{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:08:32Z","timestamp":1790798912170,"version":"4.1.0"},"reference-count":92,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T00:00:00Z","timestamp":1545177600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T00:00:00Z","timestamp":1545177600000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T00:00:00Z","timestamp":1545177600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000288","name":"Royal Society","doi-asserted-by":"publisher","award":["NF120319"],"award-info":[{"award-number":["NF120319"]}],"id":[{"id":"10.13039\/501100000288","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>Vestibular function was established early in vertebrates and has remained, for the most part, unchanged. In contrast, each group of tetrapods underwent independent evolutionary processes to solve the problem of hearing on land, resulting in a remarkable mixture of conserved, divergent and convergent features that define extant auditory systems. The vestibuloacoustic nuclei of the hindbrain develop from a highly conserved ground plan and provide an ideal framework on which to address the participation of developmental processes to the evolution of neuronal circuits. We employed an electroporation strategy to unravel the contribution of two dorsoventral and four axial lineages to the development of the chick hindbrain vestibular and auditory nuclei. We compare the chick developmental map with recently established genetic fate-maps of the developing mouse hindbrain. Overall, we find considerable conservation of developmental origin for the vestibular nuclei. In contrast, a comparative analysis of the developmental origin of hindbrain auditory structures echoes the complex evolutionary history of the auditory system. In particular, we find that the developmental origin of the chick auditory interaural time difference circuit supports its emergence from an ancient vestibular network, unrelated to the analogous mammalian counterpart.<\/jats:p>","DOI":"10.7554\/elife.40232","type":"journal-article","created":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T08:00:31Z","timestamp":1545206431000},"source":"Crossref","is-referenced-by-count":40,"title":["Conserved and divergent development of brainstem vestibular and auditory nuclei"],"prefix":"10.7554","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9328-0328","authenticated-orcid":true,"given":"Marcela","family":"Lipovsek","sequence":"first","affiliation":[{"name":"Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience, King\u2019s College London, London, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1662-6097","authenticated-orcid":true,"given":"Richard JT","family":"Wingate","sequence":"additional","affiliation":[{"name":"Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience, King\u2019s College London, London, United Kingdom"},{"name":"MRC Centre for Neurodevelopmental Disorders, Institute of Psychiatry, Psychology and Neuroscience, King\u2019s College London, London, United Kingdom"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2018,12,19]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/j.ydbio.2015.10.008","article-title":"En1 directs superior olivary complex neuron positioning, survival, and expression of FoxP1","volume":"408","author":"Altieri","year":"2015","journal-title":"Developmental Biology"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1111\/j.1469-7580.2012.01526.x","article-title":"Evolution of the mammalian middle ear and jaw: adaptations and novel structures","volume":"222","author":"Anthwal","year":"2013","journal-title":"Journal of Anatomy"},{"key":"bib3","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1016\/j.conb.2011.05.008","article-title":"Sound localization: Jeffress and beyond","volume":"21","author":"Ashida","year":"2011","journal-title":"Current Opinion in Neurobiology"},{"key":"bib4","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1242\/dev.127.5.1039","article-title":"Functional conservation of atonal and Math1 in the CNS and PNS","volume":"127","author":"Ben-Arie","year":"2000","journal-title":"Development"},{"key":"bib5","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1002\/cne.902970105","article-title":"Migration of neuroblasts by perikaryal translocation: role of cellular elongation and axonal outgrowth in the acoustic nuclei of the chick embryo medulla","volume":"297","author":"Book","year":"1990","journal-title":"The Journal of Comparative Neurology"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"91","DOI":"10.3389\/fncir.2016.00091","article-title":"Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians","volume":"10","author":"Branoner","year":"2016","journal-title":"Frontiers in Neural