Wilhelm His’ lasting insights into hindbrain and cranial ganglia development and evolution

Glover, Joel C.; Elliott, Karen L.; Erives, Albert; Chizhikov, Victor V.; Fritzsch, Bernd

doi:10.1016/j.ydbio.2018.02.001

Cited by 39 publications

(54 citation statements)

References 95 publications

(166 reference statements)

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“…In addition to inner ear defects, knock-out mice also display cerebellar and alar plate defects, head tossing, and circling behavior, indicative of vestibular defects (Steffes et al 2012; Glover et al 2018). We did not observe a gross vestibular, cerebellar, or cognitive phenotype currently present in our patients, although one of the two affected individuals did present with a below average intelligence.…”

Section: Discussionmentioning

confidence: 99%

A variant in LMX1A causes autosomal recessive severe-to-profound hearing impairment

et al. 2018

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Hereditary hearing impairment is a common sensory disorder that is genetically and phenotypically heterogeneous. In this study, we used a homozygosity mapping and exome sequencing strategy to study a consanguineous Pakistani family with autosomal recessive severe-to-profound hearing impairment. This led to the identification of a missense variant (p.Ile369Thr) in the LMX1A gene affecting a conserved residue in the C-terminus of the protein, which was predicted damaging by an in silico bioinformatics analysis. The p.Ile369Thr variant disrupts several C-terminal and homeodomain residue interactions, including an interaction with homeodomain residue p.Val241 that was previously found to be involved in autosomal dominant progressive HI. LIM-homeodomain factor Lmxla is expressed in the inner ear through development, shows a progressive restriction to non-sensory epithelia, and is important in the separation of the sensory and non-sensory domains in the inner ear. Homozygous Lmxla mutant mice (Dreher) are deaf with dysmorphic ears with an abnormal morphogenesis and fused and misshapen sensory organs; however, computed tomography performed on a hearing-impaired family member did not reveal any cochleovestibular malformations. Our results suggest that LMX1A is involved in both human autosomal recessive and dominant sensorineural hearing impairment.

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Section: Discussionmentioning

confidence: 99%

A variant in LMX1A causes autosomal recessive severe-to-profound hearing impairment

et al. 2018

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“…A, anterior; AC, anterior crista; Ascl1/Mash1, achaete-scute family basic helix-loop-helix transcription factor 1; Atoh7, atonal basic helix-loop-helix transcription factor 7; AVCN, antero-ventral cochlear nucleus; BMP, bone morphogenic protein; C, cochlea; CB, cerebellum; CN V, VII, IX, X, cranial nerve V, VII, IX, X; CP, choroid plexus of IV ventricle; D, dorsal; DCN, dorsal cochlear nucleus; dV, descending trigeminal tract; ELL, electroreceptive (ampullary organ) lateral line; GG, geniculate ganglion; HC, horizontal crista; L, lateral; LL, (mechanosensory) lateral line; M, medial; N, nasal; Neurog1/2, Neurogenin 1/2; NG, nodose ganglion; OB, olfactory bulb; OC, optic chiasm; OE, olfactory epithelium; P, posterior; PC, posterior crista; PG, petrosal ganglion; pV, principal trigeminal nucleus; r1, rhombomere 1; r2, rhombomere 2; S, saccule; SG, spiral ganglion; Shh, sonic hedgehog; ST, solitary tract; T, temporal; TIx3, T-cell leukemia homeobox 3; U, utricle; V, ventral; V1, ophthalmic branch of trigeminal nerve; V2, maxillary branch; V3, mandibular branch; VG, vestibular ganglion; VN, vestibular nucleus complex. Modified after 5, 12, 17, 33, 36, 54, 56, 63– 66.…”

Section: Molecular Odorant Mapmentioning

confidence: 99%

“…Central projections from distinct end organs show that the two types of vestibular receptors—the canals for angular acceleration and the otoconia bearing linear acceleration organs—have both discrete and overlapping projections 21, 123 , possibly reflecting that all angular acceleration prompts additional linear stimulation. Each of the segregated and common signals is related to rhombomere-specific nuclei with different outputs 17, 63 . An added complexity, shared with the lateral line system of mechanosensors, is the opposing polarity of hair cells in linear but not angular acceleration sensors 124, 125 .…”

