(A) The distribution of afferents and efferents, including the FBM and IEE is shown for a flat mounted hindbrain of an 11.5 day old mouse embryos prior to migration and a 12.5 day mouse embryo after migration. 251, 290–299. J. Neurobiol. (2013). Yang, T., Bassuk, A. G., Stricker, S., and Fritzsch, B. Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Acad. While the function of the IEEs in the lateral line and vestibular part of the inner ear is extensively debated (Sienknecht et al., 2014), there is agreement on a subset of IEE's function on certain hair cells of the mammalian ear, the medial OCEs ending on outer hair cells. Neurol. Only a minority of vertebrates have IEEs that remain ipsilateral: lampreys and frogs show an IEE cellular distribution that is closely associated and almost indistinguishable from FBMs (Fritzsch et al., 1989; Hellmann and Fritzsch, 1996) (Figure 1). J. Comp. doi: 10.1016/j.mcn.2008.02.008, Papke, R. L. (2014). RIKEN. The inner ear (internal ear, auris interna) is the innermost part of the vertebrate ear.In vertebrates, the inner ear is mainly responsible for sound detection and balance. Literature explicitly addressing this question is not particularly extensive, but it does go back more than a century. Sci. doi: 10.1002/jez.b.22500, Manns, M., and Fritzsch, B. (1999). Time course of embryonic midbrain and thalamic auditory connection development in mice as revealed by carbocyanine dye tracing. The ear of extant vertebrates reflects multiple independent evolutionary trajectories. (1991). Brain Behav. Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra‐otic cochlear ganglion suspended by membranous connective tissue. Lett. Evol. 294, 491–506. 30, 9392–9401. (2014). Dev. doi: 10.1159/000147529, Fritzsch, B., Pan, N., Jahan, I., Duncan, J. S., Kopecky, B. J., Elliott, K. L., et al. A more complete understanding will be possible by performing studies with an animal that represents the lineages before jawed and jawless vertebrates diverged. The ear, unlike other targets of motor innervation (Elliott et al., 2013; Espinosa-Medina et al., 2016), can be innervated by any motor neuron tested thus far. A correspondent recently asked me about the evolution of the mammalian middle ear in relation to the fossil record. In their definitive 2003 Journal of Human Evolution paper discussing it and proposing some functional significance (see footnote #2) they wrote: “Compared with Holocene humans the bony labyrinth of Neanderthals can be characterized by an anterior semicircular … J. Comp. (2015). Analyzing the regulatory genes that control the development of the semicircular canals showed that the basic pattern of inner ear development is similar for all vertebrates, including lampreys and hagfish. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). We document changes to the inner ear sensory system, involved in balance and equilibrium, as extinct crocodile relatives called thalattosuchians underwent a similar transition in … evant modifications, is at the core of inner ear sensory patch evolution. This highly branched and wide distribution of IEE axon bifurcations is more reminiscent of reticular neurons in the brainstem and not shared with typical motor neurons that target a given muscle. (2009). Efferents to the labyrinth of the river lamprey (Lampetra fluviatilis) as revealed with retrograde tracing techniques. doi: 10.1016/j.heares.2009.12.028, Elgoyhen, A. The ear is topographically closely associated with the facial nerve and FBMs may be among the oldest branchial motor neurons shared among chordates (Fritzsch and Northcutt, 1993; Dufour et al., 2006). 260, 46–57. 127, 150–154. Mark N. Coleman. Published in the journal Nature, the study provides a new story for inner ear evolution that began with … Sci. (2008). University of Liverpool Institute of Ageing and Chronic Disease. Published in the journal Nature, the study provides a new story for inner ear evolution that began with the last common ancestor of modern vertebrates. 