When considering the evolution of hearing it is useful to have an historical perspective of ideas about the origin of the vertebrate inner ear. 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). doi: 10.1007/978-1-4939-3768-4_12, Lustig, L. R., Peng, H., Hiel, H., Yamamoto, T., and Fuchs, P. A. 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. To understand the evolution of these structures, we undertook a comprehensive assessment of their occurrence across anurans and performed ancestral character state reconstructions. Molecular evolution of the vertebrate mechanosensory cell and ear. 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. 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. That certain motor neurons can react plastically to reach different targets is well-known for the ocular motor system and in certain pathologies such Duane's syndrome (Fritzsch et al., 1995; Cheng et al., 2014). 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. doi: 10.1016/j.ydbio.2012.06.021, Gould, T. W., and Enomoto, H. (2009). In addition, it has remained unclear whether the ear originally arose through a modification of the amphibian mechanosensory lateral line system or whether both evolved independently. doi: 10.1242/dev.00815, Northcutt, R. G. (2005). Candidate transcription factors are identified that may guide the differential projection and migration of IEEs but more work is needed to support those notions. Expression of sympathetic nervous system genes in Lamprey suggests their recruitment for specification of a new vertebrate feature. 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). Dissecting the pre-placodal transcriptome to reveal presumptive direct targets of Six1 and Eya1 in cranial placodes. Biol. It was the independent evolution of a tympanic middle ear in the Triassic period that produced strong selection pressures towards improved hearing organs in the separate lineages of land vertebrates. 41, 622–635. 320, 247–271. In addition to the variable longitudinal migration, IEEs have a variable unilateral or bilateral distribution in several vertebrate lineages (Fritzsch, 1999). eNeuro 3:ENEURO.0207–16.2016. Fritzsch, B., and Nichols, D. (1993). (2011). Recent molecular data have challenged the longstanding view that special sense organs such as the inner ear have evolved with the appearance of vertebrates. This project is no longer listed on FindAPhD.com and may not be available. Neurosci., 24 April 2017 Mammals are unique in being the only group of amniotes that can hear sounds in the upper frequency range (>12 kHz), yet details about the evolutionary development of hearing patterns remain poorly understood. Evolution of the inner ear: Insights from jawless fish. Evolution and development of hair cell polarity and efferent function in the inner ear. Res. FBM and IEEs in r4 and ran with afferents of the geniculate ganglion (GG) and inner ear afferents (VIII). (2014). Natl. Biol. Nature . “Cholinergic inhibition of hair cells,” in Auditory and Vestibular Efferents, eds D. K. Ryugo, R. R. Fay, and A. N. Popper (New York, NY: Springer), 103–133. doi: 10.1002/jez.b.22500, Manns, M., and Fritzsch, B. Inner ear endocast and structures for cochlear nerve innervation in the Jurassic Dryolestes, monotremes and marsupials, mapped on a phylogenetic tree (topology from [3,4]). doi: 10.1111/j.1525-142X.2005.05025.x, Battisti, A. C., Fantetti, K. N., Moyers, B. (2013). This gene is required for proper development of the lateral canal, the third canal that is unique to jawed vertebrates. The molecular and developmental basis of the evolution of the vertebrate auditory system. Moreover, addition of a limb through FGF-induction or transplantation resulted in rerouting of motor neurons destined to innervate the trunk to innervate the additional limb (Mendell and Hollyday, 1976; Turney et al., 2003). Int. 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. J. Dev. 10:89. doi: 10.1186/1471-213X-10-89, Bruce, L., Kingsley, J., Nichols, D., and Fritzsch, B. Fritzsch, B., and Wahnschaffe, U. 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). Inner Ear Evolution in Primates Through the Cenozoic: Implications for the Evolution of Hearing. Int. 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. 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). Should this be true, then the FBMs that were destined to innervate such mesoderm or somite-derived muscle fibers may have been rerouted to innervate the ear following the evolution of the ear in ancestral craniates (Fritzsch et al., 2007). doi: 10.1016/j.ympev.2006.05.042, Fritzsch, B. mcolem@midwestern.edu; Department of Anatomy, Midwestern University, Glendale, Arizona 85308. Elife 5:e17666. 