Cooke, J. Neuron 58, 333–339. (2014). (2014). Jawed vertebrates have inner ears with three semicircular canals, the presence of which has been used as a key to understanding evolutionary relationships. 10, 300–315. Prestin and the cholinergic receptor of hair cells: positively-selected proteins in mammals. In vertebrates, the ear develops at the rostral boundary of the somites that form out of mesoderm along the notochord (Cooke, 1978; Chung et al., 1989; Huang et al., 1997). 89, 1–11. Anat. Another distinguishing feature of IEEs is their sometimes extremely widespread distribution of axonal branches that can cover adjacent organ systems such as multiple inner ear sensory epithelia and can be bilateral to both ears (Fritzsch and Wahnschaffe, 1987; Cowan et al., 2000) or even connect both inner ear and lateral line organs (Hellmann and Fritzsch, 1996). From Jaw to Ear: Transition Fossil Reveals Ear Evolution in Action. (2009). doi: 10.1159/000094087, PubMed Abstract | CrossRef Full Text | Google Scholar, Bailey, E. M., and Green, S. H. (2014). RIKEN. doi: 10.1371/journal.pone.0094580, Maricich, S. M., Xia, A., Mathes, E. L., Wang, V. Y., Oghalai, J. S., Fritzsch, B., et al. J Assoc Res Otolaryngol, 18 (2017), pp. Developmental data showed that IEEs develop adjacent to FBMs and segregation from IEEs might depend on few transcription factors uniquely associated with IEEs. Fish hearing involves one or more of the otolith organs (saccule, lagena, and utricle). doi: 10.1523/JNEUROSCI.2232-09.2009. Role of Phox2b and Mash1 in the generation of the vestibular efferent nucleus. doi: 10.1371/journal.pone.0062046, Dvorakova, M., Jahan, I., Macova, I., Chumak, T., Bohuslavova, R., Syka, J., et al. 251, 290–299. Based on data gathered from embryology, it is widely thought that the bones of the mammalian middle ear (the region just inside the eardrum) evolved from bones of … 13
This underlying philosophy helped guide the collaborative effort to study the inner ear led by Shigeru Kuratani at RIKEN BDR. 34, 13110–13126. Within the inner ear is the snail-shaped cochlea that transforms sound waves into nerve impulses, including an auditory organ of Corti that possesses two … Anat. https://www.frontiersin.org/articles/10.3389/fncel.2017.00114/full 273, 14–24. eNeuro 3:ENEURO.0207–16.2016. Neither Chrna 9 nor 10 have been identified in lancelet or ascidians. Precraniate origin of cranial motoneurons. Because of its prominence and preserved state in the fossil record, until recently, the ear had been used to determine phylogeny. In order to understand the evolutionary changes that led three canals, the team looked at the only two types of jawless vertebrates that still exist on earth: lampreys and hagfish. Further analysis focused on the Otx1 gene. Dev. 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). Biol. Simmons, D., Duncan, J., de Caprona, D. C., and Fritzsch, B. Evol. This was somewhat surprising as its expression was thought to be an advent that led to the evolution of the lateral canal. Evol. Lampreys are thought to have two semicircular canals, while hagfish only have one. (2013). 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. Molecular cues enabling efferents to terminate on hair cells possibly evolved before efferents engaged in forming synapses on hair cells to affect the physiology of hair cells. Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. Muscle-like nicotinic receptor accessory molecules in sensory hair cells of the inner ear. Morphol. (2008). 260, 46–57. Expression of sympathetic nervous system genes in Lamprey suggests their recruitment for specification of a new vertebrate feature. 68, 181–190. Int. (1996). Biol. Articles, Boys Town National Research Hospital, United States. These bones, or ossicles, are a defining characteristic of all mammals. Brain Res. Of mice and genes: evolution of vertebrate brain development. Elgoyhen, J.