Circuits"},{"key":"bib7","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1002\/cne.20334","article-title":"Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways","volume":"481","author":"Burger","year":"2005","journal-title":"The Journal of Comparative Neurology"},{"key":"bib8","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1152\/jn.00205.2011","article-title":"Inhibition in the balance: binaurally coupled inhibitory feedback in sound localization circuitry","volume":"106","author":"Burger","year":"2011","journal-title":"Journal of Neurophysiology"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1111\/j.1749-6632.1992.tb25222.x","article-title":"Patterns of connectivity in the vestibular nuclei","volume":"656","author":"B\u00fcttner-Ennever","year":"1992","journal-title":"Annals of the New York Academy of Sciences"},{"key":"bib10","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1002\/1096-9861(20001127)427:4<522::AID-CNE3>3.0.CO;2-Y","article-title":"Rostrocaudal nuclear relationships in the avian medulla oblongata: a fate map with quail chick chimeras","volume":"427","author":"Cambronero","year":"2000","journal-title":"The Journal of Comparative Neurology"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1016\/S0361-9230(03)00050-9","article-title":"Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei","volume":"60","author":"Cant","year":"2003","journal-title":"Brain Research Bulletin"},{"key":"bib12","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.conb.2016.07.001","article-title":"Evolutionary trends in directional hearing","volume":"40","author":"Carr","year":"2016","journal-title":"Current Opinion in Neurobiology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1159\/000063565","article-title":"Evolutionary convergence and shared computational principles in the auditory system","volume":"59","author":"Carr","year":"2002","journal-title":"Brain, Behavior and Evolution"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1159\/000456646","article-title":"Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective","volume":"90","author":"Chagnaud","year":"2017","journal-title":"Brain, Behavior and Evolution"},{"key":"bib15","doi-asserted-by":"publisher","first-page":"e34762","DOI":"10.1371\/journal.pone.0034762","article-title":"Hoxb1 controls anteroposterior identity of vestibular projection neurons","volume":"7","author":"Chen","year":"2012","journal-title":"PLoS ONE"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"1253","DOI":"10.1242\/dev.02289","article-title":"Krox20 hindbrain cis-regulatory landscape: interplay between multiple long-range initiation and autoregulatory elements","volume":"133","author":"Chomette","year":"2006","journal-title":"Development"},{"key":"bib17","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1038\/519168a","article-title":"Evolutionary biology: The origin of terrestrial hearing","volume":"519","author":"Clack","year":"2015","journal-title":"Nature"},{"key":"bib18","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1006\/dbio.2000.9779","article-title":"Embryonic origins of auditory brain-stem nuclei in the chick hindbrain","volume":"224","author":"Cramer","year":"2000","journal-title":"Developmental Biology"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1016\/j.conb.2008.08.016","article-title":"Cochlear amplification, outer hair cells and prestin","volume":"18","author":"Dallos","year":"2008","journal-title":"Current Opinion in Neurobiology"},{"key":"bib20","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1016\/S0306-4522(02)00834-5","article-title":"Plurisegmental vestibulocerebellar projections and other hindbrain cerebellar afferents in midterm chick embryos: biotinylated dextranamine experiments in vitro","volume":"117","author":"Daz","year":"2003","journal-title":"Neuroscience"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"e1003249","DOI":"10.1371\/journal.pgen.1003249","article-title":"Assembly of the auditory circuitry by a Hox genetic network in the mouse brainstem","volume":"9","author":"Di Bonito","year":"2013","journal-title":"PLoS Genetics"},{"key":"bib22","doi-asserted-by":"publisher","DOI":"10.1523\/ENEURO.0096-15.2015","article-title":"Loss of Projections, Functional Compensation, and Residual Deficits in the Mammalian Vestibulospinal System of Hoxb1-Deficient Mice","volume":"2","author":"Di Bonito","year":"2015","journal-title":"eNeuro"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"3509","DOI":"10.1007\/s00429-017-1416-0","article-title":"Nuclear derivatives and axonal projections originating from rhombomere 4 in the mouse hindbrain","volume":"222","author":"Di Bonito","year":"2017","journal-title":"Brain Structure and Function"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"18","DOI":"10.3389\/fncir.2017.00018","article-title":"Cellular and Molecular Underpinnings of Neuronal Assembly in the Central Auditory System during Mouse Development","volume":"11","author":"Di