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Origin of acoustic–vestibular ganglionic neuroblasts in chick embryos and their sensory connections

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Abstract

The inner ear is a complex three-dimensional sensory structure with auditory and vestibular functions. It originates from the otic placode, which generates the sensory elements of the membranous labyrinth and all the ganglionic neuronal precursors. Neuroblast specification is the first cell differentiation event. In the chick, it takes place over a long embryonic period from the early otic cup stage to at least stage HH25. The differentiating ganglionic neurons attain a precise innervation pattern with sensory patches, a process presumably governed by a network of dendritic guidance cues which vary with the local micro-environment. To study the otic neurogenesis and topographically-ordered innervation pattern in birds, a quail–chick chimaeric graft technique was used in accordance with a previously determined fate-map of the otic placode. Each type of graft containing the presumptive domain of topologically-arranged placodal sensory areas was shown to generate neuroblasts. The differentiated grafted neuroblasts established dendritic contacts with a variety of sensory patches. These results strongly suggest that, rather than reverse-pathfinding, the relevant role in otic dendritic process guidance is played by long-range diffusing molecules.

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Acknowledgements

We express our gratitude to Dr Tanaka for providing us with QN antibodies.

Funding

This work was supported by the following Grant sponsors: Spanish Ministry of Science, BFU2010-1946; Junta de Extremadura, GR10152, GR15158 and IB18046 (to M.H.-S.); Spanish MICINN Grant BFU2014-57516P; SENECA Foundation contract 19904/GERM/15 (to L.P.); Junta de Extremadura pre-doctoral studentshipvaage; Grant number PRE/08031 (to L.-O.S.-G.).

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Authors and Affiliations

  1. Department of Cell Biology, School of Science, University of Extremadura, E06071, Badajoz, Spain

    Luis Óscar Sánchez-Guardado & Matías Hidalgo-Sánchez

  2. Department of Human Anatomy and Psychobiology, School of Medicine, University of Murcia, E30100, Murcia, Spain

    Luis Puelles

  3. Instituto Murciano de Investigaciones Biosanitarias (IMIB-Arrixaca), E30100, Murcia, Spain

    Luis Puelles

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  1. Luis Óscar Sánchez-Guardado
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  3. Matías Hidalgo-Sánchez
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Contributions

MH-S, L-OS-G and LP designed experiments. L-OS-G and MH-S performed experiments. MH-S, L-OS-G and LP analysed data and wrote the manuscript.

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Correspondence to Matías Hidalgo-Sánchez.

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S1 Figure. Related to Figure 4. Grafted area of Type 1 graft.

(a) Schematic representation of the Type 1 experiment at the 10-somite stage, involving the macula utriculi area. (b-g) Horizontal sections through a representative Type 1 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the macula utriculi (between arrowheads in b, d) and a contiguous small area in the utricle wall (arrows in b, d). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (ac, pc, and mn in c, c’; lc and mu in d, d’; bp in e-g; ml in g). Differentiated neurons from the grafted area were also observed (arrows in e, f). (h, i) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 1 grafted-cell distribution. The horizontal sections are indicated in h and i. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral. (TIFF 14975 kb)

S2 Figure. Related to Figure 5. Grafted area of Type 2 graft.

(a) Schematic representation of the Type 2 experiment at the 10-somite stage, involving the macula sacculi area. (b-e) Horizontal sections through a representative Type 2 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the macula sacculi (between arrowheads in b, d) and a contiguous small area in the saccule wall (arrows in b, d). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (ac, pc, and mn in c, c’; lc and mu in d; bp in e; ml, not shown). (f, g) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 2 grafted-cell distribution. The horizontal sections are indicated in f and g. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral. (TIFF 15385 kb)

S3 Figure. Related to Figure 6. Grafted area of Type 3 graft.

(a) Schematic representation of the Type 3 experiment at the 10-somite stage, involving the entire basilar papilla area. (b-e) Horizontal sections through a representative Type 3 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the basilar papilla (between arrowheads in b, e) and a contiguous small area in the cochlear duct wall (arrows in b, e). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (ac, pc, and mn in c, c’; lc, mu, and ms in d; ml in f). (f, g) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 3 grafted-cell distribution. The horizontal sections are indicated in f and g. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral (TIFF 16438 kb)

S4 Figure. Related to Figure 7. Grafted area of Type 4 graft.

(a) Schematic representation of the Type 4 experiment at the 10-somite stage, involving the macula lagena and macula neglecta areas. (b-f) Horizontal sections through a representative Type 4 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the macula lagena and macula neglecta areas (between arrowheads in b, c) and their contiguous non-sensory areas (arrows in b, c, d). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (ac and pc in d; lc, mu, and ms in e; bp in f). Differentiated neurons from the grafted area were also observed (arrow in f). The graft formed a dorsoventrally arranged band in the cochlear duct (arrowheads in e, f). (g, h) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 4 grafted-cell distribution. The horizontal sections are indicated in g and h. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral. (TIFF 16723 kb)

S5 Figure. Related to Figure 8. Grafted area of Type 5 graft.

(a) Schematic representation of the Type 5 experiment at the 10-somite stage, involving the anterior and lateral cristae area. (b-e) Horizontal sections through a representative Type 5 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the anterior and lateral cristae area (between arrowheads in b, c, d) and their contiguous non-sensory areas (arrows in b, c, d). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (pc in d’; lc, mu, and ms in d; bp in e, f; ml in f). Some QCPN-stained cells from the grafted mesenchyme were also observed (short arrows in f). Differentiated neurons from the grafted area were also observed (large arrows in f, e). (g, h) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 5 grafted-cell distribution. The horizontal sections are indicated in g and h. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral. (TIFF 17270 kb)

S6 Figure. Related to Figure 9. Grafted area of Type 6 graft.

(a) Schematic representation of the Type 6 experiment at the 10-somite stage, involving the posterior crista area. (b-e) Horizontal sections through a representative Type 6 chimaeric embryo at 10 days of incubation (E10). The QCPN-positive grafted area contained exclusively the posterior crista area (between arrowheads in b, c) and its contiguous non-sensory areas (arrows in b, c). The rest of the sensory and non-sensory elements were completely devoid of QCPN-positive grafted quail cells (ac and mn in c; lc, mu, and ms in d; bp and ml in e). (f, g) Three-dimensional diagrams of a chimaeric inner ear summarising the Type 6 grafted-cell distribution. The horizontal sections are indicated in f and g. Abbreviations: C, caudal; D, dorsal; M, medial; R, rostral. (TIFF 13497 kb)

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Sánchez-Guardado, L.Ó., Puelles, L. & Hidalgo-Sánchez, M. Origin of acoustic–vestibular ganglionic neuroblasts in chick embryos and their sensory connections. Brain Struct Funct 224, 2757–2774 (2019). https://doi.org/10.1007/s00429-019-01934-5

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  • DOI: https://doi.org/10.1007/s00429-019-01934-5

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