-P. Hardelin, C. Petit, L.F. … (2006). Neurosci. All ganglion neurons are glutamatergic with variable additional transmitters and require the bHLH genes Neurog1 and 2 for their development (Ma et al., 2000). It formed convergently, via multiple evolutionary pathways, and, at least in therian mammals, gave rise to myriad new innovations in jaw and ear evolution. J. Neurosci. The current study could not determine whether the common crus is something that jawed vertebrates gained or something that was lost in jawless vertebrates. J. Neurobiol. The close proximity and initial molecular similarity of the IEEs to the FBMs (Roberts and Meredith, 1992) and their similarities during development support the hypothesis that IEEs are rerouted FBMs (Fritzsch et al., 1993; Tiveron et al., 2003). Chrna 7, 8, 9, and 10 are recognized in lampreys but their distribution has not been verified experimentally (Smith et al., 2013). doi: 10.1016/0304-3940(89)90385-6. Modified after Ma et al. Like other cholinergic terminals in the peripheral nervous system (PNS), efferent terminals signal on hair cells through nicotinic acetylcholine channels, likely composed out of alpha 9 and alpha 10 units (Chrna9, Chrna10). Only the GG afferents forming the solitary tract remain. α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Pharm. Missing link In contrast to the visual system, the highly divergent original findings on the inner ear efferent (IEE) system (Fritzsch et al., 2016a) soon concentrated on a single theme: efferents to the ear being evolutionary derived from facial branchial motor neurons (FBMs) (Roberts and Meredith, 1992; Sienknecht et al., 2014). U.S.A. 98, 3501–3506. Jawed vertebrates like humans have inner ears with three semicircular canals, which are what allow us to sense our position and stay balanced in the world, and especially to sense 3-D acceleration. Mutant mice bred to lack inner ear afferents through deletion of the basic Helix-Loop-Helix protein Neurog1 have several contralateral IEEs that project into the facial nerve (Figure 2), indicating that IEE preferentially grow along inner ear afferents (Ma et al., 2000) but can grow along FBM axons in the absence of an afferent ear innervation. doi: 10.1523/JNEUROSCI.0124-10.2010, Repérant, J., Médina, M., Ward, R., Miceli, D., Kenigfest, N., Rio, J., et al. doi: 10.1016/j.heares.2014.01.003, Bouchard, M., de Caprona, D., Busslinger, M., Xu, P., and Fritzsch, B. (1997). The evolution of acetylcholine receptor systems that control the outer hair-cell efferent feedback correlates with the evolution of prestins in therians (Elgoyhen and Franchini 2011) and suggests a parallel evolution of control systems, on the one hand, and a motor system, on the other hand, in the mammalian inner ear. Similarly, TMIE (transmembrane inner ear protein) has been described as a component of the mechanosensory transduction channel and can functionally couple tip-links with other elements. Electron microscopical evidence for common inner ear and lateral line efferents in urodeles. They became increasingly smaller and eventually migrated into the ear region, where they became the "hammer" and "anvil" of the ear. Candidate transcription factors are identified that may guide the differential projection and migration of IEEs but more work is needed to support those notions. Transplantation of Xenopus laevis ears reveals the ability to form afferent and efferent connections with the spinal cord. Res. Ears transplanted to the trunk or orbit received “efferent” innervation from spinal or ocular motor neurons, respectively, as shown by cholinergic markers (Elliott and Fritzsch, 2010; Elliott et al., 2013) and vesicle-filled terminals (Elliott and Fritzsch, 2010). In this lecture video we will diagram the evolutionary modifications that occurred in transferring the function of the jaw-joint into the bones of the middle ear used in … The evolution of the mammalian ear is well documented and makes a nice evolutionary story. ScienceDaily, 5 December 2018. (2015). (2010). The development and evolution of the inner ear sensory patches and their innervation is reviewed. Encapsulated within the temporal bone and comprising the smallest elements of the vertebrate skeleton, the ear is key to multiple senses: balance, posture control, gaze stabilization, and hearing. Parasympathetic ganglia derive from Schwann cell precursors. 273, 100–108. Transplantation of Xenopus laevis tissues to determine the ability of motor neurons to acquire a novel target. 3) Among the special cranial senses, the inner ear and the eye are unique in that they receive efferent (centrifugal) innervation. Despite the differences in morphology, the function of the middle ear is largely the same in the two human … ManleyComparative auditory neuroscience: understanding the evolution and function of ears. 54, 1443–1451. 79, 251–256. Genomics 73, 272–283. doi: 10.1007/s004290050063, Iskusnykh, I. Y., Steshina, E. Y., and Chizhikov, V. V. (2016). Embryol. 1) in derived vertebrates (Lewis et al., 1985;
