Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction

Dyballa, Sylvia; Savy, Thierry; Germann, Philipp; Mikula, Karol; Remešíková, Mariana; Špir, Róbert; Zecca, Andrea; Peyriéras, Nadine; Pujades, Cristina

doi:10.7554/elife.22268

Cited by 20 publications

(23 citation statements)

References 42 publications

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“…We sought to determine how size control is achieved in the zebrafish otic vesicle, a 3D lumenized epithelial cyst that becomes the inner ear. Prior studies used qualitative observations and 4D imaging to examine the formation of the otic vesicle (Haddon and Lewis, 1996; Hoijman et al, 2015; Dyballa et al, 2017). To systematically investigate inner ear morphogenesis at longer timescales between 12–45 hours post-fertilization (hpf), we used high-resolution 3D+ t confocal imaging combined with automated algorithms for quantifying cell and tissue morphology (Figure 1—figure supplement 1A–F) (Megason, 2009).…”

Section: Resultsmentioning

confidence: 99%

Size control of the inner ear via hydraulic feedback

Mosaliganti

Swinburne

Chan

et al. 2019

eLife

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Animals make organs of precise size, shape, and symmetry but how developing embryos do this is largely unknown. Here, we combine quantitative imaging, physical theory, and physiological measurement of hydrostatic pressure and fluid transport in zebrafish to study size control of the developing inner ear. We find that fluid accumulation creates hydrostatic pressure in the lumen leading to stress in the epithelium and expansion of the otic vesicle. Pressure, in turn, inhibits fluid transport into the lumen. This negative feedback loop between pressure and transport allows the otic vesicle to change growth rate to control natural or experimentally-induced size variation. Spatiotemporal patterning of contractility modulates pressure-driven strain for regional tissue thinning. Our work connects molecular-driven mechanisms, such as osmotic pressure driven strain and actomyosin tension, to the regulation of tissue morphogenesis via hydraulic feedback to ensure robust control of organ size.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (<xref ref-type="decision-letter" rid="SA1">see decision letter</xref>).

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Section: Resultsmentioning

confidence: 99%

Size control of the inner ear via hydraulic feedback

Mosaliganti

Swinburne

Chan

et al. 2019

eLife

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“…The pattern of hair cell innervation of afferents along the mediolateral axis of the ganglion suggested a possible link between developmental sequence and connectivity. In the vestibular ganglion, early born afferents occupy the most lateral edge of the nascent ganglion (Dyballa et al, 2017;Vemaraju et al, 2012;Zecca et al, 2015). Later-born afferents are added more medially, forming a half-shell around the earliest born somata.…”

Section: Organization Of the Utricular Ganglion By Developmental Sequencementioning

confidence: 99%

The organization of the gravity-sensing system in zebrafish

Liu

Hildebrand

Morgan

et al. 2021

Preprint

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Motor circuits develop in sequence from those governing fast movements to those governing slow. Here we examine whether upstream sensory circuits are organized by similar principles. Using serial-section electron microscopy in larval zebrafish, we generated a complete map of the gravity-sensing (utricular) system from the inner ear to the brainstem. We find that both sensory tuning and developmental sequence are organizing principles of vestibular topography. Patterned rostrocaudal innervation from hair cells to afferents creates a directional tuning map in the utricular ganglion, forming segregated pathways for rostral and caudal tilt. Furthermore, the mediolateral axis of the ganglion is linked to both developmental sequence and temporal kinetics. Early-born pathways carrying phasic information preferentially excite fast escape circuits, whereas later-born pathways carrying tonic signals excite slower postural and oculomotor circuits. These results demonstrate that vestibular circuits are organized by tuning direction and kinetics, aligning them with downstream motor circuits and behaviors.

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“…Thirdly, neuronal connectivity could be conferred retrogradely from the oculomotor neuron pools, which are segregated spatially during development (Greaney et al, 2016), as has been suggested for the chick (Glover, 1996) and shown for spinal interneurons (Baek et al, 2017). Finally, temporal cues could guide fate decisions: recent in vivo timelapse imaging demonstrated how peripheral afferents develop systematically in time (Zecca et al, 2015; Dyballa et al, 2017). Similar organization by birthdate has been demonstrated in extraocular motoneurons (Greaney et al, 2016) and spinal motor circuits (McLean and Fetcho, 2009) using genetically-encoded photoconvertible markers of post-mitotic neurons.…”

Section: Open Questions Well-suited To the Zebrafish Modelmentioning

confidence: 99%

Development of vestibular behaviors in zebrafish

Bagnall

Schoppik

2018

Current Opinion in Neurobiology

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Most animals orient their bodies with respect to gravity to facilitate locomotion and perception. The neural circuits responsible for these orienting movements have long served as a model to address fundamental questions in systems neuroscience. Though postural control is vital, we know little about development of either balance reflexes or the neural circuitry that produces them. Recent work in a genetically and optically accessible vertebrate, the larval zebrafish, has begun to reveal the mechanisms by which such vestibular behaviors and circuits come to function. Here we highlight recent work that leverages the particular advantages of the larval zebrafish to illuminate mechanisms of postural development, the role of sensation for balance circuit development, and the organization of developing vestibular circuits. Further, we frame open questions regarding the developmental mechanisms for functional circuit assembly and maturation where studying the zebrafish vestibular system is likely to open new frontiers.

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Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction

Cited by 20 publications

References 42 publications

Size control of the inner ear via hydraulic feedback

Size control of the inner ear via hydraulic feedback

The organization of the gravity-sensing system in zebrafish

Development of vestibular behaviors in zebrafish

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