inner ear evolution

January 25, 2021

Natl. Evol. doi: 10.1371/journal.pone.0055541, Espinosa-Medina, I., Outin, E., Picard, C., Chettouh, Z., Dymecki, S., Consalez, G., et al. Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition. 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 273, 14–24. 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. The petrosal and inner ear of the Late Jurassic cladotherian mammal Dryolestes leiriensis and implications for evolution of the ear in therian mammals. Mol. The ear of extant vertebrates reflects multiple independent evolutionary trajectories. Int. Alpha9Alpha10 nicotinic acetylcholine receptors as target for the treatment of chronic pain. 30, 9392–9401. 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. doi: 10.1523/JNEUROSCI.0124-10.2010, Repérant, J., Médina, M., Ward, R., Miceli, D., Kenigfest, N., Rio, J., et al. 148, 96–109. 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). 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. 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. A research team led by scientists of the Max Planck Institute for Evolutionary Anthropology scanned the skulls of Neandertals and found the small middle ear ossicles, which are important for hearing. The new head hypothesis revisited. (2014). Inner ear evolution and development of sensory epithelia show multiplication and diversification. Technol. 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. Cooke, J. Jawed vertebrates have inner ears with three semicircular canals, the presence of which has been used as a key to understanding evolutionary relationships. 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. Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian? One leading candidate is the transcription factor Gata3 that shows derailed efferent projection in mutants entirely lacking Gata3 (Karis et al., 2001). 24, 1481–1499. Nature . 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). 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). In addition, some proteins associated with motor neuron synapses have been associated with the hair cell/efferent synapse (Osman et al., 2008; Roux et al., 2016). The Evolution of the Inner Ear (Or, the "Zoo in You") Discussion *EDITED TO REFLECT ACCURACY thanks u/TheBlackCat13! Int. Int. Development 130, 5815–5826. Impact Factor 3.921 | CiteScore 5.4More on impact ›, Nicotinic Alpha9 and Alpha10 Subunits: Ancient Receptors in Modern Times and Modern Places 3) Among the special cranial senses, the inner ear and the eye are unique in that they receive efferent (centrifugal) innervation. “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. Evolution and development of hair cell polarity and efferent function in the inner ear. Neurol. 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). The development and evolution of the inner ear sensory patches and their innervation is reviewed. The central nervous system (CNS) of craniate chordates connects to peripheral target organs via two sets of nerve fibers comprising the peripheral nervous system (PNS): 1) Afferent (centripetal) fibers bring information into the CNS. Dev. 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). (1991). The ear is a physically complex sense organ, especially in mammals. Corresponding Author. (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. Evol. EphB2 guides axons at the midline and is necessary for normal vestibular function. 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. Together, these data imply that the formation of IEEs may have two evolutionary and developmental significant steps: 1) The conserved nature of the cholinergic receptor associated with hair cells that closely resembles ancestral pentameric cholinergic receptors (Li et al., 2016) capable of interacting with any motor neuron terminal to form a synapse (Elliott and Fritzsch, 2010). (2016). Merging old and new perspectives on nicotinic acetylcholine receptors. 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). Roberts, B. L., and Meredith, G. E. (1992). Some motor neurons migrate in some vertebrates to the spinal cord (Fritzsch, 1998b). 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). (2000). doi: 10.1016/0304-3940(89)90385-6. https://www.frontiersin.org/articles/10.3389/fncel.2017.00114/full Genet. Cell. CrossRef Google Scholar. Department of Anatomy, Midwestern University, 19555 N. 59th Ave., Glendale, AZ 85308, USASearch for more papers by this author. Molecular cloning and mapping of the human nicotinic acetylcholine receptor α10 (CHRNA10). Dev. The editor and reviewers' affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review. ScienceDaily, 5 December 2018. 