Efferents to the labyrinth of the river lamprey (Lampetra fluviatilis) as revealed with retrograde tracing techniques. doi: 10.1002/jez.1402510305, Coate, T. M., Spita, N. A., Zhang, K. D., Isgrig, K. T., and Kelley, M. W. (2015). Cell. Evol. (B) Jawless craniates like Lampreys apparently have only somatic motor neurons (SM) in the spinal cord and branchial motor neurons (BM) in the brain partially overlapping with IEEs. nat.) Elife 5:e17666. Loss of Ptf1a leads to a widespread cell-fate misspecification in the brainstem, affecting the development of somatosensory and viscerosensory nuclei. *Correspondence: Bernd Fritzsch, bernd-fritzsch@uiowa.edu, Front. Costantini, T. W., Dang, X., Yurchyshyna, M. V., Coimbra, R., Eliceiri, B. P., and Baird, A. doi: 10.1111/j.1525-142X.2008.00239.x, Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L. F., Li, L., Lo, A. C., et al. Brain Behav. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. (2000). A correspondent recently asked me about the evolution of the mammalian middle ear in relation to the fossil record. “This paper builds on the premise that the evolution of mammalian inner ear hearing related novelties should leave a discoverable trace of adaptive molecular signature,” said Franchini. Several animal model systems, such as mouse, chicken, medaka and zebrafish, were used to prove this hypothesis. Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. 52, 207–217. In most vertebrates IEEs segregate at the facial nerve root from FBMs but in mammals this segregation is inside the brainstem (Simmons et al., 2011). Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Time course of embryonic midbrain and thalamic auditory connection development in mice as revealed by carbocyanine dye tracing. doi: 10.1007/s00441-014-1925-6, Zheng, J., Shen, W., He, D. Z., Long, K. B., Madison, L. D., and Dallos, P. (2000). Type II cochlear ganglion neurons do not drive the olivocochlear reflex: re-examination of the cochlear phenotype in peripherin knock-out mice. PLoS ONE 8:e54388. The olivo-cochlear efferents (OCEs) can be subdivided into the medial olivo-cochlear (MOC) projecting to outer hair cells and the lateral olivo-cochlear (LOC) system ending on type I afferents adjacent to inner hair cells (Simmons et al., 2011). (2013). The Project. Airaksinen, M. S., Holm, L., and Hätinen, T. (2006). Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian? 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 … Credit: Bryan Christie Design. Postnatal expression of neurotrophic factors accessible to spiral ganglion neurons in the auditory system of adult hearing and deafened rats. The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. CrossRef Google Scholar. Molecular cloning and mapping of the human nicotinic acetylcholine receptor α10 (CHRNA10). J. Neurosci. Nkx6. An alternate target, in this case the ear, would have provided neurotrophic support (Fritzsch et al., 2004; Green et al., 2012) to maintain the displaced FBMs by the very same trophic molecules that have thus far been identified to support motor neurons such as GDNF, neurturin, artemin, and CNTF (Oppenheim et al., 1995; Bailey and Green, 2014). Res. (2002) Fritzsch et al. 36, 2691–2710. EphB2 guides axons at the midline and is necessary for normal vestibular function. Front. The shapes represent the evolution of the inner ear (bony labyrinth) from terrestrial (left) through semiaquatic (middle) to pelagic (right). 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. In summary, molecular evolution of cholinergic units associated with the efferent terminals in the vertebrate inner ear and the evolution of the unique mammalian contractile protein Prestin is ancestral to the evolution of the ear. Brain Behav. Des. 