Home MicroRNAs in the auditory system: tiny molecules with big impact
Article
Licensed
Unlicensed Requires Authentication

MicroRNAs in the auditory system: tiny molecules with big impact

  • Lena Ebbers

    Lena Ebbers studied biology at the Universities of Göttingen and Oldenburg. She received her Ph.D. from the University of Oldenburg where she is currently working as a scientist in the neurogenetics division of Hans Gerd Nothwang.

     EMAIL logo     , Faiza Altaf

    Faiza Altaf did her master’s degree in molecular genetics at Comsats University Islamabad, Pakistan. In her master’s thesis she quantified the expression of RNA editing enzyme genes in congenital heart defect patients. She is currently doing her Ph.D. in the neurogenetics division at the University of Oldenburg under the supervision of Hans Gerd Nothwang. Here, her research focuses on functional characterization of microRNAs in auditory brainstem of mice.

         and Hans Gerd Nothwang

    Hans Gerd Nothwang studied biology at the University of Stuttgart, where he also received his Ph.D., while performing his work at the Institute Jacques Monod in Paris. He did his habilitation in animal physiology and neurobiology with Eckhard Friauf in Kaiserslautern. Since 2007, he holds a professorship in Neurogenetics at the University of Oldenburg. There, he currently serves as dean of the faculty of Medicine and Health Sciences.

Published/Copyright: October 7, 2022
Become an author with De Gruyter Brill
Author Information
Neuroforum
From the journal Neuroforum Volume 28 Issue 4

Abstract

“Blindness separates from things; deafness separates from people.” This quote attributed to the deaf-blind author and activist Helen Keller (1880–1968) indicates the importance of proper hearing for social interaction in our society which is largely driven by acoustic communication. A major cause for auditory dysfunction lies in our genome with currently more than 100 genes linked to hearing loss. One example is the microRNA gene Mir-96 of the microRNA-183 family. MicroRNAs are small regulatory RNAs involved in the finetuning of gene expression. Analyses of transgenic mouse models established this microRNA family as a major regulator for the function of the inner ear as well as synaptic transmission in the auditory brainstem. The microRNA-183 family might therefore play an important role in coordinating the development of the peripheral and central auditory system and their specializations.

Zusammenfassung

„Blindheit trennt von Dingen; Taubheit von Menschen.“ Dieses Zitat, das der taubblinden Autorin und Aktivistin Helen Keller (1880–1968) zugeschrieben wird, zeigt die Bedeutung des Hörens für soziale Interaktion in unserer Gesellschaft auf, die zu einem großen Teil von akustischer Kommunikation geprägt ist. Eine Hauptursache von Taubheit liegt in unserem Genom. Mehr als 100 Gene werden derzeit mit einem Hörverlust in Verbindung gebracht. Ein Beispiel ist das Gen Mir-96 der microRNA-183-Familie. MicroRNAs sind kleine regulatorische RNAs, die an der Feinjustierung der Genexpression beteiligt sind. Untersuchungen in Mausmodellen, denen Mitglieder der microRNA-183-Familie fehlen, demonstrierten ihre Bedeutung für die Funktion des Innenohrs sowie die synaptische Übertragung im auditorischen Hirnstamm. Sie spielen daher vermutlich eine wichtige Rolle bei der Koordinierung der Entwicklung des peripheren und zentralen Hörsystems und ihrer Spezialisierungen.

Keywords: auditory brainstem; deafness; development; posttranscriptional gene regulation; sensory systems
Schlüsselwörter: auditorischer Hirnstamm; Entwicklung; posttranskriptionelle Genregulation; sensorische Systeme; Taubheit
Corresponding author: Lena Ebbers, Division of Neurogenetics, Department of Neuroscience, School of Medicine and Health Sciences, Carl von Ossietzky University Oldenburg, 26129 Oldenburg, Germany, E-mail:

Funding source: Deutsche Forschungsgemeinschaft

Award Identifier / Grant number: GRK 1885

About the authors

Lena Ebbers

Lena Ebbers studied biology at the Universities of Göttingen and Oldenburg. She received her Ph.D. from the University of Oldenburg where she is currently working as a scientist in the neurogenetics division of Hans Gerd Nothwang.