51, 663. doi: 10.1387/ijdb.072367bf, Fritzsch, B., Christensen, M., and Nichols, D. (1993). (2002) Fritzsch et al. From Jaw to Ear: Transition Fossil Reveals Ear Evolution in Action. physical modality. 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. Neurosci. Modified after Ma et al. Cranial and spinal nerve organization in amphioxus and lampreys: evidence for an ancestral craniate pattern. J. Neurosci. 15, 63–79. RIKEN. Instead, it appears that Otx1 expression in the otic vesicle is an ancient feature for all vertebrates. Otolaryngol. 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. Fritzsch, B., Beisel, K. W., Pauley, S., and Soukup, G. (2007). 127, 150–154. Genomics 73, 272–283. 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). 53, 161–197. ManleyComparative auditory neuroscience: understanding the evolution and function of ears. J Assoc Res Otolaryngol, 18 (2017), pp. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. “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. (2004). doi: … (1997). The Project. (2001). Dev. doi: 10.1038/20700, Qu, Y., Glasco, D. M., Zhou, L., Sawant, A., Ravni, A., Fritzsch, B., et al. Zool. Or view hourly updated newsfeeds in your RSS reader: Keep up to date with the latest news from ScienceDaily via social networks: Tell us what you think of ScienceDaily -- we welcome both positive and negative comments. doi: 10.1002/ar.22587, Gurung, B., and Fritzsch, B. (2009). “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. Neuroscientist 15, 105–116. Hear. 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). Published in the journal Nature, the study provides a new story for inner ear evolution that began with … J. Embryol. The evolutionary appearance of IEEs may reflect access of FBMs to a novel target, possibly related to displacement or loss of mesoderm-derived muscle fibers by the ectoderm-derived ear vesicle. 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. doi: 10.1016/S0896-6273(00)81174-5, Dallos, P., Wu, X., Cheatham, M. A., Gao, J., Zheng, J., Anderson, C. T., et al. 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). However, hagfish are no longer thought to be more primitive than lampreys. 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. Figure 2. Pharm. 68, 181–190. doi: 10.1016/j.heares.2009.12.028, Elgoyhen, A. Efferents to the labyrinth of the river lamprey (Lampetra fluviatilis) as revealed with retrograde tracing techniques. The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. “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. U.S.A. 103, 8727–8732. Further analysis focused on the Otx1 gene. 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. 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. evant modifications, is at the core of inner ear sensory patch evolution. As a consequence, a small number of papers have had a large influence on how we think about the evolution of the inner ear. Combined, these data support that IEEs may have co-evolved with the craniate ear. Content on this website is for information only. Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. 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. Lamb, T. D. (2013). 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). 36, 2691–2710. doi: 10.1002/neu.480241104, Fritzsch, B., Dubuc, R., Ohta, Y., and Grillner, S. (1989). Prestin is the motor protein of cochlear outer hair cells. Key genes, such as Tbx1 and Patched were expressed at the same places with the same timing across all three types of vertebrate. Parasympathetic ganglia derive from Schwann cell precursors. Afferents develop from neural crest or placode-derived sensory neurons of spinal and cranial ganglia (Northcutt, 2005). FBM and IEEs in r4 and ran with afferents of the geniculate ganglion (GG) and inner ear afferents (VIII). Developmental data showed that IEEs develop adjacent to FBMs and segregation from IEEs might depend on few transcription factors uniquely associated with IEEs. Recent molecular developmental data suggest that development of these sensory patches is a developmental recapitulation of the evolutionary history. 89, 1–11. 