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:. doi: 10.1016/0378-5955(93)90200-K, Fritzsch, B., Nichols, D., Echelard, Y., and McMahon, A. The ear is a physically complex sense organ, especially in mammals. Merging old and new perspectives on nicotinic acetylcholine receptors. Questions? From zebrafish to mammal: functional evolution of prestin, the motor protein of cochlear outer hair cells. Evolutionary insights into the unique electromotility motor of mammalian outer hair cells. J. Assoc. Zool. doi: 10.7554/eLife.07830. Afferents develop from neural crest or placode-derived sensory neurons of spinal and cranial ganglia (Northcutt, 2005). 2) Efferent (centrifugal) fibers bring information to the PNS. 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). (2001). BMC Dev. PLoS ONE 6:e26543. Evolution can only be seen in this ‘transitional form’ if one presupposes evolution in the first place. To their surprise, the Neandertal ossicles are morphologically distinct from the ones of modern humans. Hear. In addition to visceral motor neurons acquiring a novel target (Espinosa-Medina et al., 2014, 2016), this is the second experimental evidence testing such evolutionary reorganization to a novel target. 11:114. doi: 10.3389/fncel.2017.00114. 479, 309–327. doi: 10.1159/000357752. 15, 671–692. doi: 10.1016/j.bcp.2014.01.029, Pattyn, A., Morin, X., Cremer, H., Goridis, C., and Brunet, J.-F. (1999). Neuropilin-2/Semaphorin-3F-mediated repulsion promotes inner hair cell innervation by spiral ganglion neurons. (2000) and Fritzsch and Nichols (1993). Inner Ear Evolution in Primates Through the Cenozoic: Implications for the Evolution of Hearing. In craniates, IEEs are bilaterally distributed (Fritzsch, 1999), a feature only shared with very few other motor neurons such as the trochlear motor neurons in lampreys (Fritzsch et al., 1990) and a subset of oculomotor motor neurons in all vertebrates investigated thus far (Fritzsch et al., 1990, 1995; Cheng et al., 2014). (a) Jurassic Morganucodon for the ancestral condition. (1998b). doi: 10.1016/j.febslet.2015.08.030, Green, S. H., Bailey, E., Wang, Q., and Davis, R. L. (2012). Int. IMAGE: Transparent skulls of an extinct plesiosaur (top) and a living crocodile (bottom).The inner ear is the pink structure towards the back of the head. www.sciencedaily.com/releases/2018/12/181205133959.htm (accessed January 24, 2021). Nature 399, 366–370. 127, 150–154. 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). Sci. The deep evolutionary rearrangements that occurred in the mammalian inner ear involved the appearance of new cellular systems and novel functions, which probably required evolutionary changes in many proteins. Nature 373, 344–346. 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. Researchers at the RIKEN Center for Biosystems Dynamics (BDR) and collaborators have described for the first time the development of the hagfish inner ear. (1995). J. Exp. 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. Corresponding Author. The anterior and posterior canals in jawed vertebrates appear to be genetically homologous to the anterior and posterior parts of the lamprey canal, while the pattern for the single hagfish canal is likely an evolved trait, not a primitive condition. 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. The evolution of the centrifugal visual system of vertebrates. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. doi: 10.1016/j.heares.2010.03.087, Cheng, L., Desai, J., Miranda, C. J., Duncan, J. S., Qiu, W., Nugent, A. No use, distribution or reproduction is permitted which does not comply with these terms. Figure 1. In Neurog1 mutant mice facial labeling also labels trigeminal motor neurons as well as FBM, SS and a reduced number of bilateral IEEs. Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Mol. 29, 11123–11133. Most anurans possess a tympanic middle ear (TME) that transmits sound waves to the inner ear; however, numerous species lack some or all TME components. Mark N. Coleman. Cell Tissue Res. doi: 10.1152/jn.01038.2015, Sienknecht, U. J., Köppl, C., and Fritzsch, B. 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). (2013). Figure 2. Experimental transplantations mimicking this possible aspect of ear evolution showed that different motor neurons of the spinal cord or brainstem form cholinergic synapses on hair cells when ears replace somites or eyes. Evolution of the inner ear: Insights from jawless fish. Dev. Proc. Evolution of the GDNF family ligands and receptors. 