Section: Vestibular Maps For Linear and Angular Acceleration Detectionmentioning

confidence: 99%

“…Instead of a point-to-point connection, each of the hindbrain targeting sensory neurons forms an extended longitudinal track along the alar plate of the hindbrain ( Figure 1C and Figure 2A). As a first approximation, the hindbrain alar plate can be regarded as a highly transformed part of the spinal cord that has developed rhombomere-specific nuclei, which receive hindbrain-specific innervation 109, 63, 178, 179 . Within each of the longitudinal hindbrain tracks, rhombomere-specific nuclei can be identified 5, 17, 178, 179– 182 , and each has its own higher-order projection.…”

Section: Overview Of Brainstem Mapsmentioning

confidence: 99%

“…In addition to “birth-dating” map of secondary neurons of the alar plate, the cell cycle exit varies among peripheral neurons ( Table 1), most obviously in the auditory system 57, 120 . The epibranchial derived neurons innervating the taste buds of the tongue project early in development to the solitary tract ( Table 1), long recognized as the first tract to form in the mammalian hindbrain 63, 170 . First-born and projecting neurons of a given ganglion form the most ventral projection in the alar plate and within a given alar plate nucleus 65, 183 .…”

Section: Overview Of Brainstem Mapsmentioning

confidence: 99%

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Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system

2019

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Interaction with the world around us requires extracting meaningful signals to guide behavior. Each of the six mammalian senses (olfaction, vision, somatosensation, hearing, balance, and taste) has a unique primary map that extracts sense-specific information. Sensory systems in the periphery and their target neurons in the central nervous system develop independently and must develop specific connections for proper sensory processing. In addition, the regulation of sensory map formation is independent of and prior to central target neuronal development in several maps. This review provides an overview of the current level of understanding of primary map formation of the six mammalian senses. Cell cycle exit, combined with incompletely understood molecules and their regulation, provides chemoaffinity-mediated primary maps that are further refined by activity. The interplay between cell cycle exit, molecular guidance, and activity-mediated refinement is the basis of dominance stripes after redundant organ transplantations in the visual and balance system. A more advanced level of understanding of primary map formation could benefit ongoing restoration attempts of impaired senses by guiding proper functional connection formations of restored sensory organs with their central nervous system targets.

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Transplantation of Ears Provides Insights into Inner Ear Afferent Pathfinding Properties

Gordy

Houston

Fritzsch

et al. 2018

Developmental Neurobiology

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Numerous tissue transplantations have demonstrated that otocysts can develop into normal ears in any location in all vertebrates tested thus far, though the pattern of innervation of these transplanted ears has largely been understudied. Here, expanding on previous findings that transplanted ears demonstrate capability of local brainstem innervation and can also be innervated themselves by efferents, we show that inner ear afferents grow toward the spinal cord mostly along existing afferent and efferent fibers and preferentially enter the dorsal spinal cord. Once in the dorsal funiculus of the spinal cord, they can grow toward the hindbrain and can diverge into vestibular nuclei. Inner ear afferents can also project along lateral line afferents. Likewise, lateral line afferents can navigate along inner ear afferents to reach hair cells in the ear. In addition, transplanted ears near the heart show growth of inner ear afferents along epibranchial placode-derived vagus afferents. Our data indicate that inner ear afferents can navigate in foreign locations, likely devoid of any local ear-specific guidance cues, along existing nerves, possibly using the nerve-associated Schwann cells as substrate to grow along. However, within the spinal cord and hindbrain, inner ear afferents can navigate to vestibular targets, likely using gradients of diffusible factors that define the dorso-ventral axis to guide them. Finally, afferents of transplanted ears functionally connect to native hindbrain vestibular circuitry, indicated by eliciting a startle behavior response, and providing excitatory input to specific sets of extraocular motoneurons.

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Wilhelm His’ lasting insights into hindbrain and cranial ganglia development and evolution

Cited by 39 publications

References 95 publications

A variant in LMX1A causes autosomal recessive severe-to-profound hearing impairment

A variant in LMX1A causes autosomal recessive severe-to-profound hearing impairment

Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system

Transplantation of Ears Provides Insights into Inner Ear Afferent Pathfinding Properties

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