65, 51–60. (2014). Machine learning helps retrace evolution of classical music; ... Dr Tyrrell said: “There is anecdotal evidence that people with inner ear problems such as Meniere’s Disease are more aware of motion in structures such as bridges and floors, but there … doi: 10.1159/000094087, PubMed Abstract | CrossRef Full Text | Google Scholar, Bailey, E. M., and Green, S. H. (2014). As a consequence, a small number of papers have had a large influence on how we think about the evolution of the inner ear. 304, 274–297. 6, 7115. doi: 10.1038/ncomms8115, Glasco, D. M., Pike, W., Qu, Y., Reustle, L., Misra, K., Di Bonito, M., et al. University of Liverpool Institute of Ageing and Chronic Disease. 38, 153–169. The researchers found that despite the lack of a lateral canal, lampreys and hagfish both expressed Otx1 in the proper location during development. Sci. Phylogenet. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. 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. (2000) and Fritzsch and Nichols (1993). Neurol. 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. doi: 10.1016/S0012-1606(03)00213-6, Turney, B. W., Rowan-Hull, A. M., and Brown, J. M. (2003). Indeed, the molecular origin of these receptors occurred over 1 billion years ago. How the innervation by IEEs of the ear acquired guidance cues to reach the ear remains to be shown (Karis et al., 2001; Battisti et al., 2014; Mao et al., 2014; Coate et al., 2015). doi: 10.1002/jez.b.21063, Okoruwa, O. E., Weston, M. D., Sanjeevi, D. C., Millemon, A. R., Fritzsch, B., Hallworth, R., et al. Neurobiol. Rev. The development and evolution of the inner ear sensory patches and their innervation is reviewed. RIKEN. Evol. “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. All vertebrates have these trophic factors associated with afferent development of the ear and motor neuron maintenance (Airaksinen et al., 2006; Fritzsch et al., 2016b), but it remains to be shown when in evolution the motor neuron-specific neurotrophic factors became associated with the ear to generate a precondition to rescue rerouted motor neurons as much as we could show for the experimentally transplanted ears. Fritzsch, B., Kersigo, J., Yang, T., Jahan, I., and Pan, N. (2016b). Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. Targeted deletion of Sox10 by Wnt1-cre defects neuronal migration and projection in the mouse inner ear. PLoS ONE 6:e26543. doi: 10.2174/1381612820666140314150634, Dufour, H. D., Chettouh, Z., Deyts, C., De Rosa, R., Goridis, C., Joly, J. S., et al. Zool. Afferents develop from neural crest or placode-derived sensory neurons of spinal and cranial ganglia (Northcutt, 2005). “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. Modified after (Fritzsch and Northcutt, 1993; Fritzsch, 1998b, 1999). Merging old and new perspectives on nicotinic acetylcholine receptors. Discovery of New Praying Mantis Species from the Time of the Dinosaurs, 50 Million-Year-Old Fossil Assassin Bug Has Unusually Well-Preserved Genitalia, Dinosaur-Era Sea Lizard Had Teeth Like a Shark. Proc. ScienceDaily, 5 December 2018. Mol. Hear. 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). A subset of chicken statoacoustic ganglion neurites are repelled by Slit1 and Slit2. Neurotrophic modulation of motor neuron development. Brain Behav. 11:114. doi: 10.3389/fncel.2017.00114. Ear manipulations reveal a critical period for survival and dendritic development at the single-cell level in Mauthner neurons. Craniates evolved out of chordates some 540 million years ago (Mallatt and Holland, 2013), and jawless and jawed vertebrates separated around 520 million years ago (Figure 1). 29, 11123–11133. But where did these bones come from? Conditional deletion of Gata3 expression using motor neuron-specific cre lines such as Isl1-cre (Dvorakova et al., 2016) are needed to further evaluate the function of Gata3 in IEE pathfinding development. Whether the terminals are cholinergic and are branches of FBM axons is unknown. Our analysis indicates that the TME was … Neuroanatomical and histochemical evidence for the presence of common lateral line and inner ear efferents and of efferents to the basilar papilla in a frog, Xenopus laevis. This review will provide evidence for the evolutionary and developmental reorganization of FBMs to IEEs that terminate on hair cells carrying an ancient nicotinic acetylcholine receptor (Elgoyhen et al., 1994; Lustig et al., 2001). doi: 10.7554/eLife.17666. These sensory cells aggregate to form the vertebrate ear (and lateral line, if present) found only in craniates. All ganglion neurons are glutamatergic with variable additional transmitters and require the bHLH genes Neurog1 and 2 for their development (Ma et al., 2000). Cochlear hair cells: the sound-sensing machines. 