Bonito","year":"2017","journal-title":"Frontiers in Neural Circuits"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1007\/978-1-4614-1704-0","volume-title":"In Sensing in Nature","author":"Duncan","year":"2012"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"197","DOI":"10.1007\/978-3-319-21059-9_10","article-title":"What the Toadfish Ear Tells the Toadfish Brain About Sound","volume":"877","author":"Edds-Walton","year":"2016","journal-title":"Advances in Experimental Medicine and Biology"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/j.neuron.2006.03.014","article-title":"Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps","volume":"50","author":"Farago","year":"2006","journal-title":"Neuron"},{"key":"bib28","doi-asserted-by":"publisher","first-page":"8541","DOI":"10.1128\/MCB.25.19.8541-8552.2005","article-title":"Hoxb1 enhancer and control of rhombomere 4 expression: complex interplay between PREP1-PBX1-HOXB1 binding sites","volume":"25","author":"Ferretti","year":"2005","journal-title":"Molecular and Cellular Biology"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.ydbio.2017.08.034","article-title":"Gene, cell, and organ multiplication drives inner ear evolution","volume":"431","author":"Fritzsch","year":"2017","journal-title":"Developmental Biology"},{"key":"bib30","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1007\/s00359-013-0865-z","article-title":"Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies","volume":"200","author":"Fritzsch","year":"2014","journal-title":"Journal of Comparative Physiology A"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"2049","DOI":"10.1242\/dev.033480","article-title":"Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1","volume":"136","author":"Fujiyama","year":"2009","journal-title":"Development"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1242\/dev.099119","article-title":"Independently specified Atoh1 domains define novel developmental compartments in rhombomere 1","volume":"141","author":"Green","year":"2014","journal-title":"Development"},{"key":"bib33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1749-8104-9-1","article-title":"Developmental origins of diversity in cerebellar output nuclei","volume":"9","author":"Green","year":"2014","journal-title":"Neural Development"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/nrn1136","article-title":"New roles for synaptic inhibition in sound localization","volume":"4","author":"Grothe","year":"2003","journal-title":"Nature Reviews Neuroscience"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1007\/978-1-4419-8957-4","volume-title":"Evolution of Vertebrate Auditory System","author":"Grothe","year":"2004"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"983","DOI":"10.1152\/physrev.00026.2009","article-title":"Mechanisms of sound localization in mammals","volume":"90","author":"Grothe","year":"2010","journal-title":"Physiological Reviews"},{"key":"bib37","doi-asserted-by":"publisher","first-page":"116","DOI":"10.3389\/fncir.2014.00116","article-title":"The natural history of sound localization in mammals--a story of neuronal inhibition","volume":"8","author":"Grothe","year":"2014","journal-title":"Frontiers in Neural Circuits"},{"key":"bib38","doi-asserted-by":"publisher","first-page":"e148","DOI":"10.1093\/nar\/gku750","article-title":"A 'tool box' for deciphering neuronal circuits in the developing chick spinal cord","volume":"42","author":"Hadas","year":"2014","journal-title":"Nucleic Acids Research"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1002\/jmor.1050880104","article-title":"A series of normal stages in the development of the chick embryo","volume":"88","author":"Hamburger","year":"1951","journal-title":"Journal of Morphology"},{"key":"bib40","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1242\/dev.127.6.1185","article-title":"Autoregulation and multiple enhancers control Math1 expression in the developing nervous system","volume":"127","author":"Helms","year":"2000","journal-title":"Development"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1002\/cne.21031","article-title":"Formation of the avian nucleus magnocellularis from the auditory anlage","volume":"498","author":"Hendricks","year":"2006","journal-title":"The Journal of Comparative Neurology"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"530","DOI":"10.1016\/j.neuron.2008.07.012","article-title":"Making an effort to listen: mechanical amplification in the ear","volume":"59","author":"Hudspeth","year":"2008","journal-title":"Neuron"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1037\/h0061495","article-title":"A place theory of sound localization","volume":"41","author":"Jeffress","year":"1948","journal-title":"Journal of Comparative and Physiological Psychology"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"3016","DOI":"10.1523\/JNEUROSCI.5175-10.2011","article-title":"Axonal