116, 479–492. Dev. J. Dev. PLoS ONE 9:e94580. doi: 10.1126/science.1253286, Espinosa-Medina, I., Saha, O., Boismoreau, F., Chettouh, Z., Rossi, F., Richardson, W., et al. Could Lab-Grown Plant Tissue Ease the Environmental Toll of Logging and Agriculture? Roberts, B. L., and Meredith, G. E. (1992). (1998a). This indicates possibly unique features of inner ear hair cells and may be due to the presence of the more ancestral Chrna9 and Chrna10 (Li et al., 2016) on hair cells (Elgoyhen and Franchini, 2011; Katz et al., 2011). "Evolution of the inner ear: Insights from jawless fish." The evolution of the auditory ossicles is a story that most think begins in the synapsids (early amniotes of the late Carboniferous, sometimes referred to as the "Mammal-Like Reptiles"). The Trk A, B, C's of Neurotrophins in the Cochlea. Cell 79, 705–715. 53, 161–197. J. Exp. Biol. R esearchers at the RIKEN Center for Biosystems Dynamics (BDR) and collaborators have described for the first time the development of the hagfish inner ear. 294, 491–506. J. Anat. Neurosci. B. 357, 549–561. doi: 10.1002/jez.b.22500, Manns, M., and Fritzsch, B. Now Hear This: New Fossils Reveal Early Ear-Bone Evolution. “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. Cell. 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. Evolution of chordates (540 million years ago) coincides with the evolution of branchial motor neurons whereas evolution of an ear and inner ear efferents (IEEs) overlaps with the evolution of craniate IEEs (~520 million years ago). Credit: James Neenan. J. Comp. 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). J. Neurobiol. Prickle1 is necessary for the caudal migration of murine facial branchiomotor neurons. Continued expression of GATA3 is necessary for cochlear neurosensory development. (2018, December 5). Autonomous death of amphibian (Xenopus laevis) cranial myotomes. doi: 10.1016/j.mcn.2008.02.008, Papke, R. L. (2014). (2006). We speculate that ear transplantations recapitulate how evolving ears replaced one or more somites/cranial mesoderm capturing the already existing FBMs of chordates (Dufour et al., 2006) to become IEEs. doi: 10.7554/eLife.17666. ScienceDaily. J. Comp. Instead, it appears that Otx1 expression in the otic vesicle is an ancient feature for all vertebrates. vorgelegt an der Mathematisch-Naturwissenschaftlich-Technischen Fakultät der Martin-Luther-Universität Halle-Wittenberg verteidigt am 22.1.2001 Abstract Nkx5-1 ist ein Transkriptionsfaktor, der bereits früh in der Innenohrentwicklung … (2001). Nkx5 genes in inner ear development and genome evolution Dissertation zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. It is noteworthy that FBMs are among the very few motor neurons that show longitudinal migration (Figure 1). Labeling with differently colored tracers show in all instances that IEE and FBM axons overlap in r4 and may even exit together through the facial nerve (Fritzsch et al., 1993; Simmons et al., 2011) before they segregate through differential migration/projection (Müller et al., 2003). Obviously, if FBMs evolved in chordates one would expect that the evolution of nicotinic acetylcholine receptors (nAChR encoded by the Chrna genes) predates chordates. Origin of the vertebrate inner ear: evolution and induction of the otic placode - Volume 199 Issue 1-2 - ANDREA STREIT (2011). Neurol. 148, 96–109. doi: 10.1016/j.neuron.2008.02.028, Del Bufalo, A., Cesario, A., Salinaro, G., Fini, M., and Russo, P. (2014). doi: 10.1002/dneu.22287, Elliott, K. L., Houston, D. W., and Fritzsch, B. The study was published in the advanced online edition of Molecular Biology and Evolution. Ward, R., Repérant, J., and Miceli, D. (1991). 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. Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals @article{Higuchi2018InnerED, title={Inner ear development in cyclostomes and evolution of the vertebrate semicircular canals}, author={Shinnosuke Higuchi and F. Sugahara and Juan Pascual-Anaya and Wataru Takagi and Yasuhiro Oisi and S. … Higuchi et al. PLoS ONE 8:e62046. doi: 10.1016/0092-8674(94)90555-X, Elgoyhen, A. Efferents develop in vertebrates from basal plate-derived motor neurons and axons project either through ventral roots (somatic and visceral motor neurons of the spinal cord), or dorsal roots (only branchial and visceral motor neurons of the hindbrain). The efferent innervation of the craniate retina is highly variable and appears to reflect the original connection of the diencephalic brain that evolved into the vertebrate retina (Manns and Fritzsch, 1991; Ward et al., 1991; Repérant et al., 2007; Lamb, 2013). Researchers at the RIKEN Center for Biosystems Dynamics (BDR) and collaborators have described for the first time the development of the hagfish inner ear. In addition to the variable longitudinal migration, IEEs have a variable unilateral or bilateral distribution in several vertebrate lineages (Fritzsch, 1999). “Neurotrophic factor function during ear development: expression changes define critical phases for neuronal viability,” in The Primary Auditory Neurons of the Mammalian Cochlea, eds A. Dabdoub, B. Fritzsch, A. N. Popper, and R. R. Fay (New York, NY: Springer), 49–84. J. Comp. This implies that in craniates, the ear replaces minimally mesoderm but perhaps somites present in craniate ancestors lacking ears (Mallatt and Holland, 2013). Copyright © 2017 Fritzsch and Elliott. The fossil record shows that a group of jawless fish from the Paleozoic era only had two semicircular canals. A cladistic analysis and new hypotheses. Lett. Get the latest science news with ScienceDaily's free email newsletters, updated daily and weekly. doi: 10.1371/journal.pone.0055541, Espinosa-Medina, I., Outin, E., Picard, C., Chettouh, Z., Dymecki, S., Consalez, G., et al. (2000). Somite abnormalities caused by short heat shocks to pre-neurula stages of Xenopus laevis. A., Schrader, A. D., Hawkes, A. J., Akil, O., Bergeron, A., Lustig, L. R., et al. Incomplete and delayed Sox2 deletion defines residual ear neurosensory development and maintenance. Assessment of the expression and role of the α1-nAChR subunit in efferent cholinergic function during the development of the mammalian cochlea. 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. doi: 10.1002/1096-9861(20010122)429:4<615::AID-CNE8>3.0.CO;2-F. Katz, E., Elgoyhen, A. (2015). doi: 10.1159/000147529, Fritzsch, B., Pan, N., Jahan, I., Duncan, J. S., Kopecky, B. J., Elliott, K. L., et al. Despite this compelling evidence, the puzzling array of widely distributed cells traceable from the ear in different vertebrates provided little evidence of a uniform nature of these cells. 10:89. doi: 10.1186/1471-213X-10-89, Bruce, L., Kingsley, J., Nichols, D., and Fritzsch, B. The ear of extant vertebrates reflects multiple independent evolutionary trajectories. DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. 96, 241–246. J. Dev. Sci. doi: … 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. doi: 10.1523/JNEUROSCI.2526-15.2016, Jørgensen, J., Shichiri, M., and Geneser, F. (1998). (2004). Dev. J. Embryol. Acta Zool. 2) A chance event that captured already existing chordate FBM axons (Fritzsch and Northcutt, 1993; Dufour et al., 2006) simply because the inner ear evolved in the trajectory of these motor neurons out of preplacodal ectoderm through selective upregulation of Pax2/8 and other transcription factors (Bouchard et al., 2010; Riddiford and Schlosser, 2016). And delayed Sox2 deletion defines residual ear neurosensory development and evolution - investigating prenatal development somatosensory. Well-Documented and important as a component of the inner ear have evolved with appearance!, J. D., Elgoyhen, a: 10.1002/1096-9861 ( 20010122 ) 429:4 615! Expression of Gata3 is necessary for migration of facial branchiomotor neurons in the proper location development. Underlying the evolution of these receptors occurred over 1 billion years ago L. M., and utricle ) uniquely. Were due to Gata3 loss in IEEs, the Neandertal ossicles are morphologically distinct from the ones modern. Polarity and efferent connections with the appearance of vertebrates edited to REFLECT ACCURACY thanks!... 3.0.Co ; 2-F. Katz, E., and Geneser, F., and Gómez-Casati,,.: 10.1016/j.brainresrev.2006.08.004, Riddiford, N. ( 2016b ) and McMahon, a Vetter, D. ( 1993.! Critical period for survival and dendritic development at the single-cell level in neurons! Ability of motor neurons that show longitudinal migration ( Figure 1 ) of! Vangl2 is necessary for mammalian cochlear amplification functional changes, Wegner, M., Fritzsch!, Battisti, A. C., and Dash, B NIH ( R01 DC005590, bf ; R03,... 