Faiza Altaf

Faiza Altaf did her master’s degree in molecular genetics at Comsats University Islamabad, Pakistan. In her master’s thesis she quantified the expression of RNA editing enzyme genes in congenital heart defect patients. She is currently doing her Ph.D. in the neurogenetics division at the University of Oldenburg under the supervision of Hans Gerd Nothwang. Here, her research focuses on functional characterization of microRNAs in auditory brainstem of mice.

Hans Gerd Nothwang

Hans Gerd Nothwang studied biology at the University of Stuttgart, where he also received his Ph.D., while performing his work at the Institute Jacques Monod in Paris. He did his habilitation in animal physiology and neurobiology with Eckhard Friauf in Kaiserslautern. Since 2007, he holds a professorship in Neurogenetics at the University of Oldenburg. There, he currently serves as dean of the faculty of Medicine and Health Sciences.

Acknowledgments

Figures 1–3 were created with BioRender.com. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) Graduate School “Molecular Basis of Sensory Biology” Grant DFG GRK 1885.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was supported by Deutsche Forschungsgemeinschaft (GRK 1885).

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

Ambros, V. and Horvitz, H.R. (1984). Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226, 409–416. https://doi.org/10.1126/science.6494891.Search in Google Scholar PubMed

Ambros, V. and Horvitz, H.R. (1987). The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev. 1, 398–414. https://doi.org/10.1101/gad.1.4.398.Search in Google Scholar PubMed

Arzhanov, I., Sintakova, K., and Romanyuk, N. (2022). The role of miR-20 in Health and disease of the central nervous system. Cells 11, 1–22, doi:https://doi.org/10.3390/cells11091525.Search in Google Scholar PubMed PubMed Central

Bak, M., Silahtaroglu, A., Møller, M., Christensen, M., Rath, M.F., Skryabin, B., Tommerup, N., and Kauppinen, S. (2008). MicroRNA expression in the adult mouse central nervous system. RNA (New York, N.Y.) 14, 432–444, https://doi.org/10.1261/rna.783108.Search in Google Scholar PubMed PubMed Central

Banks, M.I. and Smith, P.H. (1992). Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 12, 2819–2837. https://doi.org/10.1523/JNEUROSCI.12-07-02819.1992.Search in Google Scholar PubMed PubMed Central

Banks, S.A., Pierce, M.L., and Soukup, G.A. (2020). Sensational MicroRNAs: neurosensory roles of the MicroRNA-183 family. Mol. Neurobiol. 57, 358–371. https://doi.org/10.1007/s12035-019-01717-3.Search in Google Scholar PubMed

Bartel, D.P. (2018). Metazoan MicroRNAs. Cell 173, 20–51. https://doi.org/10.1016/j.cell.2018.03.006.Search in Google Scholar PubMed PubMed Central

Bernstein, E., Kim, S.Y., Carmell, M.A., Murchison, E.P., Alcorn, H., Li, M.Z., Mills, A.A., Elledge, S.J., Anderson, K.V., and Hannon, G.J. (2003). Dicer is essential for mouse development. Nat. Genet. 35, 215–217. https://doi.org/10.1038/ng1253.Search in Google Scholar PubMed

Borst, J.G.G. and van Soria Hoeve, J. (2012). The calyx of Held synapse: from model synapse to auditory relay. Annu. Rev. Physiol. 74, 199–224. https://doi.org/10.1146/annurev-physiol-020911-153236.Search in Google Scholar PubMed

Chalfie, M. (1981). Mutations that lead to reiterations in the cell lineages of C. elegans. Cell 24, 59–69. https://doi.org/10.1016/0092-8674(81)90501-8.Search in Google Scholar PubMed

Chen, Y. and Wang, X. (2020). miRDB: an online database for prediction of functional microRNA targets. Nucleic Acids Res. 48, D127–D131. https://doi.org/10.1093/nar/gkz757.Search in Google Scholar PubMed PubMed Central

Dambal, S., Shah, M., Mihelich, B., and Nonn, L. (2015). The microRNA-183 cluster: the family that plays together stays together. Nucleic Acids Res. 43, 7173–7188, https://doi.org/10.1093/nar/gkv703.Search in Google Scholar PubMed PubMed Central