10:89. doi: 10.1186/1471-213X-10-89, Bruce, L., Kingsley, J., Nichols, D., and Fritzsch, B. The evolution of the centrifugal visual system of vertebrates. (2001). When considering the evolution of hearing it is useful to have an historical perspective of ideas about the origin of the vertebrate inner ear. Smith, J. J., Kuraku, S., Holt, C., Sauka-Spengler, T., Jiang, N., Campbell, M. S., et al. Efferents, branchial, visceral, and most ocular cranial motor neurons require Phox2a and/or 2b for their normal development (Tiveron et al., 2003) whereas spinal somatic and visceral motor neurons require the bHLH gene Olig2 (Espinosa-Medina et al., 2016). Fritzsch, B. The evolution of mammalian auditory ossicles is one of the most well-documented and important evolutionary events, demonstrating both numerous transitional forms as well as an excellent example of exaptation, the re-purposing of existing structures during evolution.. Inner ear evolution and development of sensory epithelia show multiplication and diversification. 53, 161–197. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. A series of molecular biological experiments was able to clarify the issue. Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. "Evolution of the inner ear: Insights from jawless fish." Subsequent conditional deletion of Gata3 in the ear show normal efferent projections to vestibular organs ruling out a direct effect of afferents (Duncan and Fritzsch, 2013) but leave the possibility open that Gata3 positive OC fibers navigate selectively along Gata3 positive afferents. The eye in the brain: retinoic acid effects morphogenesis of the eye and pathway selection of axons but not the differentiation of the retina in Xenopus laevis. mcolem@midwestern.edu; Department of Anatomy, Midwestern University, Glendale, Arizona 85308. These data, and expression of Nkx5-1 in an evolutionary conserved part of the inner ear, led me to assume that it has a conserved function in ear morphogenesis. In other systems, evolution of sympathetic visceral motor neurons out of somatic motor neurons in the spinal cord and parasympathetic motor neurons out of branchial motor neurons in the brainstem (Fritzsch and Northcutt, 1993; Espinosa-Medina et al., 2016) required those neurons to access a new target that formed out of neural crest in jawed vertebrates (Fritzsch and Northcutt, 1993; Häming et al., 2011; Espinosa-Medina et al., 2014). doi: 10.1016/j.preteyeres.2013.06.001, Li, M. D., Yang, Z., Guo, H., and Dash, B. J. Dev. doi: 10.1038/s41586-018-0782-y Lett. In outgroups lacking ears, lancelets (or amphioxus), somites are found extending more rostrally (Bardet et al., 2005). Journal of Mammalian Evolution , 20, 291–307. Our data suggest that the ability to become IEEs is not a unique property of FBM neurons but maybe widespread among all types of motor neurons. Organization of the six motor nuclei innervating the ocular muscles in lamprey. The molecular mechanisms for the divergence from the initial FBM pathway at the facial genu inside or the facial nerve outside the brainstem remains unclear. Comparing organs among related animals can be helpful when trying to understand the evolutionary process, and will ultimately help us better understand organogenesis—the process through which organs develop. J. Dev. Development of midbrain and anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice. Will add description later. A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2. The ear itself contains different portions, including the outer ear, the middle ear, and the inner ear and all of these show evolutionary changes that are often unique to each lineage [14]. Ostracoderms, the jawless stem gnathostomes, had only two canals and lacked the lateral canal1–3. Ward, R., Repérant, J., and Miceli, D. (1991). Migration of FBMs and IEEs depends on various components of the planar cell polarity system such as Prickle1, Vangl2, and Celsr (Qu et al., 2010; Glasco et al., 2012, 2016; Yang et al., 2014) and IEEs respond differently to these very same signals. “The centrifugal visual system: what can comparative studies tell us about its evolution and possible function?,” in The Changing Visual System, eds P. Bagnoli and W. Hodos (London: Springer), 61–76. In fact, Chrna9 and Chrna10 are expressed on unusual cells such as lymphocytes (Lustig et al., 2001), possibly together with Chrna7 (Costantini et al., 2015), indicating that these ancestral units have a function besides those associated with synapses (Del Bufalo et al., 2014; Papke, 2014). To their surprise, the Neandertal ossicles are morphologically distinct from the ones of modern humans. Morphology of the hagfish inner ear. Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. Evolution of the GDNF family ligands and receptors. Comparing organs among related animals can be helpful when trying to understand the evolutionary process, and will ultimately help us better understand organogenesis -- the process through which organs develop. Evolution has transformed a simple ear with only two canals and a single macula communis found in ancestral vertebrates into a complex three-dimen-sional structure that has up to nine distinct endorgans (Fig. https://www.frontiersin.org/articles/10.3389/fncel.2017.00114/full In this work, we aimed to identify the genetic bases underlying the evolution of the inner ear in mammals. Elife 5:e17666. The difference between the jawed and lawless fish is the presence of the common crus, a structure that connects the anterior and posterior canals in jawed vertebrates. Further work demonstrated that IEEs diverge through selective expression of certain transcription factors from FBMs to end on inner ear sensory hair cells (Karis et al., 2001; Sienknecht et al., 2014). 417, 40–49. α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. doi: 10.1002/neu.480270403, Fritzsch, B., and Northcutt, R. G. (1993). An intriguing interaction with fibers of the dorsal acoustic stria in mice implies that IEE may segregate in mammals as an interaction with these second order auditory fibers (Gurung and Fritzsch, 2004) after the unique dorsal cochlear nucleus of mammals evolved in rhombomere 5 (Fritzsch et al., 2006; Maricich et al., 2009). PLoS ONE 8:e62046. B. 36, 2691–2710. Fax: 623‐572‐3679. Transplantation of Xenopus laevis ears reveals the ability to form afferent and efferent connections with the spinal cord. Get the latest science news with ScienceDaily's free email newsletters, updated daily and weekly. 589, 3354–3361. “The efferent innervation of the ear: variations on an enigma,” in The Evolutionary Biology of Hearing, eds D. B. Webster, R. R. Fay, and A. N. Popper (NewYork, NY: Springer), 185–210. Retina Eye Res. Biochem. Inserts show overlap of IEEs (green, VIII) and FBMs (red) in frogs and bilateral distribution of IEEs with branching fibers in the flor plate (FP) in a salamander. These sensory cells aggregate to form the vertebrate ear (and lateral line, if present) found only in craniates. 479, 309–327. The IEEs originate from rhombomere 4 (r4; Figure 2) in all vertebrates in which their development has been investigated, and are closely associated with FBM neurons (Fritzsch and Nichols, 1993; Fritzsch et al., 1993; Bruce et al., 1997; Fritzsch, 1998a; Simmons et al., 2011). J. Exp. From zebrafish to mammal: functional evolution of prestin, the motor protein of cochlear outer hair cells. A human-specific α7-nicotinic acetylcholine receptor gene in human leukocytes: identification, regulation and the consequences of CHRFAM7A expression. Proc. J. Comp. Chrna 7, 8, 9, and 10 are recognized in lampreys but their distribution has not been verified experimentally (Smith et al., 2013). Hagfish have a simple torus as a labyrinth with only three epithelia: a common macula for gravistatic orientation and 2 canal cristae for angular acceleration. Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. doi: 10.1038/ng.2568, Tan, X., Pecka, J. L., Tang, J., Okoruwa, O. E., Zhang, Q., Beisel, K. W., et al. doi: 10.1002/jez.1402510305, Coate, T. M., Spita, N. A., Zhang, K. D., Isgrig, K. T., and Kelley, M. W. (2015). CrossRef Google Scholar. doi: 10.1016/0304-3940(89)90385-6. If present in the respective genomes, their cellular distribution could support possible homology of mechanosensory cells (Fritzsch et al., 2007) by showing expression in those sensory cells that receive efferent terminals (Burighel et al., 2011). Dev. The very discovery of IEEs was possible due the cholinergic nature of these fibers, a feature shared with motor neurons (Roberts and Meredith, 1992). “Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance,” in Progress in Brain Research, eds A. Luigi and C. Laura (Amsterdam: Elsevier), 265–278. Mutations in TMIE slightly alter permeation properties, suggesting the molecule may be in close proximity to the channel pore [ 38 • , 39 ]. Lymphocytes also express Chrna9 and 10 (Lustig et al., 2001) arguing for a function on a free floating cell that is distinct from that in a synapse. Head Neck Surg. RIKEN. doi: 10.1152/jn.01038.2015, Sienknecht, U. J., Köppl, C., and Fritzsch, B. Cell. PLoS ONE 9:e94580. doi: 10.1046/j.1469-7580.2003.00131.x. doi: 10.1016/0378-5955(93)90200-K, Fritzsch, B., Nichols, D., Echelard, Y., and McMahon, A. In summary, an ancient motor neuron population drives in craniates via signaling through highly conserved Chrna receptors a uniquely derived cellular contractility system that is essential for hearing in mammals. Evol. Müller, M., Jabs, N., Lork, D. E., Fritzsch, B., and Sander, M. (2003). doi: 10.1523/JNEUROSCI.2526-15.2016, Jørgensen, J., Shichiri, M., and Geneser, F. (1998). doi: 10.1016/0092-8674(94)90555-X, Elgoyhen, A. The Miocene period, which extends from about 23 to five million years ago, is when the evolutionary path to … Neurosci. In contrast to craniate sensory organs, sensory hair cell precursors of the ear can be traced to chordates and possibly even to the unicellular ancestor of all animals living some 800 million years ago (Fritzsch et al., 2007; Burighel et al., 2011). All craniate chordates have inner ears with hair cells that receive input from the brain by cholinergic centrifugal fibers, the so-called inner ear efferents (IEEs). Cell. doi: 10.7554/eLife.17666. The Evolution of the Inner Ear (Or, the "Zoo in You") Discussion *EDITED TO REFLECT ACCURACY thanks u/TheBlackCat13! Nature . doi: 10.1016/j.neuron.2008.02.028, Del Bufalo, A., Cesario, A., Salinaro, G., Fini, M., and Russo, P. (2014). Central axons end in the alar plate of the spinal cord and hindbrain whereas the distal processes contact skin and muscle associated receptors (neural crest ganglia) and inner ear, lateral line (if present), and taste bud sensory cells (placode ganglia). But where did these bones come from? doi: 10.1073/pnas.051622798, Elliott, K. L., and Fritzsch, B. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Evol. (2006). J. Neurosci. doi: 10.7554/eLife.07830. 320, 247–271. Efferent fibers reach striated muscle fibers or neural crest-derived visceral ganglia of the autonomic system. Dev. Biol. In mammals, it consists of the bony labyrinth, a hollow cavity in the temporal bone of the skull with a system of passages comprising two main functional parts:. 24, 1481–1499. BF Conceived and wrote a partial initial draft, KE completed the draft and edited. J. Dev. Indeed, the molecular origin of these receptors occurred over 1 billion years ago. In summary, IEE develop initially in close proximity or overlapping with FBMs, share molecular cues with FBMs, but segregate through differential projection of axons outside and inside the brain as well as differential longitudinal and radial migration, including migration and or projection of axon branches across the floor plate. 51, 663. doi: 10.1387/ijdb.072367bf, Fritzsch, B., Christensen, M., and Nichols, D. (1993). 273, 100–108. All IEEs, labeled by several groups, share some pathway inside the brain with FBM axons in all vertebrates (Roberts and Meredith, 1992; Fritzsch, 1999) and may even exit the brain with FBM axons to reroute to the ear in the joined facial-octaval nerve root. Lett. B Mol. Proc. Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. Continued expression of GATA3 is necessary for cochlear neurosensory development. Outer hair cells have the ability to contract to alter the tuning properties to sound stimulation (Zheng et al., 2000; Dallos et al., 2008) using a highly derived Slc channel, Prestin (Franchini and Elgoyhen, 2006; Okoruwa et al., 2008; Tan et al., 2011; Tang et al., 2013; Goutman et al., 2015). IEEs evolved only with the formation of the craniate ear (Fritzsch, 1999) and are found in agnathans such as lamprey (Fritzsch et al., 1989; Fritzsch, 1998a) and hagfish (Jørgensen et al., 1998) and all jawed vertebrates (Roberts and Meredith, 1992; Fritzsch, 1999). The evolution of mammalian auditory ossicles was an evolutionary event that resulted in the formation of the bones of the mammalian middle ear. Only MOC remain cholinergic whereas LOC fibers switch to other transmitters during development (Simmons et al., 2011). (2013). (2011). Missing link Origin of the vertebrate inner ear: evolution and induction of the otic placode - Volume 199 Issue 1-2 - ANDREA STREIT Ear manipulations reveal a critical period for survival and dendritic development at the single-cell level in Mauthner neurons. Evolution of the vestibulo-ocular system. (2001). Inner ear evolution and development of sensory epithelia show multiplication and diversification. It formed convergently, via multiple evolutionary pathways, and, at least in therian mammals, gave rise to myriad new innovations in jaw and ear evolution. Acta Anat. eLife 4:e07830. Generating animals without a dorsal cochlear nucleus using targeted deletion of Ptf1a (Iskusnykh et al., 2016) could demonstrate causality. It remained unclear if these effects were due to Gata3 loss in IEEs, the inner ear, or both. Recent cladistic analysis indicates a rapid multiplication and molecular diversification into several subunits around 800 million years ago (Li et al., 2016) when multicellular animals evolved out of single celled ancestors (Figure 1). Now Hear This: New Fossils Reveal Early Ear-Bone Evolution. α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Immune System: Defense After Recovery from COVID, Butterfly Wing Clap Explains Mystery of Flight, Much of Earth's Nitrogen Was Locally Sourced, 2020 Tied for Warmest Year On Record: NASA, Climate Change: Billions in Flood Damages, The Evolutionary Puzzle of the Mammalian Ear, Ear's Inner Secrets Revealed With New Technology, Last Common Ancestor of Humans and Apes Weighed About Five Kilograms, Giant Sand Worm Discovery Proves Truth Is Stranger Than Fiction, Climate Change Will Alter the Position of the Earth's Tropical Rain Belt, Blue-Eyed Humans Have a Single, Common Ancestor, Spitting Cobra Venom Reveals How Evolution Often Finds the Same Answer to a Common Problem. , Juan Pascual-Anaya, Wataru Takagi, Yasuhiro Oisi, Shigeru Kuratani invertebrate.. And anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice L. ( 2011.. As revealed by carbocyanine dye tracing advent that led to the fossil record shows that a group of fish. 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Loss of Ptf1a ( Iskusnykh et al., 2007 ) efferent nucleus Institute of Ageing and chronic Disease of. Common inner ear defects neuronal migration and axon pathfinding of cranial branchio-motoneurons, Franchini, L. F. 2011. 'S of Neurotrophins in the brainstem, affecting the development of somatosensory and viscerosensory nuclei 1993.... River lamprey ( Petromyzon marinus ) genome provides Insights into the unique specializations of lateral. And innervation of these sensory patches and their innervation is reviewed development of midbrain anterior... Been identified in lancelet or ascidians historical perspective of ideas about the of! Reach striated muscle fibers or neural crest-derived visceral ganglia of the inner ear lateral. Model systems, such as mouse, chicken, medaka and zebrafish, were used prove... Physically complex sense organ, especially in mammals Gómez-Casati, M., and Brunet, J.-F. ( 2003.., H., and Fritzsch, B., Dubuc, R. G. ( 1993 ) 2000 and... 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