Talking back: Development of the olivocochlear efferent system

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Michelle M. Frank, Lisa V. Goodrich

Published Online: Jun 26 2018

DOI: 10.1002/wdev.324

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Developing sensory systems must coordinate the growth of neural circuitry spanning from receptors in the peripheral nervous system (PNS) to multilayered networks within the central nervous system (CNS). This breadth presents particular challenges, as nascent processes must navigate across the CNS–PNS boundary and coalesce into a tightly intermingled wiring pattern, thereby enabling reliable integration from the PNS to the CNS and back. In the auditory system, feedforward spiral ganglion neurons (SGNs) from the periphery collect sound information via tonotopically organized connections in the cochlea and transmit this information to the brainstem for processing via the VIII cranial nerve. In turn, feedback olivocochlear neurons (OCNs) housed in the auditory brainstem send projections into the periphery, also through the VIII nerve. OCNs are motor neuron‐like efferent cells that influence auditory processing within the cochlea and protect against noise damage in adult animals. These aligned feedforward and feedback systems develop in parallel, with SGN central axons reaching the developing auditory brainstem around the same time that the OCN axons extend out toward the developing inner ear. Recent findings have begun to unravel the genetic and molecular mechanisms that guide OCN development, from their origins in a generic pool of motor neuron precursors to their specialized roles as modulators of cochlear activity. One recurrent theme is the importance of efferent–afferent interactions, as afferent SGNs guide OCNs to their final locations within the sensory epithelium, and efferent OCNs shape the activity of the developing auditory system. This article is categorized under: Nervous System Development > Vertebrates: Regional Development

Organization of the mammalian olivocochlear efferent system. Auditory information transduced by inner (IHCs) and outer hair cells (OHCs) is conveyed to the auditory brainstem via Type I and Type II spiral ganglion neurons (SGNs), respectively. SGNs project into the brain via the VIII nerve and synapse onto neurons in the cochlear nuclear complex (CNC). The superior olivary complex (SOC, dashed circle) contains multiple nuclei involved in sound localization, including the medial superior olive (MSO), lateral superior olive (LSO), ventral nucleus of the trapezoid body (VNTB), lateral nucleus of the trapezoid body (LNTB), medial nucleus of the trapezoid body (MNTB), and the superior periolivary nucleus (SPN). Medial (MOCs) and lateral (LOCs) olivocochlear neurons reside primarily in VNTB and LSO, respectively, and project back to the sensory epithelium via the VIII nerve. Other types of neurons are also housed in VNTB and LSO, including the neurons that mediate afferent responses, but only MOCs and LOCs are indicated for simplicity. Within the cochlea, LOCs form synapses with Type I SGNs, whereas MOCs terminate on OHCs

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Development and refinement of cochlear wiring in the mouse. (a) By P0, MOCs have arrived in the vicinity of IHCs. Both Type I and Type II SGNs have projected to IHCs and OHCs, respectively. Between P0 and P4, both MOC neurons and Type I SGNs form synapses with IHCs, while Type II SGNs form connections with OHCs. The MOC axons then grow on toward the OHC region. At least some of these fibers appear to be branches from MOC axons in the IHC region. Over the next two weeks, both SGNs and MOCs prune excess synapses. By adulthood, MOCs project exclusively to OHCs. (b) Development of IHC synapses. At P0, both Type I SGN and MOC projections are present at the IHC surface. Although synaptic machinery is present in IHCs, many components are not yet localized to the cell membrane. Synaptogenesis proceeds over the next several days, and by P4 all IHCs respond to MOC stimulation. The arrival of MOC terminals coincides with the expression of SK2 calcium‐gated potassium channels and α9/α10 nicotinic acetylcholine receptors (nAChR) in IHCs. Ribbon synapses (purple) presynaptic to Type I SGNs also mature over this time period. By adulthood, both MOC terminals and their postsynaptic receptors in IHCs have been eliminated. LOCs also innervate the cochlea during this period (not shown)

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Organization and growth of OCN and SGN projections in the cochlea. (a) Organization of the mature cochlea. MOC axons project along the intraganglionic spiral bundle (IGSB) before turning to branch among the OHC layers. LOCs also travel within the IGSB before turning to the IHC layer. LOCs either turn unilaterally or branch to spiral on either side of IHCs in the inner spiral bundle (ISB) and tunnel spiral bundle (TSB). MOC and LOC neuron traces inspired by Brown, . (b) E17.5 mouse cochlea showing OCNs (red) and SGNs (white). OCNs appear to grow along SGN axons, as indicated by the close association between OCNs and SGNs and the way incoming OCN projections lag behind extending SGN peripheral axons. Image provided by N. Druckenbrod

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Transcription factors driving the production of FBMNs and IEEs. FBMNs and IEEs arise in the fourth rhombomere (r4), which is specified by an autoregulatory Hoxb1/b2 network. Within the pMNv domain of r4, SHH induces expression of a suite of transcription factors (gray box), including Nkx2‐2, Nkx2‐9, Nkx6‐1, and Nkx6‐2 that direct a branchiovisceral motor neuron (MN) fate. The presence of Hoxb1 and Nkx factors collectively induce Phox2b, which is subsequently maintained in branchiovisceral precursors, including those that become IEEs or FBMNs. Within r4, Nkx6 factors are required for the maintenance (but not the onset) of Hoxb1 expression (gray arrow). In branchiovisceral precursors, Phox2b drives expression of early markers of visceral and branchial MN identity, including Phox2a, Isl1, and Chat. In addition, Nkx6‐1 and Ascl1 expression persists after the MNv progenitors exit the cell cycle and become branchiovisceral precursors. Within this pool of precursors, those that will become IEEs likely deviate from an FBMN fate due to the expression of Gata2/3. Together, Phox2b and Hoxb1 drive expression of Gata2, which in turn drives expression of Gata3. Ascl1 remains active in postimitotic IEEs (but not FBMNs) until about E12.5 and influences the level of Gata3 expression. Many of these transcription factors impinge on each other and on common cassettes of gene expression, with some acting at multiple stages and in multiple ways. For simplicity, only the key transcriptional interactions that drive the specification and differentiation of IEEs are shown. See Table for additional details regarding the specific contributions of each factor

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Cell body movements of inner ear efferents (IEEs) and facial branchial motor neurons (FBMNs) during mouse embryogenesis. (a) As shown in a sagittal view, FBMNs and IEEs both derive from a common pool of visceral motor neuron (MNv) progenitors in rhombomere 4 (r4). During embryogenesis, FBMNs move caudally. IEEs gradually separate into distinct subtypes and migrate to their final positions in r4 and r5. Rostral is left and dorsal is up. LOC = lateral olivocochlear neuron; MOC = medial olivocochlear neuron; VEN = vestibular efferent neuron. (b) Starting around E9, IEEs and FBMNs begin to differentiate from a shared pool of cells in the progenitor domain of visceral motor neurons (pMNv), directly adjacent to the floor plate (FP), illustrated in a transverse view of r4. As they develop, immature neurons exit the cell cycle and migrate from the ventricular zone (VZ) to the mantle zone (MZ). By E10.5, IEEs and FBMNs have begun to separate: FBMN cell bodies migrate caudally (see (a)), while IEEs begin to send projections (or translocate) across the floor plate. Both FBMNs and IEEs also begin extending projections to the periphery via the VII and VIII nerves. By E13.5, FBMNs and IEEs have fully separated, and olivocochlear neurons (OCNs) have separated from VENs. OCNs migrate toward the pial surface whereas VENs migrate dorsally. Some other hindbrain neurons derive from progenitors in the rhombic lip (RL)

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References

Abdul Wahab,, N. A., Wahab,, S., Abdul Rahman,, A. H., Sidek,, D., & Zakaria,, M. N. (2016). The hyperactivity of efferent auditory system in patients with schizophrenia: A transient evoked otoacoustic emissions study. Psychiatry Investigation, 13(1), 82–88. https://doi.org/10.4306/pi.2016.13.1.82
Ahn,, D., Ruvinsky,, I., Oates,, A. C., Silver,, L. M., & Ho,, R. K. (2000). tbx20, a new vertebrate T‐box gene expressed in the cranial motor neurons and developing cardiovascular structures in zebrafish. Mechanisms of Development, 95(1–2), 253–258. https://doi.org/10.1016/S0925-4773(00)00346-4
