Abstract
Most studies on development of the human auditory system and hearing loss have to date focused on the sensory apparatus, the cochlea. With advancements in magnetic resonance imaging (MRI), there has recently been increasing interest in the subject of cochlear nerve deficiency (CND) and dysfunction. Cochlear nerve deficiency (CND) amongst individuals with congenital sensorineural hearing loss (SNHL) is not as rare as previously thought, with prevalence as high as 18–21 % reported amongst cochlear implant recipients. Cochlear nerve (CN) morphogenesis is a complex process involving cell populations from two disparate progenitors of the otic placode and neural crest cells. In the first trimester, the basic foundation of the auditory pathway is laid down, with the vestibulocochlear ganglion cells delaminating from the otocyst and establishing peripheral and central connections with the developing cochlea and brainstem, respectively. The second trimester is a period of proliferation, growth and myelination. As the number of axons is pruned back closer to the adult level, myelination begins in the intra-cochlear portion of CN and extends proximally. In the third trimester, further maturation of the neuronal connections in conjunction with paralleled development of the cochlea and brainstem leads to emergence of foetal responses to auditory stimuli. Based on the currently available knowledge of the embryological development of CN, various phenotypes of CND are discussed. It is hoped that better understanding of CN ontogenesis will not only lead to further refinement of auditory implant candidacy but also open doors to potential regeneration therapies such as stem cell therapy in the future.
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References
Adunka OF, Roush PA, Teagle HFB, Brown CJ, Zdanski CJ, Jewells V, et al. Internal auditory canal morphology in children with cochlear nerve deficiency. Otol Neurotol. 2006;27(6):793–801.
McClay JE, Booth TN, Parry DA, Johnson R, Roland P. Evaluation of pediatric sensorineural hearing loss with magnetic resonance imaging. Arch Otolaryngol Head Neck Surg. 2008;134(9):945–52. doi:10.1001/archotol.134.9.945.
Wu CM, Lee LA, Chen CK, Chan KC, Tsou YT, Ng SH. Impact of cochlear nerve deficiency determined using 3-dimensional magnetic resonance imaging on hearing outcome in children with cochlear implants. Otol Neurotol. 2015;36(1):14–21. doi:10.1097/MAO.0000000000000568.
Rosenbluth J. The fine structure of acoustic ganglia in the rat. J Cell Biol. 1962;12:329–59.
Harrison RG. Neuroblast versus sheath cell in the development of peripheral nerves. J Comp Neurol. 1924;37:123–205.
Yntema CL. An experimental study on the origin of the sensory neurones and sheath cells of the IXth and Xth cranial nerves in Amblystoma punctatum. J Exp Zool. 1943;92:93–119.
D’Amico-Martel A, Noden D. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat. 1983;166:445–68.
Fekete DM, Wu DK. Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol. 2002;12:35–42.
Barald KF, Kelley MW. From placode to polarization: new tunes in inner ear development. Development. 2004;131:4119–30.
Breuskin I, Bodson M, Thelen N, Thiry M, Borgs L, Nguyen L, et al. Glial but not neuronal development in the cochleo-vestibular ganglion requires Sox10. J Neurochem. 2010;114:1827–39. doi:10.1111/j.1471-4159.2010.06897.x.
Freyer L, Aggarwal V, Morrow BE. Dual embryonic origin of the mammalian otic vesicle forming the inner ear. Development. 2011;138:5403–14. doi:10.1242/dev.069849.
Sandell LL, Butler Tjaden NE, Barlow AJ, Trainor PA. Cochleovestibular nerve development is integrated with migratory neural crest cells. Dev Biol. 2014;385(2):200–10. doi:10.1016/j.ydbio.2013.11.009.
O’Rahilly R. The early development of the otic vesicle in staged human embryos. J Embryol Exp Morphol. 1963;11:741–55.
Ladher RK, O’Neill P, Begbie J. From shared lineage to distinct functions: the development of the inner ear and epibranchial placodes. Development. 2010;137(11):1777–85. doi:10.1242/dev.040055.
Chen J, Streit A. Induction of the inner ear: stepwise specification of otic fate from multipotent progenitors. Hear Res. 2013;297:3–12. doi:10.1016/j.heares.2012.11.018.