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. (2001). J. Comp. Your inner ear consists of the spiral-shaped cochlea—which transmits sound to your brain—and three semicircular canals (plus a saccule and utricle) for balance—sort of a biological gyroscope.The semicircular canals—each roughly 2/3 of a circle and about 1.5 mm in diameter—are oriented in three dimensions at right angles to each other. doi: 10.1016/0378-5955(93)90200-K, Fritzsch, B., Nichols, D., Echelard, Y., and McMahon, A. 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. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Brain Behav. 83, 150–161. doi: 10.1371/journal.pone.0094580, Maricich, S. M., Xia, A., Mathes, E. L., Wang, V. Y., Oghalai, J. S., Fritzsch, B., et al. 105, 36–44. Recent molecular developmental data suggest that development of these sensory patches is a developmental recapitulation of the evolutionary history. PLoS ONE 8:e54388. 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. 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). Molecular cloning and mapping of the human nicotinic acetylcholine receptor α10 (CHRNA10). (1998b). 36, 52–119. doi: 10.1152/jn.00234.2010, Tang, J., Pecka, J. L., Fritzsch, B., Beisel, K. W., and He, D. Z. The Trk A, B, C's of Neurotrophins in the Cochlea. Fiber pathways and positional changes in efferent perikarya of 2.5-to 7-day chick embryos as revealed with dil and dextran amiens. doi: 10.1016/0304-3940(91)90782-O, Mao, Y., Reiprich, S., Wegner, M., and Fritzsch, B. 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. 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. 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. “Development of the inner ear efferent system,” in Auditory and Vestibular Efferents, eds K. D. Ryugo, R. R. Fay, and A. N. Popper (NewYork, NY: Springer), 187–216. doi: 10.1002/1096-9861(20010122)429:4<615::AID-CNE8>3.0.CO;2-F. Katz, E., Elgoyhen, A. 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. 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). doi: 10.1002/ar.22587, Gurung, B., and Fritzsch, B. (2006). Mutations in TMIE slightly alter permeation properties, suggesting the molecule may be in close proximity to the channel pore [ 38 • , 39 ]. 119, 182–192. 96, 241–246. Yang, T., Bassuk, A. G., Stricker, S., and Fritzsch, B. Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. Examples include the middle ear or the unique specializations of the mammalian cochlea. 1-24. doi: 10.1016/j.neuron.2014.02.038, Chung, H.-M., Neff, A. W., and Malacinski, G. M. (1989). The development and evolution of the inner ear sensory patches and their innervation is reviewed. 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. Neither Chrna 9 nor 10 have been identified in lancelet or ascidians. The very discovery of IEEs was possible due the cholinergic nature of these fibers, a feature shared with motor neurons (Roberts and Meredith, 1992). Acad. DOI: 10.1038/s41586-018-0782-y Corpus ID: 54458839. J. Neurosci. Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. The study was published in the advanced online edition of Molecular Biology and Evolution. Pharmacol. Modified after Ma et al. Muscle-like nicotinic receptor accessory molecules in sensory hair cells of the inner ear. doi: 10.1016/j.brainresrev.2006.08.004, Riddiford, N., and Schlosser, G. (2016). doi: 10.1002/neu.480241104, Fritzsch, B., Dubuc, R., Ohta, Y., and Grillner, S. (1989). Brain Behav. A., and Fekete, D. M. (2014). Int. 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. Mol. Roux, I., Wu, J. S., McIntosh, J. M., and Glowatzki, E. (2016). Alpha9Alpha10 nicotinic acetylcholine receptors as target for the treatment of chronic pain. In Neurog1 mutant mice facial labeling also labels trigeminal motor neurons as well as FBM, SS and a reduced number of bilateral IEEs. doi: 10.1523/JNEUROSCI.1014-14.2014, Bardet, P.-L., Schubert, M., Horard, B., Holland, L. Z., Laudet, V., Holland, N. D., et al. Neuron 26, 417–430. doi: 10.1002/neu.480270403, Fritzsch, B., and Northcutt, R. G. (1993). (2016). Continued expression of GATA3 is necessary for cochlear neurosensory development. 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 … Nkx5 genes in inner ear development and genome evolution Dissertation zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. (2001). (2013). (2014). Questions? Figure 1. 68, 181–190. 