Altieri,, S. C., Jalabi,, W., Zhao,, T., Romito‐DiGiacomo,, R. R., & Maricich,, S. M. (2015). En1 directs superior olivary complex neuron positioning, survival, and expression of FoxP1. Developmental Biology, 408(1), 99–108. https://doi.org/10.1016/j.ydbio.2015.10.008
Appler,, J. M., & Goodrich,, L. V. (2011). Connecting the ear to the brain: Molecular mechanisms of auditory circuit assembly. Progress in Neurobiology, 93(4), 488–508. https://doi.org/10.1016/j.pneurobio.2011.01.004
Appler,, J. M., Lu,, C. C., Druckenbrod,, N. R., Yu,, W.‐M., Koundakjian,, E. J., & Goodrich,, L. V. (2013). Gata3 is a critical regulator of cochlear wiring. The Journal of Neuroscience, 33(8), 3679–3691. https://doi.org/10.1523/JNEUROSCI.4703-12.2013
Auclair,, F., Valdés,, N., & Marchand,, R. (1996). Rhombomere‐specific origin of branchial and visceral motoneurons of the facial nerve in the rat embryo. The Journal of Comparative Neurology, 369(3), 451–461. https://doi.org/10.1002/(SICI)1096-9861(19960603)369:3%3C451::AID-CNE9%3E3.0.CO;2-4
Bell,, E., Lumsden,, A., & Graham,, A. (1999). Expression of GATA‐2 in the developing avian rhombencephalon. Mechanisms of Development, 84(1–2), 173–176. https://doi.org/10.1016/S0925-4773(99)00070-2
Bell,, E., Wingate,, R. J. T., & Lumsden,, A. (1999). Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science, 284(5423), 2168–2171. https://doi.org/10.1126/science.284.5423.2168
Bennetto,, L., Keith,, J. M., Allen,, P. D., & Luebke,, A. E. (2017). Children with autism spectrum disorder have reduced otoacoustic emissions at the 1 kHz mid‐frequency region. Autism Research, 10(2), 337–345. https://doi.org/10.1002/aur.1663
Beutner,, D., & Moser,, T. (2001). The presynaptic function of mouse cochlear inner hair cells during development of hearing. The Journal of Neuroscience, 21(13), 4593–4599. https://doi.org/10.1523/JNEUROSCI.21-13-04593.2001
Bingham,, S., Higashijima,, S., Okamoto,, H., & Chandrasekhar,, A. (2002). The zebrafish trilobite gene is essential for tangential migration of branchiomotor neurons. Developmental Biology, 242(2), 149–160. https://doi.org/10.1006/dbio.2001.0532
Bingham,, S. M., Sittaramane,, V., Mapp,, O., Patil,, S., Prince,, V. E., & Chandrasekhar,, A. (2009). Multiple mechanisms mediate motor neuron migration in the zebrafish hindbrain. Developmental Neurobiology, 70(2), 87–99. https://doi.org/10.1002/dneu.20761
Blankenship,, A. G., & Feller,, M. B. (2010). Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nature Reviews. Neuroscience, 11(1), 18–29. https://doi.org/10.1038/nrn2759
Boord,, R. L. (1961). The efferent cochlear bundle in the caiman and pigeon. Experimental Neurology, 3(3), 225–239. https://doi.org/10.1016/0014-4886(61)90014-0
Brandt,, N., Kuhn,, S., Munkner,, S., Braig,, C., Winter,, H., Blin,, N., … Engel,, J. (2007). Thyroid hormone deficiency affects postnatal spiking activity and expression of Ca²⁺ and K⁺ channels in rodent inner hair cells. The Journal of Neuroscience, 27(12), 3174–3186. https://doi.org/10.1523/JNEUROSCI.3965-06.2007
Briscoe,, J., Pierani,, A., Jessell,, T. M., & Ericson,, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell, 101(4), 435–445. https://doi.org/10.1016/S0092-8674(00)80853-3
Briscoe,, J., Sussel,, L., Serup,, P., Hartigan‐O`Connor,, D., Jessell,, T. M., Rubenstein,, J. L. R., & Ericson,, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded sonic hedgehog signalling. Nature, 398(6728), 622–627. https://doi.org/10.1038/19315
Brown,, M. C. (2011). Anatomy of olivocochlear neurons. In D. K. Ryugo,, R. R. Fay,, & A. N. Popper, (Eds.), Auditory and vestibular efferents (pp. 17‐37). New York, NY: Springer. https://doi.org/10.1007/978‐1‐4419‐7070‐1
Brown,, M. C., & Levine,, J. L. (2008). Dendrites of medial olivocochlear neurons in mouse. Neuroscience, 154(1), 147–159. https://doi.org/10.1016/j.neuroscience.2007.12.045
Brown,, M. C., & Nuttall,, A. L. (1984). Efferent control of cochlear inner hair cell responses in the guinea‐pig. The Journal of Physiology, 354, 625–646.
Bruce,, L. L., Christensen,, M. A., & Warr,, W. B. (2000). Postnatal development of efferent synapses in the rat cochlea. The Journal of Comparative Neurology, 423(3), 532–548. https://doi.org/10.1002/1096-9861(20000731)423:3%3C532::AID-CNE14%3E3.0.CO;2-T
Bruce,, L. L., Kingsley,, J., Nichols,, D. H., & Fritzsch,, B. (1997). The development of vestibulocochlear efferents and cochlear afferents in mice. International Journal of Developmental Neuroscience, 15(4–5), 671–692. https://doi.org/10.1016/S0736-5748(96)00120-7
Campbell,, J., & Henson,, M. (1988). Olivocochlear neurons in the brainstem of the mouse. Hearing Research, 35(2–3), 271–274. https://doi.org/10.1016/0378-5955(88)90124-4
Carney,, P. R., & Silver,, J. (1983). Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. The Journal of Comparative Neurology, 215(4), 359–369. https://doi.org/10.1002/cne.902150402
Chandrasekhar,, A. (2004). Turning heads: Development of vertebrate branchiomotor neurons. Developmental Dynamics, 229(1), 143–161. https://doi.org/10.1002/dvdy.10444
Clause,, A., Kim,, G., Sonntag,, M., Weisz,, C. J. C., Vetter,, D. E., Rűbsamen,, R., & Kandler,, K. (2014). The precise temporal pattern of prehearing spontaneous activity is necessary for tonotopic map refinement. Neuron, 82(4), 822–835. https://doi.org/10.1016/j.neuron.2014.04.001
Cole,, K. S., & Robertson,, D. (1992). Early efferent innervation of the developing rat cochlea studied with a carbocyanine dye. Brain Research, 575(2), 223–230. https://doi.org/10.1016/0006-8993(92)90083-L
Collet,, L., Roge,, B., Descouens,, D., Moron,, P., Duverdy,, F., & Urgell,, H. (1993). Objective auditory dysfunction in infantile autism. Lancet, 342(8876), 923–924. https://doi.org/10.1016/0140-6736(93)91969-S
Coppola,, E., Pattyn,, A., Guthrie,, S. C., Goridis,, C., & Studer,, M. (2005). Reciprocal gene replacements reveal unique functions for Phox2 genes during neural differentiation. The EMBO Journal, 24(24), 4392–4403. https://doi.org/10.1038/sj.emboj.7600897
Cowan,, C. A., Yokoyama,, N., Bianchi,, L. M., Henkemeyer,, M., & Fritzsch,, B. (2000). EphB2 guides axons at the midline and is necessary for normal vestibular function. Neuron, 26(2), 417–430. https://doi.org/10.1016/S0896-6273(00)81174-5
Cramer,, K. S., & Gabriele,, M. L. (2014). Axon guidance in the auditory system: Multiple functions of Eph receptors. Neuroscience, 277, 152–162. https://doi.org/10.1016/j.neuroscience.2014.06.068
Darrow,, K. N., Maison,, S. F., & Liberman,, M. C. (2006). Cochlear efferent feedback balances interaural sensitivity. Nature Neuroscience, 9(12), 1474–1476. https://doi.org/10.1038/nn1807
Darrow,, K. N., Maison,, S. F., & Liberman,, M. C. (2007). Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. Journal of Neurophysiology, 97(2), 1775–1785. https://doi.org/10.1152/jn.00955.2006
Darrow,, K. N., Simons,, E. J., Dodds,, L., & Liberman,, M. C. (2006). Dopaminergic innervation of the mouse inner ear: Evidence for a separate cytochemical group of cochlear efferent fibers. The Journal of Comparative Neurology, 498(3), 403–414. https://doi.org/10.1002/cne.21050
Davey,, C. F., Mathewson,, A. W., & Moens,, C. B. (2016). PCP signaling between migrating neurons and their planar‐polarized neuroepithelial environment controls filopodial dynamics and directional migration. PLoS Genetics, 12(3), e1005934. https://doi.org/10.1371/journal.pgen.1005934
Davey,, C. F., & Moens,, C. B. (2017). Planar cell polarity in moving cells: Think globally, act locally. Development, 144(2), 187–200. https://doi.org/10.1242/dev.122804
Delacroix,, L., & Malgrange,, B. (2015). Cochlear afferent innervation development. Hearing Research, 330, 157–169. https://doi.org/10.1016/j.heares.2015.07.015
Dennis,, D. J., Han,, S., & Schuurmans,, C. (2018). bHLH transcription factors in neural development, disease, and reprogramming. Brain Research. https://doi.org/10.1016/j.brainres.2018.03.013
Dessaud,, E., McMahon,, A. P., & Briscoe,, J. (2008). Pattern formation in the vertebrate neural tube: A sonic hedgehog morphogen‐regulated transcriptional network. Development, 135(15), 2489–2503. https://doi.org/10.1242/dev.009324
Dewson,, J. H. (1967). Olivocochlear bundle: Relationships to signal discrimination in noise. The Journal of the Acoustical Society of America, 42(5), 1189–1189. https://doi.org/10.1121/1.2144106
Di Bonito,, M., Narita,, Y., Avallone,, B., Sequino,, L., Mancuso,, M., Andolfi,, G., … Studer,, M. (2013). Assembly of the auditory circuitry by a Hox genetic network in the mouse brainstem. PLoS Genetics, 9(2), e1003249. https://doi.org/10.1371/journal.pgen.1003249
Di Bonito,, M., & Studer,, M. (2017). Cellular and molecular underpinnings of neuronal assembly in the central auditory system during mouse development. Frontiers in Neural Circuits, 11, 1–25. https://doi.org/10.3389/fncir.2017.00018
Dubreuil,, V., Hirsch,, M.‐R., Jouve,, C., Brunet,, J.‐F., & Goridis,, C. (2002). The role of Phox2b in synchronizing pan‐neuronal and type‐specific aspects of neurogenesis. Development, 129(22), 5241–5253.