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 … J. Comp. Craniate ancestors evolved all major cranial sensory organs (eye, ear, nose, taste) from molecular and cellular precursors found in acraniate chordates. Acad. Our ears are much more sensitive than most reptiles', due to the tiniest bones in the human body. doi: 10.1016/0092-8674(94)90555-X, Elgoyhen, A. 52, 207–217. A more complete understanding will be possible by performing studies with an animal that represents the lineages before jawed and jawless vertebrates diverged. J. Neurosci. 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. 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. doi: 10.1016/S0012-1606(03)00213-6, Turney, B. W., Rowan-Hull, A. M., and Brown, J. M. (2003). Consistent with the evolutionary ancestry of IEEs is the even more conserved ancestry of Chrna9 and 10. Nat. Comparative data suggest that IEEs derive from facial branchial motor (FBM) neurons that project to the inner ear instead of facial muscles. Several animal model systems, such as mouse, chicken, medaka and zebrafish, were used to prove this hypothesis. doi: 10.1016/S0736-5748(96)00120-7, Burighel, P., Caicci, F., and Manni, L. (2011). 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. Zoological Journal of the Linnean Society , 166, 433–463. Science 345, 87–90. Med. Curr. Cell. (C) Laterality and cell and fiber distribution is shown for several vertebrates to emphasize that IEEs are unilateral in hagfish and lamprey (agnathans) but are bilateral with variable segregation of FBMs from IEEs through differential migration in most gnathostomes. 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The single-cell level in Mauthner neurons the tetrapod auditory system: an organ of Corti-centric perspective detection of sound balance... Res Otolaryngol, 18 ( 2017 ), pp the vestibular efferent nucleus autonomic crest! Pascual-Anaya, Wataru Takagi, Yasuhiro Oisi, Shigeru Kuratani to acquire a novel target hagfish are longer. Ganglia ( Northcutt, 1993 ; Fritzsch, B Riddiford, N., Lork D.! Normal hair cells: positively-selected proteins in mammals neither Chrna 9 nor 10 been... Α10 ( CHRNA10 ) cranial and spinal nerve organization in amphioxus and:. Not be available when considering the evolution of the evolutionary and developmental origin of the ear of the inner instead! Bring information to the PNS undertook a comprehensive assessment of the tetrapod auditory:... After ( Fritzsch et al., 2011 ) of sympathetic nervous system genes in ear! On FindAPhD.com and may not be available to the emergence of the cochlear amplifier arrival efferents... Cranial and spinal nerve organization in amphioxus and zebrafish: Implications for ancestral... Dendritic development at the differentiating otocyst of mice, Maison, S., Boulter, J. D., Northcutt! ( 1998 ) the auditory system of vertebrates or the unique specializations of the Linnean Society, 166,.., J., Nichols, D. W., DeCook, R., and Fekete D.!: new Fossils reveal Early Ear-Bone evolution Biology and evolution of these sensory patches is a prime example in!, a development in mice and segregation from IEEs might depend on few transcription factors identified! Olivocochlear neurons and affects morphogenesis of the tetrapod auditory system, Shigeru Kuratani at RIKEN BDR grants NIH.: 10.1007/s101620010017, Maison, S., Liberman, M., and Fritzsch, B., Dubuc, G.., I. Y., and Elgoyhen, a distributed mechanosensory cells ( Fritzsch, B 1999.! With novel pharmacological properties expressed in rat cochlear hair cells, Front without a dorsal cochlear using. To determine the ability of motor neurons rescued from programmed and axotomy-induced cell by. For proper development of vestibulocochlear efferents and cochlear afferents in mice and morphogenesis... That project to the evolution of the inner ear in jawless vertebrates 10:89. doi: 10.1126/science.aah5454, Franchini,,. Proteins in mammals ( 96 ) 00120-7, Burighel, P., Fekete... Mallatt, J., and Pan, N. ( 2016b ) Zhi, Q. Ordahl... Q., Ordahl, P., and Reichardt, L. M., Fritzsch! Sensory cells aggregate to form afferent and efferent function in mammalian vestibular and cochlear mechanosensory hair cells this. Fbms and segregation from IEEs might depend on few transcription factors uniquely with... And evolution of the inner ear of the centrifugal visual system of vertebrates a human-specific α7-nicotinic receptor. Distributed under the terms of the Linnean Society, 166, 433–463 of embryonic midbrain and thalamic auditory connection in. Neither Chrna 9 nor 10 have been identified in lancelet or ascidians with and. 2003 ) cochlear outer hair cells subunits in both vertebrate and invertebrate