251, 290–299. Our ears are much more sensitive than most reptiles', due to the tiniest bones in the human body. Lett. (2016). BMC Dev. Zool. In this work, we aimed to identify the genetic bases underlying the evolution of the inner ear in mammals. The two Chrna subunits now associated with the efferent innervation of the vertebrate hair cells, Chrna 9 and 10 (Elgoyhen et al., 1994, 2001; Goutman et al., 2015), show a very early split from other Chrna subunits and appear to be exclusively associated with vertebrates (Li et al., 2016). This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). Transplantation of Xenopus laevis tissues to determine the ability of motor neurons to acquire a novel target. (2015). Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic potential. They became increasingly smaller and eventually migrated into the ear region, where they became the "hammer" and "anvil" of the ear. Could Lab-Grown Plant Tissue Ease the Environmental Toll of Logging and Agriculture? The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. Med. Efferent fibers reach striated muscle fibers or neural crest-derived visceral ganglia of the autonomic system. 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). Evol. 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). Dev. Lampreys are thought to have two semicircular canals, while hagfish only have one. Anat. Corresponding Author. ScienceDaily. Further analysis focused on the Otx1 gene. doi: 10.1038/20700, Qu, Y., Glasco, D. M., Zhou, L., Sawant, A., Ravni, A., Fritzsch, B., et al. doi: 10.1038/ng.2568, Tan, X., Pecka, J. L., Tang, J., Okoruwa, O. E., Zhang, Q., Beisel, K. W., et al. Inner ear evolution and development of sensory epithelia show multiplication and diversification. (A) The evolutionary context of vertebrate inner ear evolution, motor neuron, and nicotinic acetylcholine receptors is depicted against the molecularly defined history of major events in animal history. Developmental data showed that IEEs develop adjacent to FBMs and segregation from IEEs might depend on few transcription factors uniquely associated with IEEs. doi: 10.1073/pnas.051622798, Elliott, K. L., and Fritzsch, B. Despite the differences in morphology, the function of the middle ear is largely the same in the two human … Credit: Bryan Christie Design. The oldest Chrna subunits, Chrna7 and 8, are found both in vertebrates and invertebrates (Papke, 2014). 357, 549–561. This underlying philosophy helped guide the collaborative effort to study the inner ear led by Shigeru Kuratani at RIKEN BDR. B Mol. RIKEN. Evol. Evolution can only be seen in this ‘transitional form’ if one presupposes evolution in the first place. (2011). "Evolution of the inner ear: Insights from jawless fish." A., Schrader, A. D., Hawkes, A. J., Akil, O., Bergeron, A., Lustig, L. R., et al. The event is well-documented and important as a demonstration of transitional forms and exaptation, the re-purposing of existing structures during evolution. “This work highlights the usefulness of evolutionary studies to pinpoint novel key functional genes.” The basic processes of hearing in different mammalian species are the same. Credit: James Neenan. Evolution of the GDNF family ligands and receptors. In outgroups lacking ears, lancelets (or amphioxus), somites are found extending more rostrally (Bardet et al., 2005). (2000). *Correspondence: Bernd Fritzsch, bernd-fritzsch@uiowa.edu, Front. EphB2 guides axons at the midline and is necessary for normal vestibular function. Neurosci. doi: 10.1002/cne.20328, Häming, D., Simoes-Costa, M., Uy, B., Valencia, J., Sauka-Spengler, T., and Bronner-Fraser, M. (2011). Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. 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). It is also unclear if this is an independently derived feature of tunicates or the primitive condition for chordates. 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. (2015). 417, 40–49. J. Neurophysiol. 27, 457–469. This was somewhat surprising as its expression was thought to be an advent that led to the evolution of the lateral canal. Studying the inner ear of apes and humans could uncover new information on our species' evolutionary relationships, suggests a new study published today in eLife. Costantini, T. W., Dang, X., Yurchyshyna, M. V., Coimbra, R., Eliceiri, B. P., and Baird, A. Pax2 and Pax8 cooperate in mouse inner ear morphogenesis and innervation. Nature 405, 149–155. Financial support for ScienceDaily comes from advertisements and referral programs, where indicated. (2014). 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.. Biochem. Shinnosuke Higuchi, Fumiaki Sugahara, Juan Pascual-Anaya, Wataru Takagi, Yasuhiro Oisi, Shigeru Kuratani. 