Dubreuil,, V., Hirsch,, M. R., Pattyn,, A., Brunet,, J. F., & Goridis,, C. (2000). The Phox2b transcription factor coordinately regulates neuronal cell cycle exit and identity. Development, 127(23), 5191–5201.
Dulon,, D., & Lenoir,, M. (1996). Cholinergic responses in developing outer hair cells of the rat cochlea. The European Journal of Neuroscience, 8(9), 1945–1952. https://doi.org/10.1111/j.1460-9568.1996.tb01338.x
Dulon,, D., Luo,, L., Zhang,, C., & Ryan,, A. F. (1998). Expression of small‐conductance calcium‐activated potassium channels (SK) in outer hair cells of the rat cochlea. The European Journal of Neuroscience, 10(3), 907–915. https://doi.org/10.1046/j.1460-9568.1998.00098.x
Duncan,, J. S., & Fritzsch,, B. (2013). Continued expression of GATA3 is necessary for cochlear neurosensory development. Reh TA, ed. PLoS One, 8(4), e62046. https://doi.org/10.1371/journal.pone.0062046
Duncan,, J. S., Lim,, K.‐C., Engel,, J. D., & Fritzsch,, B. (2011). Limited inner ear morphogenesis and neurosensory development are possible in the absence of GATA3. The International Journal of Developmental Biology, 55(3), 297–303. https://doi.org/10.1387/ijdb.103178jd
Echteler,, S. M. (1992). Developmental segregation in the afferent projections to mammalian auditory hair cells. Proceedings of the National Academy of Sciences of the United States of America, 89(14), 6324–6327. https://doi.org/10.1073/pnas.89.14.6324
Ehret,, G. (1976). Development of absolute auditory thresholds in the house mouse (Mus musculus). Journal of the American Audiology Society, 1(5), 179–184.
Elgoyhen,, A. B., Johnson,, D. S., Boulter,, J., Vetter,, D. E., & Heinemann,, S. (1994). α9: An acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell, 79(4), 705–715. https://doi.org/10.1016/0092-8674(94)90555-X
Elgoyhen,, A. B., & Katz,, E. (2012). The efferent medial olivocochlear‐hair cell synapse. The Journal of Physiology, 106(1–2), 47–56. https://doi.org/10.1016/j.jphysparis.2011.06.001
Elgoyhen,, A. B., Vetter,, D. E., Katz,, E., Rothlin,, C. V., Heinemann,, S. F., & Boulter,, J. (2001). α10: A determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proceedings of the National Academy of Sciences of the United States of America, 98(6), 3501–3506. https://doi.org/10.1073/pnas.051622798
Elliott,, K. L., & Fritzsch,, B. (2010). Transplantation of Xenopus laevis ears reveals the ability to form afferent and efferent connections with the spinal cord. The International Journal of Developmental Biology, 54(10), 1443–1451. https://doi.org/10.1387/ijdb.103061ke
Elliott,, K. L., Houston,, D. W., & Fritzsch,, B. (2013). Transplantation of Xenopus laevis tissues to determine the ability of motor neurons to acquire a novel target. PLoS One, 8(2), e55541. https://doi.org/10.1371/journal.pone.0055541
Ericson,, J., Rashbass,, P., Schedl,, A., Brenner‐Morton,, S., Kawakami,, A., van Heyningen,, V., … Briscoe,, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell, 90(1), 169–180. https://doi.org/10.1016/S0092-8674(00)80323-2
Ericson,, J., Thor,, S., Edlund,, T., Jessell,, T., & Yamada,, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet‐1. Science, 256(5063), 1555–1560. https://doi.org/10.1126/science.1350865
Ernfors,, P., Van De Water,, T., Loring,, J., & Jaenisch,, R. (1995). Complementary roles of BDNF and NT‐3 in vestibular and auditory development. Neuron, 14(6), 1153–1164. https://doi.org/10.1016/0896-6273(95)90263-5
Eybalin,, M. (1993). Neurotransmitters and neuromodulators of the mammalian cochlea. Physiological Reviews, 73(2), 309–373. https://doi.org/10.1152/physrev.1993.73.2.309
Farago,, A. F., Awatramani,, R. B., & Dymecki,, S. M. (2006). Assembly of the brainstem cochlear nuclear complex is revealed by intersectional and subtractive genetic fate maps. Neuron, 50(2), 205–218. https://doi.org/10.1016/j.neuron.2006.03.014
Flores,, E. N., Duggan,, A., Madathany,, T., Hogan,, A. K., Márquez,, F. G., Kumar,, G., … García‐Añoveros,, J. (2015). A non‐canonical pathway from cochlea to brain signals tissue‐damaging noise. Current Biology, 25(5), 606–612. https://doi.org/10.1016/j.cub.2015.01.009
Fraser,, S., Keynes,, R., & Lumsden,, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature, 344(6265), 431–435. https://doi.org/10.1038/344431a0
Fritzsch,, B. (1996). Development of the labyrinthine efferent system. Annals of the New York Academy of Sciences, 781(2), 21–33.
Fritzsch,, B., Barbacid,, M., & Silos‐Santiago,, I. (1998). The combined effects of trkB and trkC mutations on the innervation of the inner ear. International Journal of Developmental Neuroscience, 16(6), 493–505. https://doi.org/10.1016/S0736-5748(98)00043-4
Fritzsch,, B., Christensen,, M. A., & Nichols,, D. H. (1993). Fiber pathways and positional changes in efferent perikarya of 2.5‐to 7‐day chick embryos as revealed with dil and dextran amiens. Journal of Neurobiology, 24(11), 1481–1499. https://doi.org/10.1002/neu.480241104
Fritzsch,, B., & Elliott,, K. L. (2017). Evolution and development of the inner ear efferent system: Transforming a motor neuron population to connect to the most unusual motor protein via ancient nicotinic receptors. Frontiers in Cellular Neuroscience, 11(April), 1–9. https://doi.org/10.3389/fncel.2017.00114
Fritzsch,, B., & Nichols,, D. H. (1993). DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Hearing Research, 65(1–2), 51–60. https://doi.org/10.1016/0378‐5955(93)90200‐K
Froud,, K. E., Wong,, A. C. Y., Cederholm,, J. M. E., Klugmann,, M., Sandow,, S. L., Julien,, J. P., … Housley,, G. D. (2015). Type II spiral ganglion afferent neurons drive medial olivocochlear reflex suppression of the cochlear amplifier. Nature Communications, 6(1), 7115. https://doi.org/10.1038/ncomms8115
Fu,, B., Le Prell,, C., Simmons,, D., Lei,, D., Schrader,, A., Chen,, A. B., & Bao,, J. (2010). Age‐related synaptic loss of the medial olivocochlear efferent innervation. Molecular Neurodegeneration, 5(1), 53. https://doi.org/10.1186/1750-1326-5-53
Fujiyama,, T., Yamada,, M., Terao,, M., Terashima,, T., Hioki,, H., Inoue,, Y. U., … Hoshino,, M. (2009). Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development, 136(12), 2049–2058. https://doi.org/10.1242/dev.033480
Gallarda,, B. W., Bonanomi,, D., Muller,, D., Brown,, A., Alaynick,, W. A., Andrews,, S. E., … Marquardt,, T. (2008). Segregation of axial motor and sensory pathways via heterotypic trans‐axonal signaling. Science, 320(5873), 233–236. https://doi.org/10.1126/science.1153758
Garel,, S., Garcia‐Dominguez,, M., & Charnay,, P. (2000). Control of the migratory pathway of facial branchiomotor neurones. Development, 127(24), 5297–5307.
Gaufo,, G. O., Flodby,, P., & Capecchi,, M. R. (2000). Hoxb1 controls effectors of sonic hedgehog and Mash1 signaling pathways. Development, 127(24), 5343–5354.