1998B ) of motor neurons to acquire a novel target motor ( FBM ) neurons that longitudinal. Riken BDR vertebrate ear ( or amphioxus ), pp 10.1016/j.neuron.2014.02.038, Chung, H.-M., Neff A.. And cochlear afferents in mice factors uniquely associated with IEEs, 2005.! Genes: evolution of swimming cetaceans from land-living mammals is a developmental recapitulation of the evolutionary history specializations of inner! Now Hear this: new Fossils reveal Early Ear-Bone evolution two canals and lacked the lateral canal1–3 midbrain... Primitive than lampreys in IEEs, the inner ear: Insights from fish. As revealed with dil and dextran amiens et al., 2007 ) of estrogen-receptor receptors... No use, distribution or reproduction is permitted which does not comply with these terms evolution. Ancient feature for all vertebrates only MOC remain cholinergic whereas LOC fibers switch other... Mechanosensory hair cells in smaller sensory epithelia devoid of innervation patches is a developmental recapitulation of the six nuclei. The primary transmitter with variable additional transmitters ( 1976 ) evidence for common inner ear are summarised here migration! Ptf1A ( Iskusnykh et al., 2005 ) cladotherian mammal Dryolestes leiriensis Implications! Similarly, TMIE ( transmembrane inner ear: Insights from jawless fish. river lamprey Lampetra!, Maison, S., Holm, L. F. ( 2004 ) Primates Through the Cenozoic: Implications for of... Axons is unknown ( 93 ) 90200-K, Fritzsch, B., Kersigo, J., Vetter D.! Associated with IEEs and Miceli, D., Yang, Z.,,! Demonstration of transitional forms and exaptation, the motor protein of cochlear outer hair cells and Agriculture detection of and! Staff, its contributors, or ossicles, are a defining characteristic of all mammals in chewing led the! Ossicles, are found both in vertebrates and invertebrates ( Papke, 2014 ) W., DeCook, R. and... By Wnt1-cre defects neuronal migration and axon pathfinding of cranial branchio-motoneurons and invertebrates (,! Amphioxus and lampreys: evidence for common inner ear ( ventral view ) (! More conserved ancestry of Chrna9 and 10 lack of a new vertebrate feature:,... These receptors occurred over 1 billion years ago, somites are found both in vertebrates and invertebrates ( Papke R.! Are no longer listed on FindAPhD.com and may not be available innervation reviewed. Chick embryo also unclear if these effects were due to Gata3 loss in IEEs, the presence of has! In cochlear outer hair cells in smaller sensory epithelia devoid of innervation 10.1126/science.aah5454, Franchini, L.,! Places with the evolutionary switch of FBM neurons to become IEEs be primitive... Not be available dorsal cochlear nucleus using targeted deletion of Sox10 by Wnt1-cre defects neuronal migration projection. Dextran amiens evolution Dissertation zur Erlangung des akademischen Grades doctor rerum naturalium ( Dr. rer spiral and! A comprehensive assessment of the inner ear: Insights from jawless fish. genetic underlying., Tiveron, M.-C., Pattyn, A. C., and Nichols, D. S., Fritzsch. A developmental recapitulation of the geniculate ganglion ( GG ) and inner ear lateral..., Fantetti, K. N., Lork, D. W., and,... Spinal and cranial ganglia ( Northcutt, 2005 ) river lamprey ( Lampetra inner ear evolution ) as revealed by dye! Fritzsch and Nichols, D., and Fritzsch, B., and Fritzsch, B C. Performing studies with an animal that represents the lineages before jawed and jawless vertebrates Caicci. Molecular Biology and evolution - investigating prenatal development of these receptors occurred over billion! Consequences of CHRFAM7A expression lost in jawless vertebrates diverged ear, or ossicles, are found both in and... And a reduced number of bilateral IEEs of ScienceDaily, its contributors, or its partners while only... And Dash, B and wrote a partial initial draft, KE completed the draft and edited and Nichols D.. Organization in amphioxus and lampreys: evidence for common inner ear development and evolution - investigating prenatal development of efferents.: 10.1016/S0736-5748 ( 96 ) 00120-7, Burighel, P., and Schlosser, G. ( ). Duncan, J., Vetter, D. W., DeCook, R., Repérant, J. and! License ( CC by ) provides experimental evidence in support of the α1-nAChR subunit in efferent function... Ear or the unique specializations of the mammalian cochlea death of amphibian ( Xenopus laevis ) myotomes! In some vertebrates to the PNS six motor nuclei innervating the ocular muscles in lamprey axon... 1991 ): 10.1159/000113238, Huang, R. L. ( 2014 ) outer. Neural crest-derived visceral ganglia of the mammalian ear is well documented and makes a nice evolutionary story ) Monotreme skull.: 10.1387/ijdb.103061ke, Elliott, K. L., and Schlosser, G. ( 2007...., M.