Eshraghi, A.A., Polineni, S.P., Davies, C., Shahal, D., Mittal, J., Al-Zaghal, Z., Sinha, R., Jindal, U., and Mittal, R. (2020). Genotype-phenotype correlation for predicting cochlear implant outcome: current challenges and opportunities. Front. Genet. 11, 1–15, doi:https://doi.org/10.3389/fgene.2020.00678.Search in Google Scholar PubMed PubMed Central

Fan, J., Jia, L., Li, Y., Ebrahim, S., May-Simera, H., Wood, A., Morell, R.J., Liu, P., Lei, J., and Kachar, B. (2017). Maturation arrest in early postnatal sensory receptors by deletion of the miR-183/96/182 cluster in mouse. Proc. Natl. Acad. Sci. USA 114, E4271–E4280, https://doi.org/10.1073/pnas.1619442114.Search in Google Scholar PubMed PubMed Central

Friedman, R.C., Farh, K.K.H., Burge, C.B., and Bartel, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105. https://doi.org/10.1101/gr.082701.108.Search in Google Scholar PubMed PubMed Central

Grothe, B., Pecka, M., and McAlpine, D. (2010). Mechanisms of sound localization in mammals. Physiol. Rev. 90, 983–1012. https://doi.org/10.1152/physrev.00026.2009.Search in Google Scholar PubMed

Held, H. (1893). Die centrale gehörleitung. Arch. für Anat. Physiol A3 +4, 201–248.Search in Google Scholar

Hildebrandt, M. and Nellen, W. (1992). Differential antisense transcription from the Dictyostelium EB4 gene locus: implications on antisense-mediated regulation of mRNA stability. Cell 69, 197–204. https://doi.org/10.1016/0092-8674(92)90130-5.Search in Google Scholar PubMed

Horvitz, H.R. and Sulston, J.E. (1980). Isolation and genetic characterization of cell-lineage mutants of the nematode Caenorhabditis elegans. Genetics 96, 435–454. https://doi.org/10.1093/genetics/96.2.435.Search in Google Scholar PubMed PubMed Central

Jensen, K.P. and Covault, J. (2011). Human miR-1271 is a miR-96 paralog with distinct non-conserved brain expression pattern. Nucleic Acids Res. 39, 701–711. https://doi.org/10.1093/nar/gkq798.Search in Google Scholar PubMed PubMed Central

Kopp-Scheinpflug, C., Tolnai, S., Malmierca, M.S., and Rübsamen, R. (2008). The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154, 160–170. https://doi.org/10.1016/j.neuroscience.2008.01.088.Search in Google Scholar PubMed

Krohs, C., Bordeynik-Cohen, M., Messika-Gold, N., Elkon, R., Avraham, K.B., and Nothwang, H.G. (2021a). Expression pattern of cochlear microRNAs in the mammalian auditory hindbrain. Cell Tissue Res. 383, 655–666. https://doi.org/10.1007/s00441-020-03290-x.Search in Google Scholar PubMed PubMed Central

Krohs, C., Körber, C., Ebbers, L., Altaf, F., Hollje, G., Hoppe, S., Dörflinger, Y., Prosser, H.M., and Nothwang, H.G. (2021b). Loss of miR-183/96 alters synaptic strength via presynaptic and postsynaptic mechanisms at a central synapse. J. Neurosci. 41, 6796–6811. https://doi.org/10.1523/JNEUROSCI.0139-20.2021.Search in Google Scholar PubMed PubMed Central

Kuhn, S., Johnson, S.L., Furness, D.N., Chen, J., Ingham, N., Hilton, J.M., Steffes, G., Lewis, M.A., Zampini, V., Hackney, C.M., et al.. (2011). miR-96 regulates the progression of differentiation in mammalian cochlear inner and outer hair cells. Proc. Natl. Acad. Sci. U. S. A. 108, 2355–2360. https://doi.org/10.1073/pnas.1016646108.Search in Google Scholar PubMed PubMed Central

Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001). Identification of novel genes coding for small expressed RNAs. Science 294, 853–858. https://doi.org/10.1126/science.1064921.Search in Google Scholar PubMed

Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., and Tuschl, T. (2002). Identification of tissue-specific MicroRNAs from mouse. Curr. Biol. 12, 735–739. https://doi.org/10.1016/s0960-9822(02)00809-6.Search in Google Scholar PubMed

Lau, N.C., Lim, L.P., Weinstein, E.G., and Bartel, D.P. (2001). An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans. Science 294, 858–862. https://doi.org/10.1126/science.1065062.Search in Google Scholar PubMed

Lee, R.C. and Ambros, V. (2001). An extensive class of small RNAs in Caenorhabditis elegans. Science 294, 862–864. https://doi.org/10.1126/science.1065329.Search in Google Scholar PubMed

Lee, R.C., Feinbaum, R.L., and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843–854. https://doi.org/10.1016/0092-8674(93)90529-Y.Search in Google Scholar PubMed

Lewis, M.A., Quint, E., Glazier, A.M., Fuchs, H., Angelis, M.H.D., Langford, C., van Dongen, S., Abreu-Goodger, C., Piipari, M., Redshaw, N., et al.. (2009). An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat. Genet. 41, 614–618. https://doi.org/10.1038/ng.369.Search in Google Scholar PubMed PubMed Central

Lewis, M.A., Di Domenico, F., Ingham, N.J., Prosser, H.M., and Steel, K.P. (2020). Hearing impairment due to Mir183/96/182 mutations suggests both loss and gain of function effects. Dis. Models Mech 14, 1–18, doi:https://doi.org/10.1242/dmm.047225.Search in Google Scholar PubMed PubMed Central

Mencía, A., Modamio-Høybjør, S., Redshaw, N., Morín, M., Mayo-Merino, F., Olavarrieta, L., Aguirre, L.A., del Castillo, I., Steel, K.P., Dalmay, T., et al.. (2009). Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat. Genet. 41, 609–613. https://doi.org/10.1038/ng.355.Search in Google Scholar PubMed

Michalski, N. and Petit, C. (2019). Genes involved in the development and physiology of both the peripheral and central auditory systems. Annu. Rev. Neurosci 42, 67–68, doi:https://doi.org/10.1146/annurev-neuro-070918-050428.Search in Google Scholar PubMed

Pasquinelli, A.E., Reinhart, B.J., Slack, F., Martindale, M.Q., Kuroda, M.I., Maller, B., Hayward, D.C., Ball, E.E., Degnan, B., Müller, P., et al.. (2000). Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408, 86–89. https://doi.org/10.1038/35040556.Search in Google Scholar PubMed

Peng, Y. and Croce, C.M. (2016). The role of MicroRNAs in human cancer. Signal Transduct. Targeted Ther. 1, 15004. https://doi.org/10.1038/sigtrans.2015.4.Search in Google Scholar PubMed PubMed Central

Peng, C., Li, L., Zhang, M.-D., Bengtsson Gonzales, C., Parisien, M., Belfer, I., Usoskin, D., Abdo, H., Furlan, A., Häring, M., et al.. (2017). miR-183 cluster scales mechanical pain sensitivity by regulating basal and neuropathic pain genes. Science 356, 1168–1171, doi:https://doi.org/10.1126/science.aam7671. 28572455.Search in Google Scholar PubMed

Pickles, J.O. (2015). Auditory pathways: anatomy and physiology. Handb. Clin. Neurol. 129, 3–25. https://doi.org/10.1016/B978-0-444-62630-1.00001-9.Search in Google Scholar PubMed

Prosser, H.M., Koike-Yusa, H., Cooper, J.D., Law, F.C., and Bradley, A. (2011). A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat. Biotechnol. 29, 840–845. https://doi.org/10.1038/nbt.1929.Search in Google Scholar PubMed PubMed Central

Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901–906. https://doi.org/10.1038/35002607.Search in Google Scholar PubMed

Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., and Bartel, D.P. (2002). MicroRNAs in plants. Genes Dev. 16, 1616–1626. https://doi.org/10.1101/gad.1004402.Search in Google Scholar PubMed PubMed Central

Rudnicki, A., Isakov, O., Ushakov, K., Shivatzki, S., Weiss, I., Friedman, L.M., Shomron, N., and Avraham, K.B. (2014). Next-generation sequencing of small RNAs from inner ear sensory epithelium identifies microRNAs and defines regulatory pathways. BMC Genom. 15, 484. https://doi.org/10.1186/1471-2164-15-484.Search in Google Scholar PubMed PubMed Central

