia Quintana‐Urzainqui Isabel Rodríguez‐Moldes Eva Candal

The olfactory system represents an excellent model for studying different aspects of the development of the nervous system ranging from neurogenesis to mechanisms of axon growth and guidance. Important findings in this field come from comparative studies. We have analyzed key events in the development of the olfactory system of the shark Scyliorhinus canicula by combining immunohistochemical and tract-tracing methods. We describe for the first time in a cartilaginous fish an early population of pioneer HuC/D-immunoreactive (ir) neurons that seemed to delaminate from the olfactory pit epithelium and migrate toward the telencephalon before the olfactory nerve was identifiable. A distinct, transient cell population, namely the migratory mass, courses later on in apposition to the developing olfactory nerve. It contains olfactory ensheathing glial (GFAP-ir) cells and HuC/D-ir neurons, some of which course toward an extrabulbar region. We also demonstrate that Pax6-ir cells coursing along the developing olfactory pathways in S. canicula are young migrating (HuC/D and DCX-ir) neurons of the migratory mass that do not form part of the terminal nerve pathway. Evidences that these Pax6 neurons originate in the olfactory epithelium are also reported. As Pax6 neurons in the olfactory epithelium show characteristics of olfactory receptor neurons, and migrating Pax6-ir neurons formed transient corridors along the course of olfactory axons at the entrance of the olfactory bulb, we propose that these neurons could play a role as guideposts for axons of olfactory receptor neurons growing toward the olfactory bulb.

Olfactory ensheathing glia

Olfactory nerve

PAX6

Vomeronasal organ

10.1007/s00429-012-0486-2

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Citations (33)

Proliferation, cell death and reelin expression during development of the retina in a teleost, the common trout (Salmo trutta fario)

The International Journal of Developmental Biology (2001)

Eva Candal Ramón Anadón HC Caruncho Isabel Rodríguez‐Moldes

We have analysed the spatiotemporal pattern of cell proliferation and apoptosis during the development of the retina in a teleost. Distribution of proliferating cells in different developmental stages (embryos, alevins, and juveniles) was analysed with an antibody against proliferating cell nuclear antigen (PCNA). After establishment of the retinal lamination, PCNA-immunoreactive (PCNA-ir) cells were frequently observed in all cell layers, with a high majority of proliferating cells located at the marginal (growing) retina. Clusters of PCNA-ir cells were characteristic of the inner nuclear layer (INL). The distribution of apoptotic cells was studied by the TUNEL method, which has revealed significant cell death before completion of the retinal lamination. We have also used an antibody against Reelin (RELN) as a marker for retinal cells that secrete this glycoprotein to the extracellular space. The pattern of RELN expression, as well as that of proliferating and dying cells was very similar to that described in tetrapods, suggesting that this protein regulates the cell migration and synaptogenesis in the different developmental stages of the retina.

Inner nuclear layer

Outer nuclear layer

Synaptogenesis

10.1387/ijdb.01450069

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Citations (2)

Regionalization of the Shark Hindbrain: A Survey of an Ancestral Organization

Frontiers in Neuroanatomy (2011)

Isabel Rodríguez‐Moldes Iván Carrera Sol Pose‐Méndez Idoia Quintana‐Urzainqui Eva Candal

Cartilaginous fishes (chondrichthyans) represent an ancient radiation of vertebrates currently considered the sister group of the group of gnathostomes with a bony skeleton that gave rise to land vertebrates. This out-group position makes chondrichthyans essential in assessing the ancestral organization of the brain of jawed vertebrates. To gain knowledge about hindbrain evolution we have studied its development in a shark, the lesser spotted dogfish Scyliorhinus canicula by analyzing the expression of some developmental genes and the origin and distribution of specific neuronal populations, which may help to identify hindbrain subdivisions and boundaries and the topology of specific cell groups. We have characterized three developmental periods that will serve as a framework to compare the development of different neuronal systems and may represent a suitable tool for comparing the absolute chronology of development among vertebrates. The expression patterns of Pax6, Wnt8, and HoxA2 genes in early embryos of S. canicula showed close correspondence to what has been described in other vertebrates and helped to identify the anterior rhombomeres. Also in these early embryos, the combination of Pax6 with protein markers of migrating neuroblasts (DCX) and early differentiating neurons (general: HuC/D; neuron type specific: GAD, the GABA synthesizing enzyme) revealed the organization of S. canicula hindbrain in both transverse segmental units corresponding to visible rhombomeres and longitudinal columns. Later in development, when the interrhombomeric boundaries fade away, accurate information about S. canicula hindbrain subdivisions was achieved by comparing the expression patterns of Pax6 and GAD, serotonin (serotoninergic neurons), tyrosine hydroxylase (catecholaminergic neurons), choline acetyltransferase (cholinergic neurons), and calretinin (a calcium-binding protein). The patterns observed revealed many topological correspondences with other vertebrates and led to reconsideration of the current view of the elasmobranch hindbrain segmentation as peculiar among vertebrates.

Hindbrain

Rhombomere

Scyliorhinus canicula

PAX6

10.3389/fnana.2011.00016

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Citations (26)

Contents, Vol. 137, 1990

Cells Tissues Organs (1990)

Isabel Rodríguez‐Moldes Jean‐Pierre Timmermans Dirk Adriaensen M.H.A. de Groodt-Lasseel D.W. Scheuermann

10.1159/000146897

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Citations (0)