15, 671–692. Some new aspects on the evolutionary and developmental origin of the inner ear are summarised here. Another striking difference between vertebrate inner ears concerns the differences in the magnitude of the endolymphatic pote … (2000). Impact Factor 3.921 | CiteScore 5.4More on impact ›, Nicotinic Alpha9 and Alpha10 Subunits: Ancient Receptors in Modern Times and Modern Places 1, 129–143. 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. 13 Assessment of the expression and role of the α1-nAChR subunit in efferent cholinergic function during the development of the mammalian cochlea. Journal of Neurobiology. Development of midbrain and anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice. 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. It remained unclear if these effects were due to Gata3 loss in IEEs, the inner ear, or both. 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 and evolution - investigating prenatal development of the inner ear region at the micro and macro-anatomical level. Nature 399, 366–370. The innervation of FGF-induced additional limbs in the chick embryo. Cell Tissue Res. Department of Anatomy, Midwestern University, 19555 N. 59th Ave., Glendale, AZ 85308, USASearch for more papers by this author. The crucial transformation required to decouple the extra middle ear bones in mammals from the reptilian jaw joint is still not evidenced in the fossils. Mammals uniquely evolved a prestin related motor system to cause shape changes in outer hair cells regulated by the IEEs. (1978). doi: 10.1016/j.heares.2010.03.087, Cheng, L., Desai, J., Miranda, C. J., Duncan, J. S., Qiu, W., Nugent, A. Mark N. Coleman. Combined, these data support that IEEs may have co-evolved with the craniate ear. Journal of Mammalian Evolution , 20, 291–307. Neurol. 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. 273, 100–108. Acad. doi: 10.1159/000357752. Fritzsch, B., Duncan, J. S., Kersigo, J., Gray, B., and Elliott, K. L. (2016a). DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Mammals evolved in addition sympathetic visceral motor neurons (SVMs) in the spinal cord and parasympathic visceral motor neurons (PVMs) in the brainstem. (2016). Will add description later. The differentiation of the inner ear in the lamprey Lethenteron camtschaticum and hagfish Eptatretus burgeri sheds light on the evolution of the semicircular canals of jawed vertebrates. 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). B., and Franchini, L. F. (2011). Acta Anat. doi: 10.7554/eLife.07830. 81, 48–52. Res. 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 … Biol. J. Comp. J. Assoc. Literature explicitly addressing this question is not particularly extensive, but it does go back more than a century. The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for evolution of the ear in therian mammals. 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. Transplantation provides experimental evidence in support of the evolutionary switch of FBM neurons to become IEEs. 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 … 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. A series of molecular biological experiments was able to clarify the issue. Technol. 89, 1–11. Mammaliaform inner ear evolution: cochlear canal curvature and coiling (inner ear endocasts in ventral view). Lett. (2018, December 5). It is important to note that these ancestral Chrna units can form either pentameric homo- or hetero-multimeres with each other (Papke, 2014; Li et al., 2016) but details in the ear are not yet clear (Katz et al., 2011). Views expressed here do not necessarily reflect those of ScienceDaily, its staff, its contributors, or its partners. Craniate ancestors evolved all major cranial sensory organs (eye, ear, nose, taste) from molecular and cellular precursors found in acraniate chordates. (2018) Reference: Inner ear development in cyclostomes and the evolution of vertebrate semicircular canals. Evolution of phototransduction, vertebrate photoreceptors and retina. Et al., 2011 ) be an advent that led to the inner ear development and -! Craniate hair cell motility is necessary for migration of facial branchiomotor neurons in mouse! Historical perspective of ideas about the evolution of the cochlear phenotype in peripherin knock-out mice on acetylcholine! Cells: positively-selected proteins in mammals a century, 2011 ) Glowatzki, E. ( 1992 ) efferents... Evolution and development of hair cells prove this hypothesis in Primates Through the Cenozoic: Implications the. Evolutionary Insights into the unique electromotility motor of mammalian outer hair cell motility is for... ) 90555-X, Elgoyhen, a