Cooper ERA. The development of the human auditory pathway from the cochlear ganglion to the medial geniculate body. Acta Anat (Basel). 1948;5(1–2):99–122.
Altman J, Bayer S. Development of the cranial nerve ganglia and related nuclei in the rat. Berlin: Springer; 1982.
Moore JK, Linthicum Jr FH. The human auditory system: a timeline of development. Int J Audiol. 2007;46:460–78.
Li Y, Yang J, Liu J, Wu H. Restudy of malformations of the internal auditory meatus, cochlear nerve canal and cochlear nerve. Eur Arch Otorhinolaryngol. 2015;272(7):1587–96. doi:10.1007/s00405-014-2951-4.
Pujol R, Lavigne-Rebillard M. Early stages of innervation and sensory cell differentiation in the human organ of Corti. Acta Otolaryngol Suppl. 1985;423:43–50.
Fritzsch B, Silos-Santiago I, Bianchi LM, Fariñas I. The role of neurotrophic factors in regulating the development of inner ear innervation. Trends Neurosci. 1997;20:159–64.
Bernd P. The role of neurotrophins during early development. Gene Expr. 2008;14:241–50.
Rubel EW, Fritzsch B. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci. 2002;25:51–101.
McPhee JR, Van De Water TR. Epithelial-mesenchymal tissue interactions guiding otic capsule formation: the role of the otocyst. J Embryol Exp Morphol. 1986;97:1–24.
Glastonbury CM, Davidson HC, Harnsberger HR, Butler J, Kertesz TR, Shelton C. Imaging findings of cochlear nerve deficiency. AJNR Am J Neuroradiol. 2002;23:635–43.
Lavigne-Rebillard M, Pujol R. Hair cell innervation in the fetal human cochlea. Acta Otolaryngol. 1988;105(5–6):398–402.
Ray B, Roy TS, Wadhwa S, Roy KK. Development of the human fetal cochlear nerve: a morphometric study. Hear Res. 2005;202(1–2):74–86.
Moore JK, Linthicum Jr FH. Myelination of the human auditory nerve: different time courses for Schwann cell and glial myelin. Ann Otol Rhinol Laryngol. 2001;110:655–61.
Birnholz JC, Benecerraf BR. The development of human fetal hearing. Science. 1983;222(4623):516–8.
Kuhlman KA, Burns KA, Depp R, Sabbagha RE. Ultrasonic imaging of normal fetal response to external vibratory acoustic stimulation. Am J Obstet Gynecol. 1988;158(1):47–51.
Starr A, Amlie RN, Martin WH, Sanders S. Development of auditory function in newborn infants revealed by auditory brainstem potentials. Pediatrics. 1977;60(6):831–9.
Krumholz A, Felix JK, Goldstein PH, McKenzie E. Maturation of the brainstem auditory evoked potentials in premature infants. Electroencephalogr Clin Neurophysiol. 1985;62(2):124–34.
Hafner H, Pratt H, Blazer S, Sujov P. Critical ages in brainstem development revealed by neonatal 3-channel Lissajous’ trajectory of auditory brainstem evoked potentials. Hear Res. 1993;66(2):157–68.
Casselman JW, Offeciers FE, Govaerts PJ, Kuhweide R, Geldof H, Somers T, et al. Aplasia and hypoplasia of the vestibulocochlear nerve: diagnosis with MR imaging. Radiology. 1997;202:773–81.
Buchman CA, Roush PA, Teagle HFB, Brown CJ, Zdanski CJ, Grose JH. Auditory neuropathy characteristics in children with cochlear nerve deficiency. Ear Hear. 2006;27:399–408.
Hossain WA, Brumwell CL, Morest DK. Sequential interactions of fibroblast growth factor-2, brain-derived neurotrophic factor, neurotrophin-3, and their receptors define critical periods in the development of cochlear ganglion cells. Exp Neurol. 2002;175:138–51.
Van De Water TR. Effects of removal of the statoacoustic ganglion complex upon the growing otocyst. Ann Otol Rhinol Laryngol. 1976;85:2–31.