Ghosh,, A., Antonini,, A., McConnell,, S. K., & Shatz,, C. J. (1990). Requirement for subplate neurons in the formation of thalamocortical connections. Nature, 347(6289), 179–181. https://doi.org/10.1038/347179a0
Giraud,, A. L., Garnier,, S., Micheyl,, C., Lina,, G., Chays,, A., & Chéry‐Croze,, S. (1997). Auditory efferents involved in speech‐in‐noise intelligibility. Neuroreport, 8(7), 1779–1783. https://doi.org/10.1097/00001756-199705060-00042
Glasco,, D. M., Pike,, W., Qu,, Y., Reustle,, L., Misra,, K., di Bonito,, M., … Chandrasekhar,, A. (2016). The atypical cadherin Celsr1 functions non‐cell autonomously to block rostral migration of facial branchiomotor neurons in mice. Developmental Biology, 417(1), 40–49. https://doi.org/10.1016/j.ydbio.2016.07.004
Glasco,, D. M., Sittaramane,, V., Bryant,, W., Fritzsch,, B., Sawant,, A., Paudyal,, A., … Chandrasekhar,, A. (2012). The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. Developmental Biology, 369(2), 211–222. https://doi.org/10.1016/j.ydbio.2012.06.021
Glowatzki,, E., & Fuchs,, P. A. (2000). Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science, 288(5475), 2366–2368. https://doi.org/10.1126/science.288.5475.2366
Goddard,, J. M., Rossel,, M., Manley,, N. R., & Capecchi,, M. R. (1996). Mice with targeted disruption of Hoxb‐1 fail to form the motor nucleus of the VIIth nerve. Development, 122(10), 3217–3228.
Goffinet,, A. M. (1984). Abnormal development of the facial nerve nucleus in reeler mutant mice. Journal of Anatomy, 138(2), 207–215.
Gómez‐Casati,, M. E., Wedemeyer,, C., Taranda,, J., Lipovsek,, M., Dalamon,, V., Elgoyhen,, A. B., & Katz,, E. (2009). Electrical properties and functional expression of ionic channels in cochlear inner hair cells of mice lacking the α10 nicotinic cholinergic receptor subunit. Journal of the Association for Research in Otolaryngology, 10(2), 221–232. https://doi.org/10.1007/s10162-009-0164-0
Goodrich,, L. V. (2016). In A. Dabdoub,, B. Fritzsch,, A. N. Popper,, & R. R. Fay, (Eds.), The primary auditory neurons of the mammalian cochlea (Vol. 52). New York, NY: Springer. https://doi.org/10.1007/978-1-4939-3031-9
Goutman,, J. D., Fuchs,, P. A., & Glowatzki,, E. (2005). Facilitating efferent inhibition of inner hair cells in the cochlea of the neonatal rat. The Journal of Physiology, 566(1), 49–59. https://doi.org/10.1113/jphysiol.2005.087460
Groff,, J. A., & Liberman,, M. C. (2003). Modulation of cochlear afferent response by the lateral olivocochlear system: Activation via electrical stimulation of the inferior colliculus. Journal of Neurophysiology, 90(5), 3178–3200. https://doi.org/10.1152/jn.00537.2003
Grothe,, B., Pecka,, M., & McAlpine,, D. (2010). Mechanisms of sound localization in mammals. Physiological Reviews, 90(3), 983–1012. https://doi.org/10.1152/physrev.00026.2009
Guinan,, J. J. (2006). Olivocochlear efferents: Anatomy, physiology, function, and the measurement of efferent effects in humans. Ear and Hearing, 27(6), 589–607. https://doi.org/10.1097/01.aud.0000240507.83072.e7
Guinan,, J. J. (2010). Cochlear efferent innervation and function. Current Opinion in Otolaryngology %26 Head and Neck Surgery, 18(5), 447–453. https://doi.org/10.1097/MOO.0b013e32833e05d6
Guinan,, J. J. (2018). Olivocochlear efferents: Their action, effects, measurement and uses, and the impact of the new conception of cochlear mechanical responses. Hearing Research, 362, 38–47. https://doi.org/10.1016/j.heares.2017.12.012
Guinan,, J. J., Norris,, B. E., & Guinan,, S. S. (1972). Single auditory units in the superior olivary complex: II: Locations of unit categories and tonotopic organization. The International Journal of Neuroscience, 4(4), 147–166. https://doi.org/10.3109/00207457209164756
Gummer,, A. W., & Mark,, R. F. (1994). Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii). Neuroreport, 5(6), 685–688.
Guthrie,, S. (2007). Patterning and axon guidance of cranial motor neurons. Nature Reviews. Neuroscience, 8(11), 859–871. https://doi.org/10.1038/nrn2254
Hammond,, R., Vivancos,, V., Naeem,, A., Chilton,, J., Mambitisaeva,, E., Andrews,, W., … Guthrie,, S. (2005). Slit‐mediated repulsion is a key regulator of motor axon pathfinding inthe hindbrain. Development, 132(20), 4483–4495. https://doi.org/10.1242/dev.02038
He,, D. Z. Z. (1997). Relationship between the development of outer hair cell electromotility and efferent innervation: A study in cultured organ of corti of neonatal gerbils. The Journal of Neuroscience, 17(10), 3634–3643. https://doi.org/10.1523/JNEUROSCI.17-10-03634.1997
He,, D. Z. Z., Cheatham,, M. A., Pearce,, M., & Vetter,, D. E. (2004). Mouse outer hair cells lacking the α9 ACh receptor are motile. Developmental Brain Research, 148(1), 19–25. https://doi.org/10.1016/j.devbrainres.2003.10.003
He,, D. Z. Z., Evans,, B. N., & Dallos,, P. (1994). First appearance and development of electromotility in neonatal gerbil outer hair cells. Hearing Research, 78(1), 77–90. https://doi.org/10.1016/0378-5955(94)90046-9
Hickman,, T. T., Liberman,, M. C., & Jacob,, M. H. (2015). Adenomatous polyposis coli protein deletion in efferent olivocochlear neurons perturbs afferent synaptic maturation and reduces the dynamic range of hearing. The Journal of Neuroscience, 35(24), 9236–9245. https://doi.org/10.1523/JNEUROSCI.4384-14.2015
Higashijima,, S., Hotta,, Y., & Okamoto,, H. (2000). Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet‐1 promoter/enhancer. The Journal of Neuroscience, 20(1), 206–218. https://doi.org/10.1523/JNEUROSCI.20-01-00206.2000
Huang,, E. J., Liu,, W., Fritzsch,, B., Bianchi,, L. M., Reichardt,, L. F., & Xiang,, M. (2001). Brn3a is a transcriptional regulator of soma size, target field innervation and axon pathfinding of inner ear sensory neurons. Development, 128(13), 2421–2432.
Irving,, S., Moore,, D. R., Liberman,, M. C., & Sumner,, C. J. (2011). Olivocochlear efferent control in sound localization and experience‐dependent learning. The Journal of Neuroscience, 31(7), 2493–2501. https://doi.org/10.1523/JNEUROSCI.2679-10.2011
Jacob,, J., Ferri,, A. L., Milton,, C., Prin,, F., Pla,, P., Lin,, W., … Briscoe,, J. (2007). Transcriptional repression coordinates the temporal switch from motor to serotonergic neurogenesis. Nature Neuroscience, 10(11), 1433–1439. https://doi.org/10.1038/nn1985
Jarrar,, W., Dias,, J. M., Ericson,, J., Arnold,, H.‐H., & Holz,, A. (2015). Nkx2.2 and Nkx2.9 are the key regulators to determine cell fate of branchial and visceral motor neurons in caudal hindbrain. PLoS One, 10(4), e0124408. https://doi.org/10.1371/journal.pone.0124408
Jessell,, T. M. (2000). Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nature Reviews. Genetics, 1(1), 20–29. https://doi.org/10.1038/35049541
Jessen,, J. R., Topczewski,, J., Bingham,, S., Sepich,, D. S., Marlow,, F., Chandrasekhar,, A., & Solnica‐Krezel,, L. (2002). Zebrafish trilobite identifies new roles for strabismus in gastrulation and neuronal movements. Nature Cell Biology, 4(8), 610–615. https://doi.org/10.1038/ncb828
Johnson,, S. L., Eckrich,, T., Kuhn,, S., Zampini,, V., Franz,, C., Ranatunga,, K. M., … Marcotti,, W. (2011). Position‐dependent patterning of spontaneous action potentials in immature cochlear inner hair cells. Nature Neuroscience, 14(6), 711–717. https://doi.org/10.1038/nn.2803
Johnson,, S. L., Wedemeyer,, C., Vetter,, D. E., Adachi,, R., Holley,, M. C., Elgoyhen,, A. B., & Marcotti,, W. (2013). Cholinergic efferent synaptic transmission regulates the maturation of auditory hair cell ribbon synapses. Open Biology, 3(11), 130163. https://doi.org/10.1098/rsob.130163
Jungbluth,, S., Bell,, E., & Lumsden,, A. (1999). Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development, 126(12), 2751–2758.