branching patterns as sources of delay in the mammalian auditory brainstem: a re-examination","volume":"31","author":"Karino","year":"2011","journal-title":"Journal of Neuroscience"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"6853","DOI":"10.1038\/ncomms7853","article-title":"Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids","volume":"6","author":"Kitazawa","year":"2015","journal-title":"Nature Communications"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"5757","DOI":"10.1523\/JNEUROSCI.4231-11.2012","article-title":"Axonal patterns and targets of dA1 interneurons in the chick hindbrain","volume":"32","author":"Kohl","year":"2012","journal-title":"Journal of Neuroscience"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.heares.2010.03.095","article-title":"Birds--same thing, but different? Convergent evolution in the avian and mammalian auditory systems provides informative comparative models","volume":"273","author":"K\u00f6ppl","year":"2011","journal-title":"Hearing Research"},{"key":"bib48","volume-title":"A Stereotaxic Atlas of the Brain of the Chick (Gallus Domesticus)","author":"Kuenzel","year":"1988"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1002\/cne.903480307","article-title":"GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus","volume":"348","author":"Lachica","year":"1994","journal-title":"Journal of Comparative Neurology"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.neuron.2005.08.028","article-title":"Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors","volume":"48","author":"Machold","year":"2005","journal-title":"Neuron"},{"key":"bib51","doi-asserted-by":"publisher","first-page":"3310","DOI":"10.1523\/JNEUROSCI.5318-09.2010","article-title":"Functional organization of vestibular commissural connections in frog","volume":"30","author":"Malinvaud","year":"2010","journal-title":"Journal of Neuroscience"},{"key":"bib52","doi-asserted-by":"publisher","first-page":"11736","DOI":"10.1073\/pnas.97.22.11736","article-title":"Cochlear mechanisms from a phylogenetic viewpoint","volume":"97","author":"Manley","year":"2000","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"bib53","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4419-8957-4","volume-title":"Evolution of Vertebrate Auditory System","author":"Manley","year":"2004"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10162-016-0579-3","article-title":"Comparative Auditory Neuroscience: Understanding the Evolution and Function of Ears","volume":"18","author":"Manley","year":"2017","journal-title":"Journal of the Association for Research in Otolaryngology"},{"key":"bib55","doi-asserted-by":"crossref","first-page":"3595","DOI":"10.1242\/dev.128.18.3595","article-title":"Independent regulation of initiation and maintenance phases of Hoxa3 expression in the vertebrate hindbrain involve auto- and cross-regulatory mechanisms","volume":"128","author":"Manzanares","year":"2001","journal-title":"Development"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"11123","DOI":"10.1523\/JNEUROSCI.2232-09.2009","article-title":"Atoh1-lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei","volume":"29","author":"Maricich","year":"2009","journal-title":"Journal of Neuroscience"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ydbio.2008.08.017","article-title":"Hox gene colinear expression in the avian medulla oblongata is correlated with pseudorhombomeric domains","volume":"323","author":"Mar\u00edn","year":"2008","journal-title":"Developmental Biology"},{"key":"bib58","doi-asserted-by":"publisher","first-page":"1714","DOI":"10.1111\/j.1460-9568.1995.tb00693.x","article-title":"Morphological fate of rhombomeres in quail\/chick chimeras: a segmental analysis of hindbrain nuclei","volume":"7","author":"Mar\u00edn","year":"1995","journal-title":"European Journal of Neuroscience"},{"key":"bib59","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1002\/dneu.22069","article-title":"Embryonic origins of the mouse superior olivary complex","volume":"73","author":"Marrs","year":"2013","journal-title":"Developmental Neurobiology"},{"key":"bib60","doi-asserted-by":"publisher","first-page":"2391","DOI":"10.1113\/jphysiol.2011.226886","article-title":"Embryonic assembly of auditory circuits: spiral ganglion and brainstem","volume":"590","author":"Marrs","year":"2012","journal-title":"The Journal of Physiology"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"11139","DOI":"10.1523\/JNEUROSCI.2303-09.2009","article-title":"Multiple transcriptional mechanisms control Ptf1a levels during neural development including autoregulation by the PTF1-J complex","volume":"29","author":"Meredith","year":"2009","journal-title":"Journal of Neuroscience"},{"key":"bib62","doi-asserted-by":"crossref","first-page":"3135","DOI":"10.1242\/dev.124.16.3135","article-title":"HOXD4 