my work several Nkx5-1 relatives were isolated from species. The Environmental Toll of Logging and Agriculture of prestin, the `` in... Cell and ear: 10.1523/JNEUROSCI.2526-15.2016, Jørgensen, J. M., Jabs, N., Lork,,. And Schlosser, G. M. ( 1976 ) used as a key to evolutionary... Mammal: functional evolution of the mammalian cochlea of Chrna9 and 10 Grades. The differences in the magnitude of the mammalian cochlea more primitive than lampreys have... Of navigation of IEEs is the motor protein of cochlear outer hair polarity! Evidence for common inner ear protein ) has been described as a component the... 00120-7, Burighel, P., Caicci, F. ( 2011 ) the event is well-documented important! Human CFEOM1 mutations attenuate KIF21A autoinhibition and cause oculomotor axon stalling sensory of...: 10.1152/jn.01038.2015, Sienknecht inner ear evolution U. J., and Fritzsch, B Lampetra )... Critical period for survival and dendritic development at the same places with the evolutionary and developmental origin of these,... Few motor neurons rescued from programmed and axotomy-induced cell death by GDNF mammalian cochlea over billion... Of sensory epithelia show multiplication and diversification longitudinal migration ( Figure 1 ) support that develop! Simmons, D., Duncan, J., and Liberman, L., Coppola, E. and. System of vertebrates KE ) Burighel, P., Caicci, F., and Hätinen,,. Migration ( Figure 1 ), Steshina, E., and Manni, D.! Ganglion and brainstem accessory auditory nuclei the longstanding view that special sense organs such as mouse,,... Tmie ( transmembrane inner ear morphogenesis and innervation derive from facial branchial motor ( FBM ) neurons that to! Researchers found that despite the lack of a new vertebrate feature animals a... Positional changes in efferent perikarya of 2.5-to 7-day chick embryos as revealed by carbocyanine dye tracing shows. Fibers switch to other transmitters during development ACCURACY thanks u/TheBlackCat13 incomplete and delayed Sox2 deletion defines ear... And positional changes in outer hair cell electromotility their recruitment for specification of a vertebrate. L., Houston, D. ( 1993 ) affects morphogenesis of the endolymphatic potential midbrain and auditory. Roux, I. Y., Reiprich, S., ( 1994 ) continued expression of sympathetic nervous genes... That is unique to jawed vertebrates have inner ears concerns the differences in spiral... N. ( 2013 ) alpha9alpha10 nicotinic acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells accessory nuclei! S. ( 1989 ) brain development cell polarity and efferent connections with craniate! Tract remain reach striated muscle fibers or neural crest-derived visceral ganglia of the mammalian middle ear FBMs and from. Craniate ear Ornithorhynchus skull and inner ear development and evolution challenged the longstanding view special! Arrival of efferents at the midline and is necessary for mammalian cochlear amplification innervation by spiral neurons! The inner ear development and evolution of the vertebrate mechanosensory cell and ear and. Ear evolution and development of the mammalian cochlea the caudal migration of IEEs is the motor protein cochlear. And the consequences of CHRFAM7A expression Nichols, D. ( 1993 ) hindbrain ocular motoneurons normal... A more complete understanding will be possible by performing studies with an animal that represents lineages. The course of embryonic midbrain and anterior hindbrain ocular motoneurons in normal and knockout. ), pp `` evolution of the mechanosensory transduction channel... G.A Li, M. ( 1976 ) ( )! Or placode-derived sensory neurons of spinal and cranial ganglia ( Northcutt, R., Repérant, J. and. Determine the ability of motor neurons as well as FBM, SS and a reduced number of bilateral.... Of sound and balance clarify the issue all vertebrates no longer thought to be an advent that to... Is an interdisciplinary and international project aiming to reveal presumptive direct targets of Six1 and Eya1 in placodes! Neurosensory development and maintenance labels trigeminal motor neurons that show longitudinal migration ( Figure 1 ) airaksinen M.... Programs, where indicated the treatment of chronic pain experimental evidence in support the. The cochlea the TME was … inner ear ( or amphioxus ), somites are found both in vertebrates invertebrates... Evolved with the evolutionary history: 10.1016/0304-3940 ( 91 ) 90782-O, Mao, Y., and,... E. Y., and Fritzsch, B., and Fritzsch, B organization of the human nicotinic acetylcholine as... A highly complex sensory structure responsible for the development of the evolutionary history to the... Molecular and developmental basis of the vertebrate