Kaf,, W. A., & Danesh,, A. A. (2013). Distortion‐product otoacoustic emissions and contralateral suppression findings in children with Asperger`s syndrome. International Journal of Pediatric Otorhinolaryngology, 77(6), 947–954. https://doi.org/10.1016/j.ijporl.2013.03.014
Kaiser,, A., Alexandrova,, O., & Grothe,, B. (2011). Urocortin‐expressing olivocochlear neurons exhibit tonotopic and developmental changes in the auditory brainstem and in the innervation of the cochlea. The Journal of Comparative Neurology, 519(14), 2758–2778. https://doi.org/10.1002/cne.22650
Kandler,, K., Clause,, A., & Noh,, J. (2009). Tonotopic reorganization of developing auditory brainstem circuits. Nature Neuroscience, 12(6), 711–717. https://doi.org/10.1038/nn.2332
Kanold,, P. O. (2004). Transient microcircuits formed by subplate neurons and their role in functional development of thalamocortical connections. Neuroreport, 15(14), 2149–2153. https://doi.org/10.1097/00001756-200410050-00001
Karis,, A., Pata,, I., van Doorninck,, J. H., Grosveld,, F., de Zeeuw,, C. I., de Caprona,, D., & Fritzsch,, B. (2001). Transcription factor GATA‐3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. The Journal of Comparative Neurology, 429(4), 615–630. https://doi.org/10.1002/1096-9861(20010122)429:4%3C615::AID-CNE8%3E3.0.CO;2-F
Katayama,, K., Zine,, A., Ota,, M., Matsumoto,, Y., Inoue,, T., Fritzsch,, B., & Aruga,, J. (2009). Disorganized innervation and neuronal loss in the inner ear of Slitrk6‐deficient mice. PLoS One, 4(11), e7786. https://doi.org/10.1371/journal.pone.0007786
Katz,, E., Elgoyhen,, A. B., Gómez‐Casati,, M. E., Knipper,, M., Vetter,, D. E., Fuchs,, P. A., & Glowatzki,, E. (2004). Developmental regulation of nicotinic synapses on cochlear inner hair cells. The Journal of Neuroscience, 24(36), 7814–7820. https://doi.org/10.1523/JNEUROSCI.2102-04.2004
Khalfa,, S., Bruneau,, N., Rogé,, B., Georgieff,, N., Veuillet,, E., Adrien,, J. L., … Collet,, L. (2001). Peripheral auditory asymmetry in infantile autism. The European Journal of Neuroscience, 13(3), 628–632. https://doi.org/10.1046/j.1460-9568.2001.01423.x
Kiecker,, C., & Lumsden,, A. (2005). Compartments and their boundaries in vertebrate brain development. Nature Reviews. Neuroscience, 6(7), 553–564. https://doi.org/10.1038/nrn1702
Kim,, K.‐T., Kim,, N., Kim,, H.‐K., Lee,, H., Gruner,, H. N., Gergics,, P., … Song,, M. R. (2016). ISL1‐based LIM complexes control Slit2 transcription in developing cranial motor neurons. Scientific Reports, 6(1), 36491. https://doi.org/10.1038/srep36491
Kim,, M., Fontelonga,, T., Roesener,, A. P., Lee,, H., Gurung,, S., Mendonca,, P. R. F., & Mastick,, G. S. (2015). Motor neuron cell bodies are actively positioned by Slit/Robo repulsion and Netrin/DCC attraction. Developmental Biology, 399(1), 68–79. https://doi.org/10.1016/j.ydbio.2014.12.014
Knudson,, I. M., Shera,, C. A., & Melcher,, J. R. (2014). Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis. Journal of Neurophysiology, 112(12), 3197–3208. https://doi.org/10.1152/jn.00576.2014
Köppl,, C. (2011). Birds – Same thing, but different? Convergent evolution in the avian and mammalian auditory systems provides informative comparative models. Hearing Research, 273(1–2), 65–71. https://doi.org/10.1016/j.heares.2010.03.095
Kraus,, F., Haenig,, B., & Kispert,, A. (2001). Cloning and expression analysis of the mouse T‐box gene Tbx20. Mechanisms of Development, 100(1), 87–91. https://doi.org/10.1016/S0925-4773(00)00499-8
Kros,, C. J., Ruppersberg,, J. P., & Rüsch,, A. (1998). Expression of a potassium current in inner hair cells during development of hearing in mice. Nature, 394(6690), 281–284. https://doi.org/10.1038/28401
Kujawa,, S. G., & Liberman,, M. C. (1997). Conditioning‐related protection from acoustic injury: Effects of chronic deefferentation and sham surgery. Journal of Neurophysiology, 78(6), 3095–3106. https://doi.org/10.1152/jn.1997.78.6.3095
Kulesza,, R. J., Lukose,, R., & Stevens,, L. V. (2011). Malformation of the human superior olive in autistic spectrum disorders. Brain Research, 1367, 360–371. https://doi.org/10.1016/j.brainres.2010.10.015
Kulesza,, R. J., & Mangunay,, K. (2008). Morphological features of the medial superior olive in autism. Brain Research, 1200, 132–137. https://doi.org/10.1016/j.brainres.2008.01.009
Kumar,, U. A., & Vanaja,, C. S. (2004). Functioning of olivocochlear bundle and speech perception in noise. Ear and Hearing, 25(2), 142–146. https://doi.org/10.1097/01.AUD.0000120363.56591.E6
Larsen,, E., & Liberman,, M. C. (2010). Contralateral cochlear effects of ipsilateral damage: No evidence for interaural coupling. Hearing Research, 260(1–2), 70–80. https://doi.org/10.1016/j.heares.2009.11.011
Lauer,, A. M., Fuchs,, P. A., Ryugo,, D. K., & Francis,, H. W. (2012). Efferent synapses return to inner hair cells in the aging cochlea. Neurobiology of Aging, 33(12), 2892–2902. https://doi.org/10.1016/j.neurobiolaging.2012.02.007
Lauer,, A. M., & May,, B. J. (2011). The medial olivocochlear system attenuates the developmental impact of early noise exposure. Journal of the Association for Research in Otolaryngology, 12(3), 329–343. https://doi.org/10.1007/s10162-011-0262-7
Lenoir,, M., Shnerson,, A., & Pujol,, R. (1980). Cochlear receptor development in the rat with emphasis on synaptogenesis. Anatomy and Embryology (Berlin), 160(3), 253–262. https://doi.org/10.1007/BF00305106
Liberman,, L. D., Wang,, H., & Liberman,, M. C. (2011). Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear‐nerve/hair‐cell synapses. The Journal of Neuroscience, 31(3), 801–808. https://doi.org/10.1523/JNEUROSCI.3389-10.2011
Liberman,, M. C. (1978). Auditory‐nerve response from cats raised in a low‐noise chamber. The Journal of the Acoustical Society of America, 63(2), 442–455. https://doi.org/10.1121/1.381736
Liberman,, M. C. (1980a). Morphological differences among radial afferent fibers in the cat cochlea: An electron‐microscopic study of serial sections. Hearing Research, 3(1), 45–63. https://doi.org/10.1016/0378-5955(80)90007-6
Liberman,, M. C. (1980b). Efferent synapses in the inner hair cell area of the cat cochlea: An electron microscopic study of serial sections. Hearing Research, 3(3), 189–204. https://doi.org/10.1016/0378-5955(80)90046-5
Liberman,, M. C. (1990). Effects of chronic cochlear de‐efferentation on auditory‐nerve response. Hearing Research, 49(1–3), 209–223. https://doi.org/10.1016/0378‐5955(90)90105‐X
Liberman,, M. C., Liberman,, L. D., & Maison,, S. F. (2014). Efferent feedback slows cochlear aging. The Journal of Neuroscience, 34(13), 4599–4607. https://doi.org/10.1523/JNEUROSCI.4923-13.2014
Liberman,, M. C., O`Grady,, D. F., Dodds,, L. W., Mcgee,, J., & Walsh,, E. J. (2000). Afferent innervation of outer and inner hair cells is normal in neonatally de‐efferented cats. The Journal of Comparative Neurology, 423(1), 132–139. https://doi.org/10.1002/1096-9861(20000717)423:1%3C132::AID-CNE11%3E3.0.CO;2-7
Liu,, C., Glowatzki,, E., & Fuchs,, P. A. (2015). Unmyelinated type II afferent neurons report cochlear damage. Proceedings of the National Academy of Sciences of the United States of America, 112(47), 14723–14727. https://doi.org/10.1073/pnas.1515228112
Lu,, C. C., Appler,, J. M., Houseman,, E. A., & Goodrich,, L. V. (2011). Developmental profiling of spiral ganglion neurons reveals insights into auditory circuit assembly. The Journal of Neuroscience, 31(30), 10903–10918. https://doi.org/10.1523/JNEUROSCI.2358-11.2011
Lumsden,, A., & Keynes,, R. (1989). Segmental patterns of neuronal development in the chick hindbrain. Nature, 337(6206), 424–428. https://doi.org/10.1038/337424a0
