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

Carrera, Iván; Sueiro, Catalina; Molíst, Pilar; Ferreiro, Susana; Adrio, Fátima; Rodríguez, Miguel Ángel; Anadón, Ramón; Rodríguez‐Moldes, Isabel

doi:10.1016/j.brainresbull.2005.02.010

Cited by 19 publications

(29 citation statements)

References 12 publications

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“…The few existing studies of the ontogeny of these hypothalamic systems in elasmobranchs reveal the existence of large temporal differences in their development. The catecholaminergic cells of the hypothalamus of the Lesser Spotted Dogfish differentiates early (stage 26), compared to structures of the mesencephalon and the rhombencephalon (stages 30-31) [Carrera et al, 2005]. The opposite happens with the hypothalamic serotoninergic cells, which differentiate late (stage 31) in relation to the rhombencephalic serotoninergic cells (stage 26) [Carrera et al, 2008b].…”

Section: Regionalization Of the Secondary Prosencephalon In The Lessementioning

confidence: 91%

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

Rodríguez‐Moldes

2009

Brain Behav Evol

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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.

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Section: Regionalization Of the Secondary Prosencephalon In The Lessementioning

confidence: 91%

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

Rodríguez‐Moldes

2009

Brain Behav Evol

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“…Although this group is a key for understanding the early evolutionary history of vertebrates, developmental studies are rather scarce. Knowledge of the development of neurotransmitter systems in Chondrichthyes is limited to a few studies of catecholaminergic and GABAergic systems in the lesser spotted dogfish Scyliorhinus canicula (Sueiro et al, 2003(Sueiro et al, , 2004(Sueiro et al, , 2007Carrera et al, 2005Carrera et al, , 2006Carrera et al, , 2008FerreiroGalve et al, 2008a,b). This dogfish has also been used in studies of gene expression during very early brain development (Sauka-Spengler et al, 2001Derobert et al, 2002a,b).…”

Section: Dogfish Cns Serotoninergic Systemmentioning

confidence: 97%

“…In order to compare the distribution of 5-HT-ir populations with that of some tyrosine hydroxylase (TH)-ir neurons (locus coeruleus, subcoeruleus reticular nucleus) previously described in developing dogfish (Carrera et al, 2005), series of sections of embryos and juveniles parallel to the series already used for TH were processed for 5-HT immunohistochemistry. In that study (Carrera et al, 2005), we followed a procedure similar to that indicated above but sections were incubated with a mouse monoclonal antibody raised against TH purified from PC12 cells (Chemicon, Temecula, CA;Cat.…”

Section: Immunocytochemistrymentioning

confidence: 99%

Development of the serotoninergic system in the central nervous system of a shark, the lesser spotted dogfish Scyliorhinus canicula

Carrera

Molíst

Anadón

et al. 2008

J of Comparative Neurology

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Chondrychthyans (cartilaginous fishes) are key to understanding the ancestral gnathostome condition since they provide an outgroup to sarcopterygians and actinopterygians. To gain comparative knowledge about the development of the vertebrate serotoninergic systems, we studied by immunohistochemistry the origin, spatiotemporal organization, and migration patterns of serotonin-containing neurons and the growth of axonal pathways in the central nervous system of a shark, the lesser spotted dogfish. Hindbrain serotonin-immunoreactive cells arose close to the floor plate and most populations migrated ventrally and mediolaterally to form the various raphe and reticular groups. The order of appearance of serotoninergic populations in the rhombencephalon and spinal cord (first the superior groups and then the inferior and spinal populations) roughly matched with that reported in other vertebrates but important differences were noted in the formation of prosencephalic groups in fishes. In addition to preoptic and hypothalamic areas, serotoninergic cerebrospinal fluid-contacting cells were observed in the isthmus (raphe dorsalis anterioris). Transient serotonin-immunoreactive cells were noted in the pineal organ, habenula, and pretectum. Further, we provide a revised anatomical framework for reticular and raphe serotoninergic populations considering their origin and segmental organization. Two distinct phases of development of the serotoninergic innervation were distinguished, that of the formation of the main axonal pathways and that of the branching of fibers. The development of main serotoninergic ascending pathways in dogfish was notably similar to that described in mammals. Our findings suggest the conservation of developmental patterns in serotoninergic systems and enhance the importance of elasmobranchs for understanding the early evolution of this system in vertebrates.

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“…However, some of the neuronal systems identified in adults as being related to the basal ganglia are not yet differentiated at this stage. A case in point are the subpallial catecholaminergic populations, which were not identified until juvenile stages, even though the diencephalic and mesencephalic catecholaminergic populations related to the basal ganglia (posterior tubercle nucleus and ventrotegmental area/substantia nigra) could be recognized from stage 26 and 31, respectively [Carrera et al, 2005[Carrera et al, , 2012.…”

Section: Stage-32 Embryosmentioning

confidence: 99%

“…2 h), at the level of the ventrotegmental area and substantia nigra. As retrogradely labeled cells were mainly observed in S. canicula in regions that contain abundant SP (as the area superficialis basalis, as shown in adults by Rodríguez-Moldes et al [1993]), and TH (as the diencephalic/mesencephalic tegmentum, as shown in embryos, juveniles, and adults by Carrera et al [2005Carrera et al [ , 2012), we performed double labeling experiments by combining the tracer with immunofluorescence for SP or TH. Double labeling of the tracer with the antibody against SP revealed double labeled cells neighboring the site of application of the tracer, as well as dorsolaterally and rostrally.…”

Section: Evidence Of Subpallial-mesencephalic Connectionsmentioning

confidence: 99%

Contributions of Developmental Studies in the Dogfish <b><i>Scyliorhinus canicula</i></b> to the Brain Anatomy of Elasmobranchs: Insights on the Basal Ganglia

Quintana‐Urzainqui

Sueiro²,

Carrera³

et al. 2012

Brain Behav Evol

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The basic anatomy of the elasmobranch brain has been previously established after studying the organization of the different subdivisions in the adult brain. However, despite the relatively abundant immunohistochemical and hodologic studies performed in different species of sharks and skates, the organization of some brain subdivisions remains unclear. The present study focuses on some brain regions in which subdivisions established on the basis of anatomical data in adults remain controversial, such as the subpallium, mainly the striatal subdivision. Taking advantage of the great potential of the lesser spotted dogfish, Scyliorhinus canicula, as a model for developmental studies, we have characterized the subpallium throughout development and postembryonic stages by analyzing the distribution of immunomarkers for GABA, catecholamines, and neuropeptides, such as substance P. Moreover, we have analyzed the expression pattern of regulatory genes involved in the regionalization of the telencephalon, such as Dlx2, Nkx2.1, and Shh, and followed their derivatives throughout development in relation to the distribution of such neurochemical markers. For further characterization, we have also analyzed the patterns of innervation of the subpallium after applying tract-tracing techniques. Our observations may shed light on postulate equivalences of regions and nuclei among elasmobranchs and support homologies with other vertebrates.

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

Cited by 19 publications

References 12 publications

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

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

Development of the serotoninergic system in the central nervous system of a shark, the lesser spotted dogfish Scyliorhinus canicula

Contributions of Developmental Studies in the Dogfish <b><i>Scyliorhinus canicula</i></b> to the Brain Anatomy of Elasmobranchs: Insights on the Basal Ganglia

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