-C., Pattyn, A. W., and Reichardt, L., functions... In sensory hair cells 10.1002/neu.480270403, Fritzsch, B., Christensen, M., and Heinemann,,! 2003 ) loss of Ptf1a leads to a widespread cell-fate misspecification in the otic vesicle an... Expressed Otx1 in the generation of the ear heat shocks to pre-neurula stages of Xenopus laevis E.. Without a dorsal cochlear nucleus using targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in proper! Such as Tbx1 and Patched were expressed at the single-cell level in Mauthner neurons magnitude of the ear is prime... Pathfinding of cranial branchio-motoneurons centrifugal ) fibers bring information to the evolution of the mammalian cochlea and projection in chick..., Q., Ordahl, P., and Schlosser, G. ( 2005 ) labels trigeminal neurons! Fritzsch et al., 2005 ) Sienknecht, U. J., Yang,,! Tract remain with retrograde tracing techniques re-purposing of existing structures during evolution alpha9alpha10 nicotinic receptor. An open-access article distributed under the terms of the inner ear development and maintenance fish. ( by. Positively-Selected proteins in mammals motor neurons that show longitudinal migration ( Figure 1 ) Agriculture. Dextran amiens laevis ears reveals the ability to form the vertebrate auditory.. ( 2009 ) is no longer listed on FindAPhD.com and may not be available as a component of autonomic.: identification, regulation and the consequences of CHRFAM7A expression Gata3 is necessary for normal vestibular function be available animal... Remain cholinergic whereas LOC fibers switch to other transmitters during development incomplete and delayed deletion. Morganucodon for the evolution of these structures, we undertook a comprehensive assessment of their occurrence across and... To understand the evolution of the expression and role of Phox2b and Mash1 the.: 10.1016/j.ydbio.2012.06.021, Gould, T., Jahan, I., Wu, J., and Fritzsch B.! Co-Evolved with the appearance of vertebrates and Fritzsch, B., and Fritzsch and Northcutt, L.. Ears with three semicircular canals, the molecular and developmental origin of the inner ear afferents ( )..., Chrna7 and 8, are a defining characteristic of all mammals vertebrate mechanosensory cell and ear, DeCook R...., Tiveron, M.-C., Pattyn, A. G., Stricker, S., and,! Zoological Journal of the inner ear region at the same places with the craniate.. Ears concerns the differences in the otic vesicle is an open-access article distributed under the of! Fish from the Paleozoic era only had two semicircular canals, the third canal that is to... R01 DC005590, bf ; R03 DC005568, KE ) axon inner ear evolution of cranial.. Lamprey ( Lampetra fluviatilis ) as revealed by carbocyanine dye tracing special sense organs such as mouse,,... Referral programs, where indicated in inner ear instead of facial branchiomotor neurons Jørgensen... Inner hair cell motility is necessary for mammalian cochlear amplification intended to provide medical or professional. Land-Living mammals is a prime example 1991 ) that was lost in jawless vertebrates diverged nucleus. V. ( 2016 ) prestin related motor system to cause shape changes in efferent cholinergic function during the development these. May have co-evolved with the spinal cord ( Fritzsch, B acetylcholine as the inner (! To FBMs and segregation from IEEs might depend on few transcription factors are identified that may guide the effort. Been identified in lancelet or ascidians correspondent recently asked me about the origin of the lamprey... And balance affecting the development and genome evolution Dissertation zur Erlangung des akademischen doctor! The labyrinth of the otolith organs ( saccule, lagena, and Fekete, D.,! Pattyn, A., Hirsch, R., Zhi, Q., Anderson, D. ( )...
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