Ma,, Q., Anderson,, D. J., & Fritzsch,, B. (2000). Neurogenin 1 mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. Journal of the Association for Research in Otolaryngology, 1(2), 129–143. https://doi.org/10.1007/s101620010017
Ma,, Q., Chen,, Z., del Barco Barrantes,, I., de la Pompa,, J. L., & Anderson,, D. J. (1998). Neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron, 20(3), 469–482. https://doi.org/10.1016/S0896-6273(00)80988-5
Maison,, S., Liberman,, L. D., & Liberman,, M. C. (2016). Type II cochlear ganglion neurons do not drive the olivocochlear reflex: Re‐examination of the cochlear phenotype in peripherin knock‐out mice. eNeuro, 3(4), 1–11. https://doi.org/10.1523/ENEURO.0207-16.2016
Maison,, S. F., Adams,, J. C., & Liberman,, M. C. (2003). Olivocochlear innervation in the mouse: Immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. The Journal of Comparative Neurology, 455(3), 406–416. https://doi.org/10.1002/cne.10490
Maison,, S. F., Usubuchi,, H., & Liberman,, M. C. (2013). Efferent feedback minimizes cochlear neuropathy from moderate noise exposure. The Journal of Neuroscience, 33(13), 5542–5552. https://doi.org/10.1016/j.pestbp.2011.02.012.Investigations
Malmierca,, M. S., & Ryugo,, D. K. (2012). Auditory system. In C. Watson,, G. Paxinos,, & L. Puelles, (Eds.), The mouse nervous system (pp. 607–645). Cambridge, MA: Academic Press. https://doi.org/10.1016/B978-0-12-369497-3.10024-X
Mapp,, O. M., Walsh,, G. S., Moens,, C. B., Tada,, M., & Prince,, V. E. (2011). Zebrafish Prickle1b mediates facial branchiomotor neuron migration via a farnesylation‐dependent nuclear activity. Development, 138(10), 2121–2132. https://doi.org/10.1242/dev.060442
Mapp,, O. M., Wanner,, S. J., Rohrschneider,, M. R., & Prince,, V. E. (2010). Prickle1b mediates interpretation of migratory cues during zebrafish facial branchiomotor neuron migration. Developmental Dynamics, 239(6), 1596–1608. https://doi.org/10.1002/dvdy.22283
Marcotti,, W., Johnson,, S. L., Holley,, M. C., & Kros,, C. J. (2003). Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. The Journal of Physiology, 548(2), 383–400. https://doi.org/10.1113/jphysiol.2002.034801
Marcotti,, W., Johnson,, S. L., & Kros,, C. J. (2004). A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. The Journal of Physiology, 560(3), 691–708. https://doi.org/10.1113/jphysiol.2004.072868
Marcotti,, W., Johnson,, S. L., Rüsch,, A., & Kros,, C. J. (2003). Sodium and calcium currents shape action potentials in immature mouse inner hair cells. The Journal of Physiology, 552(3), 743–761. https://doi.org/10.1113/jphysiol.2003.043612
Maricich,, S. M., Xia,, A., Mathes,, E. L., Wang,, V. Y., Oghalai,, J. S., Fritzsch,, B., & Zoghbi,, H. Y. (2009). Atoh1‐lineal neurons are required for hearing and for the survival of neurons in the spiral ganglion and brainstem accessory auditory nuclei. The Journal of Neuroscience, 29(36), 11123–11133. https://doi.org/10.1523/JNEUROSCI.2232-09.2009
Marrs,, G. S., Morgan,, W. J., Howell,, D. M., Spirou,, G. A., & Mathers,, P. H. (2013). Embryonic origins of the mouse superior olivary complex. Developmental Neurobiology, 73(5), 384–398. https://doi.org/10.1002/dneu.22069
Marrs,, G. S., & Spirou,, G. A. (2012). Embryonic assembly of auditory circuits: Spiral ganglion and brainstem. The Journal of Physiology, 590(10), 2391–2408. https://doi.org/10.1113/jphysiol.2011.226886
May,, B. J., Lauer,, A. M., & Roos,, M. J. (2011). Impairments of the medial olivocochlear system increase the risk of noise‐induced auditory neuropathy in laboratory mice. Otology %26 Neurotology, 32(9), 1568–1578. https://doi.org/10.1097/MAO.0b013e31823389a1
McConnell,, S., Ghosh,, A., & Shatz,, C. (1989). Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science, 245(4921), 978–982. https://doi.org/10.1126/science.2475909
McKay,, I. J., Lewis,, J., & Lumsden,, A. (1997). Organization and development of facial motor neurons in the Kreisler mutant mouse. The European Journal of Neuroscience, 9(7), 1499–1506. https://doi.org/10.1111/j.1460-9568.1997.tb01504.x
Merchán Pérez,, A., Gil‐Loyzaga,, P., Eybalin,, M., Fernández Mateos,, P., & Bartolomé,, M. V. (1994). Choline‐acetyltransferase‐like immunoreactivitity in the organ of corti of the rat during postnatal development. Developmental Brain Research, 82(1–2), 29–34. https://doi.org/10.1016/0165-3806(94)90145-7
Mulders,, W. H. A., & Robertson,, D. (2004). Dopaminergic olivocochlear neurons originate in the high frequency region of the lateral superior olive of Guinea pigs. Hearing Research, 187(1–2), 122–130. https://doi.org/10.1016/S0378-5955(03)00308-3
Müller,, M., Jabs,, N., Lorke,, D. E., Fritzsch,, B., & Sander,, M. (2003). Nkx6.1 controls migration and axon pathfinding of cranial branchio‐motoneurons. Development, 130(23), 5815–5826. https://doi.org/10.1242/dev.00815
Muniak,, M. A., Rivas,, A., Montey,, K. L., May,, B. J., Francis,, H. W., & Ryugo,, D. K. (2013). 3D model of frequency representation in the cochlear nucleus of the CBA/J mouse. The Journal of Comparative Neurology, 521(7), 1510–1532. https://doi.org/10.1002/cne.23238
Murphy,, P., Davidson,, D. R., & Hill,, R. E. (1989). Segment‐specific expression of a homoeobox‐containing gene in the mouse hindbrain. Nature, 341(6238), 156–159. https://doi.org/10.1038/341156a0
Nakamura,, P. A., & Cramer,, K. S. (2011). Formation and maturation of the calyx of Held. Hearing Research, 276(1–2), 70–78. https://doi.org/10.1016/j.heares.2010.11.004
Nardelli,, J., Thiesson,, D., Fujiwara,, Y., Tsai,, F.‐Y., & Orkin,, S. H. (1999). Expression and genetic interaction of transcription factors GATA‐2 and GATA‐3 during development of the mouse central nervous system. Developmental Biology, 210(2), 305–321. https://doi.org/10.1006/dbio.1999.9278
Nichols,, D. H., & Bruce,, L. L. (2006). Migratory routes and fates of cells transcribing the Wnt‐1 gene in the murine hindbrain. Developmental Dynamics, 235(2), 285–300. https://doi.org/10.1002/dvdy.20611
Niu,, X., & Canlon,, B. (2002). Activation of tyrosine hydroxylase in the lateral efferent terminals by sound conditioning. Hearing Research, 174(1–2), 124–132. https://doi.org/10.1016/S0378-5955(02)00646-9
Nothwang,, H. G. (2016). Evolution of mammalian sound localization circuits: A developmental perspective. Progress in Neurobiology, 141, 1–24. https://doi.org/10.1016/j.pneurobio.2016.02.003
Nothwang,, H. G., Ebbers,, L., Schlüter,, T., & Willaredt,, M. A. (2015). The emerging framework of mammalian auditory hindbrain development. Cell and Tissue Research, 361(1), 33–48. https://doi.org/10.1007/s00441-014-2110-7
Ohsawa,, R., Ohtsuka,, T., & Kageyama,, R. (2005). Mash1 and Math3 are required for development of branchiomotor neurons and maintenance of neural progenitors. The Journal of Neuroscience, 25(25), 5857–5865. https://doi.org/10.1523/JNEUROSCI.4621-04.2005
Ohshima,, T., Ogawa,, M., Takeuchi,, K., Takahashi,, S., Kulkarni,, A. B., & Mikoshiba,, K. (2002). Cyclin‐dependent kinase 5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. The Journal of Neuroscience, 22(10), 4036–4044. https://doi.org/10.1523/JNEUROSCI.22-10-04036.2002
Parker,, H. J., & Krumlauf,, R. (2017). Segmental arithmetic: Summing up the Hox gene regulatory network for hindbrain development in chordates. WIREs Developmental Biology, 6(6), e286. https://doi.org/10.1002/wdev.286
Pata,, I., Studer,, M., van Doorninck,, J. H., Briscoe,, J., Kuuse,, S., Engel,, J. D., … Karis,, A. (1999). The transcription factor GATA3 is a downstream effector of Hoxb1 specification in rhombomere 4. Development, 126(23), 5523–5531.
Pattyn,, A., Hirsch,, M.‐R., Goridis,, C., & Brunet,, J.‐F. (2000). Control of hindbrain motor neuron differentiation by the homeobox gene Phox2b. Development, 127(7), 1349–1358.