and regulation of the group 4 paralog genes","volume":"124","author":"Morrison","year":"1997","journal-title":"Development"},{"key":"bib63","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1006\/dbio.1996.0069","article-title":"A chick homologue of Serrate and its relationship with Notch and Delta homologues during central neurogenesis","volume":"174","author":"Myat","year":"1996","journal-title":"Developmental Biology"},{"key":"bib64","doi-asserted-by":"publisher","first-page":"3790","DOI":"10.1038\/ncomms4790","article-title":"Glycinergic inhibition tunes coincidence detection in the auditory brainstem","volume":"5","author":"Myoga","year":"2014","journal-title":"Nature Communications"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"33","DOI":"10.3389\/fnana.2011.00033","article-title":"The structural, functional, and molecular organization of the brainstem","volume":"5","author":"Nieuwenhuys","year":"2011","journal-title":"Frontiers in Neuroanatomy"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.pneurobio.2016.02.003","article-title":"Evolution of mammalian sound localization circuits: A developmental perspective","volume":"141","author":"Nothwang","year":"2016","journal-title":"Progress in Neurobiology"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"9670","DOI":"10.1523\/JNEUROSCI.2189-07.2007","article-title":"Fate-mapping the mammalian hindbrain: segmental origins of vestibular projection neurons assessed using rhombomere-specific Hoxa2 enhancer elements in the mouse embryo","volume":"27","author":"Pasqualetti","year":"2007","journal-title":"Journal of Neuroscience"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1016\/j.jchemneu.2008.02.003","article-title":"Morphometric analysis of the AMPA-type neurons in the Deiter's vestibular complex of the chick brain","volume":"35","author":"Passetto","year":"2008","journal-title":"Journal of Chemical Neuroanatomy"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1002\/cne.902970210","article-title":"Vestibulo-ocular projections in the 11-day chicken embryo: pathway specificity","volume":"297","author":"P\u00e9tursd\u00f3ttir","year":"1990","journal-title":"Journal of Comparative Neurology"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1016\/j.neuron.2013.09.020","article-title":"Hox genes: choreographers in neural development, architects of circuit organization","volume":"80","author":"Philippidou","year":"2013","journal-title":"Neuron"},{"key":"bib71","doi-asserted-by":"publisher","first-page":"22462","DOI":"10.1073\/pnas.0911579106","article-title":"Excitatory neurons of the proprioceptive, interoceptive, and arousal hindbrain networks share a developmental requirement for Math1","volume":"106","author":"Rose","year":"2009","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1016\/S0361-9230(03)00049-2","article-title":"Primary innervation of the avian and mammalian cochlear nucleus","volume":"60","author":"Ryugo","year":"2003","journal-title":"Brain Research Bulletin"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"706","DOI":"10.1002\/dvdy.21084","article-title":"Visualization of two distinct classes of neurons by gad2 and zic1 promoter\/enhancer elements in the dorsal hindbrain of developing zebrafish reveals neuronal connectivity related to the auditory and lateral line systems","volume":"236","author":"Sassa","year":"2007","journal-title":"Developmental Dynamics"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1002\/cne.903310208","article-title":"Projections of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive","volume":"331","author":"Smith","year":"1993","journal-title":"The Journal of Comparative Neurology"},{"key":"bib75","doi-asserted-by":"publisher","first-page":"192","DOI":"10.1002\/1096-9861(20000108)429:2<192::AID-CNE2>3.0.CO;2-5","article-title":"The cytoarchitecture of the nucleus angularis of the barn owl (Tyto alba)","volume":"429","author":"Soares","year":"2001","journal-title":"The Journal of Comparative Neurology"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1152\/jn.2002.88.1.152","article-title":"Intrinsic neuronal properties of the chick nucleus angularis","volume":"88","author":"Soares","year":"2002","journal-title":"Journal of Neurophysiology"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1016\/S0361-9230(01)00670-0","article-title":"The frog as a unique vertebrate model for studying the rhombomeric organization of functionally identified hindbrain neurons","volume":"57","author":"Straka","year":"2002","journal-title":"Brain Research Bulletin"},{"key":"bib78","doi-asserted-by":"publisher","first-page":"182","DOI":"10.3389\/fncir.2013.00182","article-title":"Vestibular blueprint in early vertebrates","volume":"7","author":"Straka","year":"2013","journal-title":"Frontiers in Neural Circuits"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1159\/000357833","article-title":"Connecting