Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve

Quintana‐Urzainqui, Idoia; Rodríguez‐Moldes, Isabel; Candal, Eva

doi:10.1007/s00429-012-0486-2

Cited by 32 publications

(35 citation statements)

References 97 publications

(178 reference statements)

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“…The specificity of the antibodies against GAD, TH, DCX and Pax6 in the brain of the lesser spotted dogfish was previously confirmed by Western blot or preadsorption test (Sueiro et al 2004;Carrera et al 2012;Quintana-Urzainqui et al 2012b). The same GAD antiserum has enabled identification of subpallial-derived GABAergic cells in the developing pallium of S. canicula ).…”

Section: Control and Specificity Of The Antibodiesmentioning

confidence: 86%

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

et al. 2014

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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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Section: Control and Specificity Of The Antibodiesmentioning

confidence: 86%

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

et al. 2014

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“…The main events that take place during the development of the olfactory system from the olfactory placode in the lesser spotted dogfish (S. canicula) have been framed into three developmental periods on the basis of tract-tracing experiments and expression of immunohistochemical markers [Quintana-Urzainqui et al, 2014]. In the present study, these developmental events in the olfactory system were used to describe a cluster of neurons and associated nerve fibers that represent the primordia of the terminal ganglia and nerve.…”

Section: Resultsmentioning

confidence: 99%

“…The fact that this neuronal population seemed to bypass the OB and projected its axons towards the rostral telencephalon, as observed from stage 28, is good evidence that it may represent the developing terminal nerve system. The putative terminal nerve population was easily discernible from ON cells by their different GFAP and Pax6 expression [Quintana-Urzainqui et al, 2014]. Unlike the ON-associated cell mass (arrows in fig.…”

Section: Second Period (Migratory Period): Stages 25-30mentioning

confidence: 98%

“…A recent developmental study from our group in the shark Scyliorhinus canicula reported a transient, heterogeneous cell population associated with the olfactory nerve (ON), which corresponds to the so-called migratory mass in rodents [Miller et al, 2010;Blanchart et al, 2011], from which a cluster of neurons seemed to deviate near the entrance to the olfactory bulb (OB), suggesting that this cluster belongs to the terminal nerve system [Quintana-Urzainqui et al, 2014]. In the present study, we characterized the development of this 'deviated' neuronal population and its relation with the olfactory system.…”

mentioning

confidence: 99%

“…In the present study, we characterized the development of this 'deviated' neuronal population and its relation with the olfactory system. For this purpose, we used tract-tracing techniques in combination with immunohistochemistry for reliable markers of the terminal nerve system (FMRF-amide peptide) and markers previously used [Ferreiro-Galve et al, 2012a;Quintana-Urzainqui et al, 2014] for characterizing components of the developing olfactory system as Pax6-expressing cells along the ON (Pax6), glial cells (GFAP, glial fibrillary acidic protein), early postmitotic neurons (HuC/D), migrating immature neurons and their growing fibers (DCX, doublecortin) and mature olfactory neurons (ORNs) and primary olfactory tracts (Gα0 protein). Due to the protracted development of S. canicula and the relative large size of the olfactory and terminal nerve structures, this species was particularly advantageous to analyze the development of these systems.…”

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Development of the Terminal Nerve System in the Shark <b><i>Scyliorhinus canicula</i></b>

Quintana‐Urzainqui

Anadón²,

Candal³

et al. 2014

Brain Behav Evol

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The nervus terminalis (or terminal nerve) system was discovered in an elasmobranch species more than a century ago. Over the past century, it has also been recognized in other vertebrate groups, from agnathans to mammals. However, its origin, functions or relationship with the olfactory system are still under debate. Despite the abundant literature about the nervus terminalis system in adult elasmobranchs, its development has been overlooked. Studies in other vertebrates have reported newly differentiated neurons of the terminal nerve system migrating from the olfactory epithelium to the telencephalon as part of a ‘migratory mass' of cells associated with the olfactory nerve. Whether the same occurs in developing elasmobranchs (adults showing anatomically separated nervus terminalis and olfactory systems) has not yet been determined. In this work we characterized for the first time the development of the terminal nerve and ganglia in an elasmobranch, the lesser spotted dogfish (Scyliorhinus canicula), by means of tract-tracing techniques combined with immunohistochemical markers for the terminal nerve (such as FMRF-amide peptide), for the developing components of the olfactory system (Gα0 protein, GFAP, Pax6), and markers for early postmitotic neurons (HuC/D) and migrating immature neurons (DCX). We discriminated between embryonic olfactory and terminal nerve systems and determined that both components may share a common origin in the migratory mass. We also localized the exact point where they split off near the olfactory nerve-olfactory bulb junction. The study of the development of the terminal nerve system in a basal gnathostome contributes to the knowledge of the ancestral features of this system in vertebrates, shedding light on its evolution and highlighting the importance of elasmobranchs for developmental and evolutionary studies.

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Wide‐ranging migration and destination of early olfactory placode‐derived neurons in chick embryos

Miyakawa

Murakmai

Uchiyama

2022

The Anatomical Record

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Cell migration from the olfactory placode (OP) is a well-known phenomenon wherein various cell types, such as gonadotropin-releasing hormone (GnRH)producing neurons, migrate toward the telencephalon (TEL) during early embryonic development. However, the spatial relationship between early migratory cells and the forebrain is unclear. We examined the early development of whole-mount chick embryos to observe the three-dimensional spatial relationship among OP-derived migratory neurons, olfactory nerve (ON), and TEL. Migratory neurons that express highly polysialylated neural cell adhesion molecule (PSA-NCAM) emerge from the OP and spread over a relatively wide TEL area at the Hamburger and Hamilton (HH) stage 17. Most migratory neurons form a cellular cord between the olfactory pit and rostral TEL within HH18-20. The earliest axons from the olfactory epithelium (OE) were detected along this neuronal cord using DiI-labeling at HH21. Furthermore, a few PSA-NCAM-positive neurons were dispersed around the cellular cord and over the lateral TEL at HH18. A long cellular cord branch extending to the lateral TEL was transiently observed within HH18-24. These results suggest a novel migratory route of OP-derived neurons during the early developmental stages. Following GFP vector introduction into the OP of HH13-15 embryos, labeled neurons were detected around and within the lateral TEL at HH23 and HH27. At HH36, labeled cells were observed in the rostral-lateral TEL, including the olfactory bulb (OB) region. GFP-labeled and calretinin-positive neurons were detected in the OB, suggesting that early OP-derived neurons enter the forebrain and function as interneurons in the OB.

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Developmental, tract-tracing and immunohistochemical study of the peripheral olfactory system in a basal vertebrate: insights on Pax6 neurons migrating along the olfactory nerve

Cited by 32 publications

References 97 publications

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

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

Development of the Terminal Nerve System in the Shark <b><i>Scyliorhinus canicula</i></b>

Wide‐ranging migration and destination of early olfactory placode‐derived neurons in chick embryos

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