Pattyn,, A., Vallstedt,, A., Dias,, J. M., Samad,, O. A., Krumlauf,, R., Rijli,, F. M., … Ericson,, J. (2003). Coordinated temporal and spatial control of motor neuron and serotonergic neuron generation from a common pool of CNS progenitors. Genes %26 Development, 17(6), 729–737. https://doi.org/10.1101/gad.255803
Pattyn,, A., Vallstedt,, A., Dias,, J. M., Sander,, M., & Ericson,, J. (2003). Complementary roles for Nkx6 and Nkx2 class proteins in the establishment of motoneuron identity in the hindbrain. Development, 130(17), 4149–4159. https://doi.org/10.1242/dev.00641
Pfaff,, S. L., Mendelsohn,, M., Stewart,, C. L., Edlund,, T., & Jessell,, T. M. (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron–dependent step in interneuron differentiation. Cell, 84(2), 309–320. https://doi.org/10.1016/S0092-8674(00)80985-X
Pierce,, E. T. (1967). Histogenesis of the dorsal and ventral cochlear nuclei in the mouse. An autoradiographic study. The Journal of Comparative Neurology, 131(1), 27–53. https://doi.org/10.1002/cne.901310104
Pierce,, E. T. (1973). Time of origin of neurons in the brain stem of the mouse. Progress in Brain Research, 40(C), 53–65. https://doi.org/10.1016/S0079-6123(08)60679-2
Pujol,, R. (1985). Morphology, synaptology and electrophysiology of the developing cochlea. Acta Oto‐Laryngologica, 99(sup421), 5–9. https://doi.org/10.3109/00016488509121751
Pujol,, R., & Carlier,, E. (1982). Cochlear synaptogenesis after sectioning the efferent bundle. Developmental Brain Research, 3(1), 151–154. https://doi.org/10.1016/0165‐3806(82)90084‐0
Pujol,, R., Carlier,, E., & Devigne,, C. (1979). Significance of presynaptic formations in early stages of cochlear synaptogenesis. Neuroscience Letters, 15(2–3), 97–102. https://doi.org/10.1016/0304-3940(79)96096-8
Qu,, Y., Glasco,, D. M., Zhou,, L., Sawant,, A., Ravni,, A., Fritzsch,, B., … Tissir,, F. (2010). Atypical cadherins Celsr1‐3 differentially regulate migration of facial branchiomotor neurons in mice. The Journal of Neuroscience, 30(28), 9392–9401. https://doi.org/10.1523/JNEUROSCI.0124-10.2010
Rasmussen,, G. L. (1946). The olivary peduncle and other fiber projections of the superior olivary complex. The Journal of Comparative Neurology, 84(2), 141–219. https://doi.org/10.1002/cne.900840204
Rasmussen,, G. L. (1953). Further observations of the efferent cochlear bundle. The Journal of Comparative Neurology, 99(1), 61–74. https://doi.org/10.1002/cne.900990105
Roberts,, B. L., & Meredith,, G. E. (1992). The efferent innervation of the ear: Variations on an enigma. In D. B. Webster,, A. N. Popper,, & R. R. Fay, (Eds.), The evolutionary biology of hearing (pp. 185–210). New York, NY: Springer. https://doi.org/10.1007/978-1-4612-2784-7_16
Robertson,, D., Anderson,, C.‐J., & Cole,, K. S. (1987). Segregation of efferent projections to different turns of the guinea pig cochlea. Hearing Research, 25(1), 69–76. https://doi.org/10.1016/0378-5955(87)90080-3
Robertson,, D., Harvey,, A. R., & Cole,, K. S. (1989). Postnatal development of the efferent innervation of the rat cochlea. Developmental Brain Research, 47(2), 197–207. https://doi.org/10.1016/0165-3806(89)90176-4
Rontal,, D. A., & Echteler,, S. M. (2003). Developmental segregation in the efferent projections to auditory hair cells in the gerbil. The Journal of Comparative Neurology, 467(4), 509–520. https://doi.org/10.1002/cne.10931
Rosengauer,, E., Hartwich,, H., Hartmann,, A. M., Rudnicki,, A., Satheesh,, S. V., Avraham,, K. B., & Nothwang,, H. G. (2012). Egr2::Cre mediated conditional ablation of dicer disrupts histogenesis of mammalian central auditory nuclei. PLoS One, 7(11), e49503. https://doi.org/10.1371/journal.pone.0049503
Rossel,, M., Loulier,, K., Feuillet,, C., Alonso,, S., & Carroll,, P. (2005). Reelin signaling is necessary for a specific step in the migration of hindbrain efferent neurons. Development, 132(6), 1175–1185. https://doi.org/10.1242/dev.01683
Roux,, I., Wersinger,, E., McIntosh,, J. M., Fuchs,, P. A., & Glowatzki,, E. (2011). Onset of cholinergic efferent synaptic function in sensory hair cells of the rat cochlea. The Journal of Neuroscience, 31(42), 15092–15101. https://doi.org/10.1523/JNEUROSCI.2743-11.2011
Roux,, I., Wu,, J. S., McIntosh,, J. M., & Glowatzki,, E. (2016). Assessment of the expression and role of the α 1‐nAChR subunit in efferent cholinergic function during the development of the mammalian cochlea. Journal of Neurophysiology, 116(2), 479–492. https://doi.org/10.1152/jn.01038.2015
Samad,, O. A., Geisen,, M. J., Caronia,, G., Varlet,, I., Zappavigna,, V., Ericson,, J., … Rijli,, F. M. (2004). Integration of anteroposterior and dorsoventral regulation of Phox2b transcription in cranial motoneuron progenitors by homeodomain proteins. Development, 131(16), 4071–4083. https://doi.org/10.1242/dev.01282
Sandell,, L. L., Butler Tjaden,, N. E., Barlow,, A. J., & Trainor,, P. A. (2014). Cochleovestibular nerve development is integrated with migratory neural crest cells. Developmental Biology, 385(2), 200–210. https://doi.org/10.1016/j.ydbio.2013.11.009
Sando,, I. (1965). The anatomical interrelationships of the cochlear nerve fibers. Acta Oto‐Laryngologica, 59(2–6), 417–436. https://doi.org/10.3109/00016486509124577
Sanes,, D. H., Merickel,, M., & Rubel,, E. W. (1989). Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. The Journal of Comparative Neurology, 279(3), 436–444. https://doi.org/10.1002/cne.902790308
Sapède,, D., Rossel,, M., Dambly‐Chaudière,, C., & Ghysen,, A. (2005). Role of SDF1 chemokine in the development of lateral line efferent and facial motor neurons. Proceedings of the National Academy of Sciences of the United States of America, 102(5), 1714–1718. https://doi.org/10.1073/pnas.0406382102
Saunders,, A., Granger,, A. J., & Sabatini,, B. L. (2015). Corelease of acetylcholine and GABA from cholinergic forebrain neurons. eLife, 4(4), 1–13. https://doi.org/10.7554/eLife.06412
Sendin,, G., Bourien,, J., Rassendren,, F., Puel,, J.‐L., & Nouvian,, R. (2014). Spatiotemporal pattern of action potential firing in developing inner hair cells of the mouse cochlea. Proceedings of the National Academy of Sciences, 111(5), 1999–2004. https://doi.org/10.1073/pnas.1319615111
Sewell,, W. F. (2011). Pharmacology and neurochemistry of olivocochlear efferents. In D. K. Ryugo,, R. R. Fay,, & A. N. Popper, (Eds.), Auditory and vestibular efferents (pp. 83–101). New York, NY: Springer. https://doi.org/10.1007/978-1-4419-7070-1_4
Shnerson,, A., Devigne,, C., & Pujol,, R. (1981). Age‐related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Developmental Brain Research, 2(1), 77–88. https://doi.org/10.1016/0165-3806(81)90060-2
Simmons,, D., Duncan,, J., de Caprona,, D. C., & Fritzsch,, B. (2011). Development of the inner ear efferent system. In D. K. Ryugo,, R. R. Fay,, & A. N. Popper, (Eds.), Auditory and vestibular efferents (pp. 187–216). New York, NY: Springer. https://doi.org/10.1007/978-1-4419-7070-1_7
Simmons,, D., Manson‐Gieseke,, L., Hendrix,, T., & McCarter,, S. (1990). Reconstructions of efferent fibers in the postnatal hamster cochlea. Hearing Research, 49(1–3), 127–139. https://doi.org/10.1016/0378-5955(90)90100-4
Simmons,, D. D. (2002). Development of the inner ear efferent system across vertebrate species. Journal of Neurobiology, 53(2), 228–250. https://doi.org/10.1002/neu.10130
Simmons,, D. D., Bertolotto,, C., Kim,, J., Raji‐Kubba,, J., & Mansdorf,, N. (1998). Choline acetyltransferase expression during a putative developmental waiting period. The Journal of Comparative Neurology, 397(2), 281–295. https://doi.org/10.1002/(SICI)1096-9861(19980727)397:2%3C281::AID-CNE9%3E3.0.CO;2-X
Simmons,, D. D., Mansdorf,, N. B., & Kim,, J. H. (1996). Olivocochlear innervation of inner and outer hair cells during postnatal maturation: Evidence for a waiting period. The Journal of Comparative Neurology, 370(4), 551–562. https://doi.org/10.1002/(SICI)1096-9861(19960708)370:4%3C551::AID-CNE10%3E3.0.CO;2-M
Simmons,, D. D., & Morley,, B. J. (1998). Differential expression of the α9 nicotinic acetylcholine receptor subunit in neonatal and adult cochlear hair cells. Molecular Brain Research, 56(1–2), 287–292. https://doi.org/10.1016/S0169-328X(98)00056-4
Simmons,, D. D., & Morley,, B. J. (2011). Spatial and temporal expression patterns of nicotinic acetylcholine alpha 9 and alpha 10 subunits in the embryonic and early postnatal inner ear. Neuroscience, 194, 326–336. https://doi.org/10.1016/j.neuroscience.2011.08.005
Simon,, H., & Lumsden,, A. (1993). Rhombomere‐specific origin of the contralateral vestibulo‐acoustic efferent neurons and their migration across the embryonic midline. Neuron, 11(2), 209–220. https://doi.org/10.1016/0896-6273(93)90179-U
Sobkowicz,, H. M., & Emmerling,, M. R. (1989). Development of acetylcholinesterase‐positive neuronal pathways in the cochlea of the mouse. Journal of Neurocytology, 18(2), 209–224. https://doi.org/10.1007/BF01206663
Song,, M.‐R., Shirasaki,, R., Cai,, C.‐L., Ruiz,, E. C., Evans,, S. M., Lee,, S. K., & Pfaff,, S. L. (2006). T‐Box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development, 133(24), 4945–4955. https://doi.org/10.1242/dev.02694
Spitzer,, N. C. (2017). Neurotransmitter switching in the developing and adult brain. Annual Review of Neuroscience, 40(1), 1–19. https://doi.org/10.1146/annurev-neuro-072116-031204
Studer,, M., Gavalas,, A., Marshall,, H., Ariza‐McNaughton,, L., Rijli,, F. M., Chambon,, P., & Krumlauf,, R. (1998). Genetic interactions between Hoxa1 and Hoxb1 reveal new roles in regulation of early hindbrain patterning. Development, 125(6), 1025–1036.