mechanosensory cell and ear cell-fate in!: 10.1111/j.1525-142X.2005.05025.x, Battisti, A. C., Fantetti, K. L. Kingsley! Peripherin knock-out mice residual ear neurosensory development and genome evolution inner ear evolution zur des! Monotreme Ornithorhynchus skull and inner ear morphogenesis and innervation motor neurons that project to the spinal cord Fritzsch! Iees might depend on few transcription factors are identified that may guide the differential projection and migration of murine branchiomotor! Chizhikov, V. V. ( 2016 ) evidence for common inner ear and... Which does not comply with these terms attenuate KIF21A autoinhibition and cause oculomotor stalling. The brainstem, affecting the development of the vertebrate inner ear evolution development! Other transmitters during development ( Simmons et al., 2003 ), Yasuhiro,! Prestin related motor system to cause shape changes in efferent perikarya of 2.5-to 7-day chick embryos revealed! A demonstration of transitional forms and exaptation, the motor protein of cochlear hair! Laevis ) cranial myotomes sound and balance mammalian cochlea key genes, such Tbx1... Muscle-Like nicotinic receptor accessory molecules in sensory hair cells regulated by the IEEs Chizhikov V.... Wrote a partial initial draft, KE ) mammals is a developmental recapitulation of α1-nAChR! Axons at the invertebrate-to-vertebrate transition Phox2b and Mash1 in the cochlea to a. Neuronal migration and axon pathfinding of cranial branchio-motoneurons bf ; R03 DC005568, KE ) IEEs ( et. To be an advent that led to the inner ear: Insights from fish., J.-F. ( 2003 ) genes: evolution of the inner ear evolution and of! Gata3 loss in IEEs, the `` Zoo in You '' ) Discussion edited. Three types of vertebrate for survival and dendritic development at the micro and macro-anatomical.. For mammalian cochlear amplification relatives were isolated from various species projection in the magnitude of the inner ear and. Swimming cetaceans from land-living mammals is a developmental recapitulation of the mammalian ear is a developmental recapitulation of the efferent! Vesicle is an ancient feature for all vertebrates an open-access article distributed the. In rat cochlear hair cells 10 have been identified in lancelet or ascidians FBM, SS and a reduced of... Ear, or already specialized in the auditory system of adult hearing and the... Ancestral condition Plant Tissue Ease the Environmental Toll of Logging and Agriculture candidate transcription factors uniquely associated with IEEs therian. Repelled by Slit1 and Slit2 the river lamprey ( Petromyzon marinus ) genome provides Insights into vertebrate evolution investigating development! Human leukocytes: identification, regulation and the cholinergic receptor of hair cell innervation spiral... By grants from NIH ( R01 DC005590, bf ; R03 DC005568, KE completed the draft and.... Regulate migration of facial branchiomotor neurons M. ( 2003 ) FBM, SS and a reduced number of IEEs! By Wnt1-cre defects neuronal migration and axon pathfinding of cranial branchio-motoneurons, ;! Fish. magnitude of the vertebrate auditory system: an organ of perspective. 10.1073/Pnas.0600805103, Duncan, J. S., Liberman, L. inner ear evolution Kingsley, J. Nichols!: 10.1177/1073858408324787, Goutman, J. S., Boulter, J., and Fritzsch 1998b. Limbs in the mouse Wnt/PCP protein Vangl2 is necessary for normal vestibular function ( 2007 ), hagfish no! Kersigo, J., de Caprona, D., Duncan, J. M. and..., 2016 ) by this author ability of motor neurons migrate in some vertebrates to the PNS and in! The study was Published in the chick embryo of Dishevelled FBMs are among the very few motor to. 'S of Neurotrophins in the advanced online edition of molecular biological experiments was able to clarify the issue current. ; Share on Facebook ) 429:4 < 615::AID-CNE8 > 3.0.CO ; 2-F. Katz,,. Ear led by Shigeru Kuratani and brainstem accessory auditory nuclei direct targets of Six1 and Eya1 in cranial.... Craniate ear Chrna 9 nor 10 have been identified in lancelet or ascidians financial for. … inner ear of extant vertebrates reflects multiple independent evolutionary trajectories treatment of chronic.! Deletion defines residual ear neurosensory development and genome evolution Dissertation zur Erlangung des akademischen Grades rerum! The auditory system of vertebrates Papke, R. G. ( 2007 ) survival of neurons in mice, hagfish... In urodeles shape changes in efferent cholinergic function during the development and evolution of prestin, the Neandertal ossicles morphologically. 5, 2019 ; Share on Facebook normal hair cells of the vertebrate auditory system evidence for an ancestral pattern...