ears to eye muscles: evolution of a 'simple' reflex arc","volume":"83","author":"Straka","year":"2014","journal-title":"Brain, Behavior and Evolution"},{"key":"bib80","doi-asserted-by":"publisher","first-page":"1493","DOI":"10.1002\/cne.22807","article-title":"Tonotopic organization of the superior olivary nucleus in the chicken auditory brainstem","volume":"520","author":"Tabor","year":"2012","journal-title":"The Journal of Comparative Neurology"},{"key":"bib81","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1002\/cne.902740206","article-title":"Projections of the cochlear nuclei and nucleus laminaris to the inferior colliculus of the barn owl","volume":"274","author":"Takahashi","year":"1988","journal-title":"The Journal of Comparative Neurology"},{"key":"bib82","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1007\/BF00196834","article-title":"Development of the nuclei and cell migration in the medulla oblongata. Application of the quail-chick chimera system","volume":"183","author":"Tan","year":"1991","journal-title":"Anatomy and Embryology"},{"key":"bib83","doi-asserted-by":"publisher","first-page":"815","DOI":"10.1007\/s00429-014-0938-y","article-title":"Crypto-rhombomeres of the mouse medulla oblongata, defined by molecular and morphological features","volume":"221","author":"Tom\u00e1s-Roca","year":"2016","journal-title":"Brain Structure and Function"},{"key":"bib84","doi-asserted-by":"publisher","first-page":"20150483","DOI":"10.1098\/rstb.2015.0483","article-title":"Major evolutionary transitions and innovations: the tympanic middle ear","volume":"372","author":"Tucker","year":"2017","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences"},{"key":"bib85","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1159\/000476028","article-title":"Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem","volume":"90","author":"Walton","year":"2017","journal-title":"Brain, Behavior and Evolution"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1016\/j.neuron.2005.08.024","article-title":"Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum","volume":"48","author":"Wang","year":"2005","journal-title":"Neuron"},{"key":"bib87","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1016\/j.gde.2015.02.006","article-title":"Development of the inner ear","volume":"32","author":"Whitfield","year":"2015","journal-title":"Current Opinion in Genetics & Development"},{"key":"bib88","doi-asserted-by":"publisher","first-page":"2149","DOI":"10.1002\/cne.22325","article-title":"Connections of the auditory brainstem in a songbird, Taeniopygia guttata. III. Projections of the superior olive and lateral lemniscal nuclei","volume":"518","author":"Wild","year":"2010","journal-title":"The Journal of Comparative Neurology"},{"key":"bib89","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1016\/j.ydbio.2006.05.028","article-title":"Temporal identity transition in the avian cerebellar rhombic lip","volume":"297","author":"Wilson","year":"2006","journal-title":"Developmental Biology"},{"key":"bib90","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1007\/BF00315083","article-title":"The vestibular nuclei in the domestic hen (Gallus domesticus). I. Normal anatomy","volume":"149","author":"Wold","year":"1976","journal-title":"Anatomy and Embryology"},{"key":"bib91","doi-asserted-by":"publisher","first-page":"27","DOI":"10.3389\/fnana.2011.00027","article-title":"The long adventurous journey of rhombic lip cells in jawed vertebrates: a comparative developmental analysis","volume":"5","author":"Wullimann","year":"2011","journal-title":"Frontiers in Neuroanatomy"},{"key":"bib92","doi-asserted-by":"publisher","first-page":"10924","DOI":"10.1523\/JNEUROSCI.1423-07.2007","article-title":"Origin of climbing fiber neurons and their developmental dependence on Ptf1a","volume":"27","author":"Yamada","year":"2007","journal-title":"Journal of Neuroscience"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/40232\/elife-40232-v2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/40232\/elife-40232-v2.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/40232","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,11]],"date-time":"2023-10-11T21:01:23Z","timestamp":1697058083000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/40232"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,12,19]]},"references-count":92,"alternative-id":["10.7554\/eLife.40232"],"URL":"https:\/\/doi.org\/10.7554\/elife.40232","archive":["CLOCKSS"],"relation":{"has-review":[{"id-type":"doi","id":"10.7554\/eLife.40232.014","asserted-by":"object"},{"id-type":"doi","id":"10.7554\/eLife.40232.015","asserted-by":"object"}],"has-preprint":[{"id-type":"doi","id":"10.1101\/372243","asserted-by":"object"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,12,19]]},"article-number":"e40232"}}