Ear and Lateral Line of Vertebrates: Organisation and Development

Abstract

In vertebrates, perception of movement and sound is accomplished by the lateral line and inner ear sensory systems. These systems sense reverberations, movement and acceleration by transducing mechanical stimuli from the environment into electrical signals by means of mechanosensory hair cells. Vestibular and auditory hair cells have associated sensory neurons that transmit these signals from the periphery to the central nervous system. During development, cranial sensory systems arise from an initially homogeneous population of cells that ultimately give rise to discrete sensory structures. Although the demands for auditory and vestibular sensation differ between species and environments, vertebrates use common cell types, genetic programmes and molecules to achieve the development of these mechanosensory organs. In this article, the structure and function of the mechanosensory hair cells, lateral line and inner ear and how these systems develop across species are discussed, and as well as the innervation of these systems.

Key Concepts:

  • The vertebrate inner ear is composed of both auditory and vestibular components.

  • Both the lateral line and the inner ear are derived from embryonic structures known as cranial placodes.

  • All cranial placodes originate from a homogenous group of cells known as the preplacodal ectoderm.

  • Hair cells are structurally and functionally similar in both auditory and lateral line systems.

  • The adult lateral line mediates sensation of movement in the aquatic environment of fishes and frogs.

  • Embryonic posterior lateral line development is accomplished by the preā€patterned posterior lateral line primordium.

  • The lateral line is an experimentally accessible model for studying mechanosensory system development and biology.

Keywords: lateral line; inner ear; mechanosensory hair cells; development; vestibular; auditory; cranial placodes; primordium

Figure 1.

Mechanosensory hair cells: Schematic showing general features of the hair cell. The apical end includes stereocilia and kinocililum‐containing hair bundle, tip links and mechanotransduction channel. Basal features include the ribbon synapse, afferent and efferent innervation. Note that the ribbon synapse was initially discovered in photoreceptors, where it has a ‘ribbon‐like’ shape, but it appears more circular in hair cells.

Figure 2.

Schematic of the inner ear and its associated sensory structures, the maculae and the cristae. (a) Depiction of the inner ear showing the three semicircular canals in blue, these canals contain the vestibular sensory structures, the cristae. Illustrated in green is the vestibular region containing the utricle and saccule, which harbour the otolith organs, the maculae. Nerve fibres of the SAG are shown in red, and the auditory component of the inner ear, the cochlea, is depicted in purple. (b) Illustration of the maculae showing in detail the otolithic membrane which covers the stereocilia of the sensory hair cells, the associated support cells and nerve fibres. (c) Representative image of the cristae contained in the semicircular canals, kinocilium of the hair cells projects into the cupula.

Figure 3.

Illustration of early otic development and patterning. (a) Dorsal view of a generalised embryo at the end of gastrulation, the horseshoe‐shaped PPE domain is depicted in red. This domain adjoins the neural plate (light blue) and is lateral to the forming neural crest (green), in blue is the non‐neural ectoderm. The PPE is defined at this stage by the expression of the factors six, dlx and Eya. (a′) A unilateral cross‐section at the indicated axis and the same time point as in (A). The neural plate (blue) and the cephalic mesoderm (green) secrete Fgfs that induce the PPE (red); Wnt and BMP inhibitors are expressed in the PPE. (b) Early neurulation stage, precursors for both the otic and epibranchial placodes are contained in a common domain (purple) defined by the expression of Foxi1 and Dlx3/4. (b′) Cross‐section of an early neurulation stage embryo at the indicated axis (b). Continued Fgf signalling from the neural tube and cephalic mesoderm induce the common otic/epibranchial domain. (c) Neurulation stage embryo illustrating the segregation of the early otic placode in blue, defined by its expression of Sox3, Pax2 and Pax8. (c′) Cross‐section of a neurulation stage embryo at the indicated axis (c). At this stage, Wnt signalling from the neural tube works in conjunction with the Notch pathway to define the early otic domain, continued Fgf signalling from the cephalic mesoderm defines the epibranchial domain. (d) Illustration of the signalling pathways involved in early otic regionalisation. Fgf defines the anterior whereas an RA gradient is responsible for the posterior; Wnt signalling imparts dorsal identity whereas hH signalling sets up the ventral axis. (d′) Factors that define molecular asymmetries during otic patterning: Dlx5, Pax2 for dorsal; Pax5, Hmx2 for anterior; Otx2 for ventral and Fst1 for posterior.

Figure 4.

Lateral line mechanosensory hair cells: (a) Schematic showing lateral views of larval (7 days postfertlisation) and adult (6 months postfertilisation) zebrafish lateral line patterns (red dots). In the adult, neuromasts are arranged in dorsal–ventral oriented ‘stitches’ on the trunk, and in dermal canals on the head. (b) Idealised schematic of a cross‐section of a single lateral line neuromast showing two representative hair cells that extend stereocilia and kinocilia (encased in the gelatinous cupula and stabilised by the actin‐rich cuticular plate at the apical end of the hair cells) into the environment to sense changes in water current. Hair cells are surrounded by supporting cells and mantle cells and are innervated by afferent and efferent axons. (c) Schematic showing a top‐down view of kinocilia and stereocilia orientation in dorsoventral and anterioposterior sensing neuromasts. All schematics are not drawn to scale.

Figure 5.

Development of the posterior lateral line: (a) 30 hpf zebrafish embryo. The posterior lateral line ganglion is positioned behind the ear, with posterior lateral line (red) migrating down the trunk. (b) Rosette renewal in the posterior lateral line. Leading region progenitors (red) give rise to columnar daughter cells (blue), which constrict apically to give rise to a nascent rosette. Mature rosettes are deposited at the trailing part of the posterior lateral line. Colours indicate the same groups of cells over time. (c) Model of apical constriction in the leading portion of the posterior lateral line. Fgf activates the Ras‐MAPK pathway, which likely transcriptionally activates shroom3. Shroom3 anchors Rho‐kinase (Rock) in the apical domain of the cell, activating the actomysoin cytoskeleton. (d) Lateral line axon extension. Pioneer axons (dark green) extend with the primordium. Follower axons (light green) extend later.

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Further Reading

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Streit A (2004) Early development of the cranial sensory nervous system: from a common field to individual placodes. Developmental Biology 276: 1–15.

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Harding, Molly, McCarroll, Matthew, McGraw, Hillary, and Nechiporuk, Alex(Nov 2013) Ear and Lateral Line of Vertebrates: Organisation and Development. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000790.pub3]