Schlüter, T., Berger, C., Rosengauer, E., Fieth, P., Krohs, C., Ushakov, K., Steel, K.P., Avraham, K.B., Hartmann, A.K., Felmy, F., et al.. (2018). miR-96 is required for normal development of the auditory hindbrain. Hum. Mol. Genet. 27, 860–874. https://doi.org/10.1093/hmg/ddy007.Search in Google Scholar PubMed

Sheffield, A.M. and Smith, R.J.H. (2019). The epidemiology of deafness. Cold Spring Harbor Perspect. Med. 9, 1–15, doi:https://doi.org/10.1101/cshperspect.a033258.Search in Google Scholar PubMed PubMed Central

Steinert, J.R., Postlethwaite, M., Jordan, M.D., Chernova, T., Robinson, S.W., and Forsythe, I.D. (2010). NMDAR-mediated EPSCs are maintained and accelerate in time course during maturation of mouse and rat auditory brainstem in vitro. J. Physiol. 588, 447–463. https://doi.org/10.1113/jphysiol.2009.184317.Search in Google Scholar PubMed PubMed Central

Sun, L., Xia, R., Jiang, J., Wen, T., Huang, Z., Qian, R., Zhang, M.D., Zhou, M., and Peng, C. (2021). MicroRNA-96 is required to prevent allodynia by repressing voltage-gated sodium channels in spinal cord. Prog. Neurobiol. 202, 102024. https://doi.org/10.1016/j.pneurobio.2021.102024.Search in Google Scholar PubMed

Taiber, S., Gwilliam, K., Hertzano, R., and Avraham, K.B. (2022). The genomics of auditory function and disease. Annu. Rev. Genom. Hum. Genet 23, 275–299, doi:https://doi.org/10.1146/annurev-genom-121321-094136.Search in Google Scholar PubMed

van Camp, G. and Smith, R.J.H. (2021). Hereditary Hearing Loss Homepage. https://hereditaryhearingloss.org/citing.Search in Google Scholar

Wang, Y., Luo, J., Zhang, H., and Lu, J. (2016). microRNAs in the same clusters evolve to coordinately regulate functionally related genes. Mol. Biol. Evol. 33, 2232–2247. https://doi.org/10.1093/molbev/msw089.Search in Google Scholar PubMed PubMed Central

Weston, M.D., Pierce, M.L., Rocha-Sanchez, S., Beisel, K.W., and Soukup, G.A. (2006). MicroRNA gene expression in the mouse inner ear. Brain Res. 1111, 95–104. https://doi.org/10.1016/j.brainres.2006.07.006.Search in Google Scholar PubMed

Wienholds, E., Kloosterman, W.P., Miska, E., Alvarez-Saavedra, E., Berezikov, E., Bruijn, E.d., Horvitz, H.R., Kauppinen, S., and Plasterk, R.H.A. (2005). MicroRNA expression in zebrafish embryonic development. Science 309, 310–311. https://doi.org/10.1126/science.1114519.Search in Google Scholar PubMed

Wightman, B., Ha, I., and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855–862. https://doi.org/10.1016/0092-8674(93)90530-4.Search in Google Scholar PubMed

Willaredt, M.A., Ebbers, L., and Nothwang, H.G. (2014). Central auditory function of deafness genes. Hear. Res. 312, 9–20. https://doi.org/10.1016/j.heares.2014.02.004.Search in Google Scholar PubMed

Wu, K.-C., Chen, X.-J., Jin, G.-H., Wang, X.-Y., Yang, D.-D., Li, Y.-P., Xiang, L., Zhang, B.-W., Zhou, G.-H., Zhang, C.-J., et al.. (2019). Deletion of miR-182 Leads to Retinal Dysfunction in Mice. Investig. Ophthalmol. Vis. Sci. 60, 1265–1274, https://doi.org/10.1167/iovs.18-24166.Search in Google Scholar PubMed