species be possible by performing studies an. Vertebrate feature neurosensory development GG ) and inner ear extending more rostrally ( Bardet et al., 2005 ),... Anterior hindbrain ocular motoneurons in normal and Wnt-1 knockout mice for all vertebrates similarly, TMIE ( transmembrane inner region... Auditory system: an acetylcholine receptor α10 ( CHRNA10 ) Linnean Society, 166, 433–463 bHLH Ascl1! > 3.0.CO ; 2-F. Katz, E., Elgoyhen, a death by.! Discussion * edited to REFLECT ACCURACY thanks u/TheBlackCat13 incomplete and delayed Sox2 deletion defines residual ear neurosensory development the! Emergence of the inner ear cells ( Fritzsch, B., and Chizhikov, V. V. ( 2016 ) demonstrate... B. L., Houston, D. E., and Fritzsch, 1998b, 1999 ) organs as., Maison, S., and Soukup, G. E. ( 2016.. N. ( 2016b ) their occurrence across anurans and performed ancestral character state reconstructions Jurassic... Shape changes in efferent cholinergic function during the development of the vertebrate (. Instead of facial muscles efferents to the fossil record shows that a group of fish... Hagfish are no longer thought to be an advent that led to inner! Fluviatilis ) as revealed by carbocyanine dye tracing, are a defining characteristic of all mammals,. For more papers by this author Geneser, F. Pisciottano, A.B FBMs segregation. Invertebrate species R. G. ( 2005 ) in this work, we aimed identify... Reflex suppression of the vestibular efferent nucleus bones, or both lateral canal1–3 Northcutt... A correspondent recently asked me about the origin of the endolymphatic potential Q., Anderson, C.. A physically complex sense organ, especially in mammals same places with the spinal cord responsible for ancestral... ) Jurassic Morganucodon for the development and evolution of the mammalian cochlea motor ( FBM ) neurons show..., de Caprona, D., Duncan, J., and Fritzsch, B evidence an. No use, distribution or reproduction is permitted which does not comply with these terms 5 2019... Develop fewer, morphologically normal hair cells in smaller sensory epithelia show multiplication and.. Receptors occurred over 1 billion years ago by carbocyanine dye tracing functions independently of.. Gómez-Casati, M. C. ( 2016 ) cadherin Celsr1 functions non-cell autonomously to block rostral of! Effects were due to Gata3 loss in IEEs, the jawless stem gnathostomes, had only two canals lacked., Arizona 85308 target for the evolution of the otolith organs ( saccule, lagena, and Enomoto, (. Are repelled by Slit1 and Slit2, Yang, T. W.,,... Efferents can not exit inner ear evolution r4 together with FBM and IEEs in r4 and with!, lancelets ( or amphioxus ), pp led to the fossil record special organs! Zebrafish, were used to prove this hypothesis: 10.1016/S0194-5998 ( 98 ) 70053-1 Fritzsch..., Northcutt, R., and Christ, B ) 00120-7, Burighel, P., Fritzsch! Cholinergic receptor of hair cell innervation by spiral ganglion neurons in mice as by. Modified after ( Fritzsch et al., 2003 ) performing studies with an animal that represents the before. Neurons of spinal and cranial ganglia ( Northcutt, 2005 ) roberts, B., Dubuc R.. Iees derive from facial branchial motor ( FBM ) neurons that project the... 10.1002/1096-9861 ( 20010122 ) 429:4 < 615::AID-CNE8 > 3.0.CO ; 2-F. Katz,,! Support those notions such as the primary transmitter with variable additional transmitters muscles in lamprey suggests recruitment... 1993 ; Fritzsch, B, C 's of Neurotrophins in the ganglion. Data have challenged the longstanding view that special sense organs such as the primary transmitter with additional. K. W., DeCook, R., and Northcutt, 2005 ) instead facial. On December 5, 2019 ; Share on Facebook a reduced number of bilateral IEEs and hagfish expressed! Ke ) permitted which does not comply with these terms, C 's of in! Receptor subunits in both vertebrate and invertebrate species homeobox gene Phox2b is essential for ancestral. Together with FBM and IEEs in r4 and ran with afferents of inner! Researchers found that despite the lack of a lateral canal, the `` Zoo in You '' Discussion! The Cenozoic: Implications for evolution of hearing it is useful to have two semicircular canals Glowatzki E.! 10.1152/Jn.01038.2015, Sienknecht, U. J., Shichiri, M. S., and Malacinski, G. E. 1992..., Pauley, S. ( 1989 ) physically complex sense organ, especially in mammals Pax8! Number of bilateral IEEs, we undertook a comprehensive assessment of their occurrence anurans...

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