Corwin JT, Cotanche DA. Development of location-specific hair cell stereocilia in denervated embryonic ears. J Comp Neurol. 1989;288(4):529–37.
Nelson EG, Hinojosa R. Aplasia of the cochlear nerve: a temporal bone study. Otol Neurotol. 2001;22(6):790–5.
Lefebvre PP, Leprince P, Weber T, Rigo JM, Delree P, Moonen G. Neuronotrophic effect of developing otic vesicle on cochleo-vestibular neurons: evidence for nerve growth factor involvement. Brain Res. 1990;507(2):254–60.
Jackler RK, Luxford WM, House WF. Sound detection with the cochlear implant in five ears of four children with congenital malformations of the cochlea. Laryngoscope. 1987;97(3 Pt 2 Suppl 40):15–7.
Shelton C, Luxford WM, Tonokawa LL, Lo WW, House WF. The narrow internal auditory canal in children: a contraindication to cochlear implants. Otolaryngol Head Neck Surg. 1989;100:227–31.
Govaerts PJ, Casselman J, Daemers K, De Beukelaer C, Yperman M, De Ceulaer G. Cochlear implants in aplasia and hypoplasia of the cochleovestibular nerve. Otol Neurotol. 2003;24:887–91.
Yan F, Li J, Xian J, Wang Z, Mo L. The cochlear nerve canal and internal auditory canal in children with normal cochlea but cochlear nerve deficiency. Acta Radiol. 2013;54(3):292–8.
Tang TP, McPherson B, Yuen KC, Wong LL, Lee JS. Auditory neuropathy/auditory dys-synchrony in school children with hearing loss: frequency of occurrence. Int J Pediatr Otorhinolaryngol. 2004;68:175Y83.
Berlin CI, Hood LJ, Morlet T, Wilensky D, Li L, Mattingly KR, et al. Multi-site diagnosis and management of 260 patients with auditory neuropathy/dys-synchrony (auditory neuropathy spectrum disorder). Int J Audiol. 2010;49(1):30–43.
Roche JP, Huang BY, Castillo M, Bassim MK, Adunka OF, Buchman CA. Imaging characteristics of children with auditory neuropathy spectrum disorder. Otol Neurotol. 2010;31:780–8.
Walton J, Gibson WP, Sanli H, Prelog K. Predicting cochlear implant outcomes in children with auditory neuropathy. Otol Neurotol. 2008;29:302–9.
Huang BY, Roche JP, Buchman CA, Castillo M. Brain stem and inner ear abnormalities in children with auditory neuropathy spectrum disorder and cochlear nerve deficiency. AJNR Am J Neuroradiol. 2010;31(10):1972–9.
Levi J, Ames J, Bacik K, Drake C, Morlet T, O’Reilly RC. Clinical characteristics of children with cochlear nerve dysplasias. Laryngoscope. 2013;123(3):752–6. doi:10.1002/lary.23636.
Thai-Van H, Fraysse B, Berry I, Berges C, Deguine O, Honegger A, et al. Functional magnetic resonance imaging may avoid misdiagnosis of cochleovestibular nerve aplasia in congenital deafness. Am J Otol. 2000;21:663–70.
Zanetti D, Guida M, Barezzani MG, Campovecchi C, Nassif N, Pinelli L, et al. Favorable outcome of cochlear implant in VIIIth nerve deficiency. Otol Neurotol. 2006;27:815–23.
Kutz Jr JW, Lee KH, Isaacson B, Booth TN, Sweeney MH, Roland PS. Cochlear implantation in children with cochlear nerve absence or deficiency. Otol Neurotol. 2011;32:956–61.
Birman CS, Powell HR, Gibson WP, Elliott EJ. Cochlear implant outcomes in cochlea nerve aplasia and hypoplasia. Otol Neurotol. 2016;37(5):438–45. doi:10.1097/MAO.0000000000000997.
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Pai, I. (2017). Embryology of Cochlear Nerve and Its Deficiency. In: Kaga, K. (eds) Cochlear Implantation in Children with Inner Ear Malformation and Cochlear Nerve Deficiency. Modern Otology and Neurotology. Springer, Singapore. https://doi.org/10.1007/978-981-10-1400-0_3
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