Xiang, L., Zhang, J., Rao, F.-Q., Yang, Q.-L., Zeng, H.-Y., Huang, S.-H., Xie, Z.-X., Lv, J.-N., Lin, D., Chen, X.-J., et al.. (2022). Depletion of miR-96 Delays, But Does Not Arrest, Photoreceptor Development in Mice. Investig. Ophthalmol. Vis. Sci. 63, 24, https://doi.org/10.1167/iovs.63.4.24.Search in Google Scholar PubMed PubMed Central

Xu, S., Witmer, P.D., Lumayag, S., Kovacs, B., and Valle, D. (2007). MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster. J. Biol. Chem. 282, 25053–25066. https://doi.org/10.1074/jbc.M700501200.Search in Google Scholar PubMed

Yang, Y.M., Aitoubah, J., Lauer, A.M., Nuriya, M., Takamiya, K., Jia, Z., May, B.J., Huganir, R.L., and Wang, L.Y. (2011). GluA4 is indispensable for driving fast neurotransmission across a high-fidelity central synapse. J. Physiol. 589, 4209–4227. https://doi.org/10.1113/jphysiol.2011.208066.Search in Google Scholar PubMed PubMed Central

Zhang, C.J., Xiang, L., Chen, X.J., Wang, X.Y., Wu, K.C., Zhang, B.W., Chen, D.F., Jin, G.H., Zhang, H., Chen, Y.C., et al.. (2020). Ablation of mature miR-183 leads to retinal dysfunction in mice. Invest. Ophthalmol. Visual Sci. 61, 12. https://doi.org/10.1167/iovs.61.3.12.Search in Google Scholar PubMed PubMed Central

Published Online: 2022-10-07
Published in Print: 2022-11-25

© 2022 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Neuroforum: vom gedruckten Heft ins elektronische Zeitalter
  4. Review articles
  5. The visual representation of space in the primate brain
  6. MicroRNAs in the auditory system: tiny molecules with big impact
  7. Non-coding repeat expansions associated with familial adult myoclonic epilepsy: a new paradigm of gene-independent monogenic disorders
  8. Forebrain development–an intricate balance decides between health and disease
  9. Presentation of scientific institutions
  10. Collaborative Research Centre (CRC 1451) “Key mechanisms of motor control in health and disease”
  11. Collaborative Research Center SFB 1528 “Cognition of Interaction”
  12. SPP2411: ‘Sensing LOOPS: cortico-subcortical interactions for adaptive sensing’
  13. Newly DFG-funded research training group at the University of Kassel: “Biological clocks on multiple time scales” GRK 2749/1
  14. Nachrichten
  15. Catching up in Cologne – 31st Neurobiology Doctoral Students Workshop in Cologne
  16. Nachrichten aus der Gesellschaft
  17. Nachrichten aus der Gesellschaft
https://doi.org/10.1515/nf-2022-0016
Keywords for this article
auditory brainstem; deafness; development; posttranscriptional gene regulation; sensory systems

Articles in the same Issue

  1. Frontmatter
  2. Editorial
  3. Neuroforum: vom gedruckten Heft ins elektronische Zeitalter
  4. Review articles
  5. The visual representation of space in the primate brain
  6. MicroRNAs in the auditory system: tiny molecules with big impact
  7. Non-coding repeat expansions associated with familial adult myoclonic epilepsy: a new paradigm of gene-independent monogenic disorders
  8. Forebrain development–an intricate balance decides between health and disease
  9. Presentation of scientific institutions
  10. Collaborative Research Centre (CRC 1451) “Key mechanisms of motor control in health and disease”
  11. Collaborative Research Center SFB 1528 “Cognition of Interaction”
  12. SPP2411: ‘Sensing LOOPS: cortico-subcortical interactions for adaptive sensing’
  13. Newly DFG-funded research training group at the University of Kassel: “Biological clocks on multiple time scales” GRK 2749/1
  14. Nachrichten
  15. Catching up in Cologne – 31st Neurobiology Doctoral Students Workshop in Cologne
  16. Nachrichten aus der Gesellschaft
  17. Nachrichten aus der Gesellschaft
Sign up now to receive a 20% welcome discount
Institutional Access
How does access work?
Have an idea on how to improve our website?
Please write us.
© 2025 De Gruyter Brill
Downloaded on 25.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/nf-2022-0016/html
Scroll to top button