Studer,, M., Lumsden,, A., Ariza‐McNaughton,, L., Bradley,, A., & Krumlauf,, R. (1996). Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb‐1. Nature, 384(6610), 630–634. https://doi.org/10.1038/384630a0
Tiveron,, M.‐C., Pattyn,, A., Hirsch,, M.‐R., & Brunet,, J.‐F. (2003). Role of Phox2b and Mash1 in the generation of the vestibular efferent nucleus. Developmental Biology, 260(1), 46–57. https://doi.org/10.1016/S0012-1606(03)00213-6
Tritsch,, N. X., & Bergles,, D. E. (2010). Developmental regulation of spontaneous activity in the mammalian cochlea. The Journal of Neuroscience, 30(4), 1539–1550. https://doi.org/10.1523/JNEUROSCI.3875-09.2010
Tritsch,, N. X., Rodríguez‐Contreras,, A., Crins,, T. T. H., Wang,, H. C., Borst,, J. G. G., & Bergles,, D. E. (2010). Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset. Nature Neuroscience, 13(9), 1050–1052. https://doi.org/10.1038/nn.2604
Tritsch,, N. X., Yi,, E., Gale,, J. E., Glowatzki,, E., & Bergles,, D. E. (2007). The origin of spontaneous activity in the developing auditory system. Nature, 450(7166), 50–55. https://doi.org/10.1038/nature06233
Varela‐Echavarría,, A., Pfaff,, S. L., & Guthrie,, S. (1996). Differential expression of LIM homeobox genes among motor neuron subpopulations in the developing chick brain stem. Molecular and Cellular Neurosciences, 8(4), 242–257. https://doi.org/10.1006/mcne.1996.0061
Vetter,, D. E., Katz,, E., Maison,, S. F., Taranda,, J., Turcan,, S., Ballestero,, J., … Boulter,, J. (2007). The α10 nicotinic acetylcholine receptor subunit is required for normal synaptic function and integrity of the olivocochlear system. Proceedings of the National Academy of Sciences of the United States of America, 104(51), 20594–20599. https://doi.org/10.1073/pnas.0708545105
Vetter,, D. E., Liberman,, M. C., Mann,, J., Barhanin,, J., Boulter,, J., Brown,, M. C., … Elgoyhen,, A. B. (1999). Role of α9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron, 23(1), 93–103. https://doi.org/10.1016/S0896-6273(00)80756-4
Vetter,, D. E., & Mugnaini,, E. (1992). Distribution and dendritic features of three groups of rat olivocochlear neurons. Anatomy and Embryology (Berlin), 185(1), 1–16. https://doi.org/10.1007/BF00213596
Veuillet,, E., Georgieff,, N., Philibert,, B., Dalery,, J., Marie‐Cardine,, M., & Collet,, L. (2001). Abnormal peripheral auditory asymmetry in schizophrenia. Journal of Neurology, Neurosurgery, and Psychiatry, 70(1), 88–94. https://doi.org/10.1136/jnnp.70.1.88
Vivancos,, V., Chen,, P., Spassky,, N., Qian,, D., Dabdoub,, A., Kelley,, M., … Guthrie,, S. (2009). Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases. Neural Development, 4(1), 7. https://doi.org/10.1186/1749-8104-4-7
Wada, H., Iwasaki, M., Sato, T., Masai, I., Nishiwaki, Y., Tanaka, H., … Okamoto, H. (2005). Dual roles of zygotic and maternal Scribble1 in neural migration and convergent extension movements in zebrafish embryos. Development, 132(10), 2273–2285. https://doi.org/10.1242/dev.01810
Wada,, H., Tanaka,, H., Nakayama,, S., Iwasaki,, M., & Okamoto,, H. (2006). Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development, 133(23), 4749–4759. https://doi.org/10.1242/dev.02665
Wan,, Y. Y. (2014). GATA3: A master of many trades in immune regulation. Trends in Immunology, 35(6), 233–242. https://doi.org/10.1016/j.it.2014.04.002
Wang,, L., Klein,, R., Zheng,, B., & Marquardt,, T. (2011). Anatomical coupling of sensory and motor nerve trajectory via axon tracking. Neuron, 71(2), 263–277. https://doi.org/10.1016/j.neuron.2011.06.021
Warr,, W. B., Beck Boche,, J., & Neely,, S. T. (1997). Efferent innervation of the inner hair cell region: Origins and terminations of two lateral olivocochlear systems. Hearing Research, 108(1–2), 89–111. https://doi.org/10.1016/S0378-5955(97)00044-0
Warr,, W. B., & Guinan,, J. J. (1979). Efferent innervation of the organ of corti: Two separate systems. Brain Research, 173(1), 152–155. https://doi.org/10.1016/0006-8993(79)91104-1
White,, J. S., & Warr,, B. W. (1983). The dual origins of the olivocochlear bundle in the albino rat. The Journal of Comparative Neurology, 219(2), 203–214. https://doi.org/10.1002/cne.902190206
Wiechers,, B., Gestwa,, G., Mack,, A., Carroll,, P., Zenner,, H.‐P., & Knipper,, M. (1999). A changing pattern of brain‐derived neurotrophic factor expression correlates with the rearrangement of fibers during cochlear development of rats and mice. The Journal of Neuroscience, 19(8), 3033–3042. https://doi.org/10.1523/JNEUROSCI.19-08-03033.1999
Wilkinson,, D. G., Bhatt,, S., Chavrier,, P., Bravo,, R., & Charnay,, P. (1989). Segment‐specific expression of a zinc‐finger gene in the developing nervous system of the mouse. Nature, 337(6206), 461–464. https://doi.org/10.1038/337461a0
Wilkinson,, D. G., Bhatt,, S., Cook,, M., Boncinelli,, E., & Krumlauf,, R. (1989). Segmental expression of Hox‐2 homoeobox‐containing genes in the developing mouse hindbrain. Nature, 341(6241), 405–409. https://doi.org/10.1038/341405a0
Wu,, J. S., Young,, E. D., & Glowatzki,, E. (2016). Maturation of spontaneous firing properties after hearing onset in rat auditory nerve fibers: Spontaneous rates, refractoriness, and interfiber correlations. The Journal of Neuroscience, 36(41), 10584–10597. https://doi.org/10.1523/JNEUROSCI.1187-16.2016
Yang,, T., Bassuk,, A. G., Stricker,, S., & Fritzsch,, B. (2014). Prickle1 is necessary for the caudal migration of murine facial branchiomotor neurons. Cell and Tissue Research, 357(3), 549–561. https://doi.org/10.1007/s00441-014-1925-6
Yin,, Y., Liberman,, L. D., Maison,, S. F., & Liberman,, M. C. (2014). Olivocochlear innervation maintains the normal modiolar‐pillar and habenular‐cuticular gradients in cochlear synaptic morphology. Journal of the Association for Research in Otolaryngology, 15(4), 571–583. https://doi.org/10.1007/s10162-014-0462-z
Zachary,, S. P., & Fuchs,, P. A. (2015). Re‐emergent inhibition of cochlear inner hair cells in a mouse model of hearing loss. The Journal of Neuroscience, 35(26), 9701–9706. https://doi.org/10.1523/JNEUROSCI.0879-15.2015

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