Tuning Neuronal Potassium Channels to the Auditory Environment

Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 64)

Abstract

Neurons in auditory brainstem nuclei have developed several molecular and cellular specializations to ensure that auditory information can be relayed and processed at high rates and with very high temporal accuracy. Among these is the expression of Kv3 family voltage-dependent potassium channels such as Kv3.1, which allow the neurons to fire many hundreds of times per second. The specific channel isoforms in auditory neurons change during development, allowing the activity and amount of Kv3.1 to be adjusted by changes in the amplitude and frequencies of sounds in the auditory environment. The molecular mechanisms that produce such adjustments include direct phosphorylation of the channels and rapid alterations in the rates at which the channels are synthesized. These mechanisms, in combination with changes in other types of channels, may maximize the accuracy of information transfer through brainstem nuclei in different auditory environments, and may contribute to the learning of auditory discrimination tasks.

Keywords

Anteroventral cochlear nucleus Calyx of Held Ion channel Kv3.1 Kv3.3 Medial nucleus of the trapezoid body Protein kinase Sound localization 

Notes

Compliance with Ethics Requirements

Leonard K. Kaczmarek has received research grants from Autifony Inc.

References

  1. Barcia, G., Fleming, M. R., Deligniere, A., Gazula, V. R., et al. (2012). De novo gain-of-function KCNT1 channel mutations cause malignant migrating partial seizures of infancy. Nature Genetics, 44(11), 1255–1259.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Bassell, G. J., & Warren, S. T. (2008). Fragile X syndrome: Loss of local mRNA regulation alters synaptic development and function. Neuron, 60(2), 201–214.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bhattacharjee, A., Gan, L., & Kaczmarek, L. K. (2002). Localization of the Slack potassium channel in the rat central nervous system. The Journal of Comparative Neurology, 454(3), 241–254.CrossRefPubMedGoogle Scholar
  4. Bhattacharjee, A., von Hehn, C. A., Mei, X., & Kaczmarek, L. K. (2005). Localization of the Na+-activated K+ channel Slick in the rat central nervous system. The Journal of Comparative Neurology, 484(1), 80–92.CrossRefPubMedGoogle Scholar
  5. Billups, B., Wong, A. Y., & Forsythe, I. D. (2002). Detecting synaptic connections in the medial nucleus of the trapezoid body using calcium imaging. Pflugers Archiv – European Journal of Physiology, 444(5), 663–669.CrossRefPubMedGoogle Scholar
  6. Brand, A., Behrend, O., Marquardt, T., McAlpine, D., & Grothe, B. (2002). Precise inhibition is essential for microsecond interaural time difference coding. Nature, 417(6888), 543–547.CrossRefPubMedGoogle Scholar
  7. Brew, H. M., & Forsythe, I. D. (2005). Systematic variation of potassium current amplitudes across the tonotopic axis of the rat medial nucleus of the trapezoid body. Hearing Research, 206(1–2), 116–132.CrossRefPubMedGoogle Scholar
  8. Brown, M. R., & Kaczmarek, L. K. (2011). Potassium channel modulation and auditory processing. Hearing Research, 279(1–2), 32–42.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brown, M. R., Kronengold, J., Gazula, V. R., Chen, Y., et al. (2010). Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nature Neuroscience, 13(7), 819–821.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Brown, M. R., El-Hassar, L., Zhang, Y., Alvaro, G., et al. (2016). Physiological modulators of Kv3.1 channels adjust firing patterns of auditory brainstem neurons. Journal of Neurophysiology, jn 00174 02016.Google Scholar
  11. Cook, K. K., & Fadool, D. A. (2002). Two adaptor proteins differentially modulate the phosphorylation and biophysics of Kv1.3 ion channel by SRC kinase. The Journal of Biological Chemistry, 277(15), 13268–13280.CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cramer, K. S. (2005). Eph proteins and the assembly of auditory circuits. Hearing Research, 206(1–2), 42–51.CrossRefPubMedGoogle Scholar
  13. Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., et al. (2001). Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell, 107(4), 489–499.CrossRefPubMedGoogle Scholar
  14. Desai, R., Kronengold, J., Mei, J., Forman, S. A., & Kaczmarek, L. K. (2008). Protein kinase C modulates inactivation of Kv3.3 channels. The Journal of Biological Chemistry, 283(32), 22283–22294.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dodson, P. D., Barker, M. C., & Forsythe, I. D. (2002). Two heteromeric Kv1 potassium channels differentially regulate action potential firing. The Journal of Neuroscience, 22(16), 6953–6961.PubMedGoogle Scholar
  16. Gan, L., & Kaczmarek, L. K. (1998). When, where, and how much? Expression of the Kv3.1 potassium channel in high-frequency firing neurons. Journal of Neurobiology, 37(1), 69–79.CrossRefPubMedGoogle Scholar
  17. Gan, L., Perney, T.M. & Kaczmarek, L.K. (1996). Cloning and characterization of the promoter for a potassium channel expressed in high frequency firing neurons, The Journal of Biological Chemistry, 271: 5859–5865.CrossRefPubMedGoogle Scholar
  18. Gan, L., Hahn, S. J., & Kaczmarek, L. K. (1999). Cell type-specific expression of the Kv3.1 gene is mediated by a negative element in the 5′ untranslated region of the Kv3.1 promoter. Journal of Neurochemistry, 73(4), 1350–1362.CrossRefPubMedGoogle Scholar
  19. Gazula, V. R., Strumbos, J. G., Mei, X., Chen, H., et al. (2010). Localization of Kv1.3 channels in presynaptic terminals of brainstem auditory neurons. The Journal of Comparative Neurology, 518(16), 3205–3220.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Grissmer, S., Nguyen, A. N., Aiyar, J., Hanson, D. C., et al. (1994). Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Molecular Pharmacology, 45(6), 1227–1234.PubMedGoogle Scholar
  21. Hall, S. S., Walter, E., Sherman, E., Hoeft, F., & Reiss, A. L. (2009). The neural basis of auditory temporal discrimination in girls with fragile X syndrome. Journal of Neurodevelopmental Disorders, 1(1), 91–99.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hardman, R. M., & Forsythe, I. D. (2009). Ether-a-go-go-related gene K+ channels contribute to threshold excitability of mouse auditory brainstem neurons. The Journal of Physiology, 587(Pt 11), 2487–2497.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. The Journal of Physiology, 117(Pt 4), 500–544.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Johnston, J., Griffin, S. J., Baker, C., Skrzypiec, A., et al. (2008). Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons. The Journal of Physiology, 586(14), 3493–3509.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Johnston, J., Forsythe, I. D., & Kopp-Scheinpflug, C. (2010). Going native: Voltage-gated potassium channels controlling neuronal excitability. The Journal of Physiology, 588(Pt 17), 3187–3200.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Joris, P. X. (1996). Envelope coding in the lateral superior olive. II. Characteristic delays and comparison with responses in the medial superior olive. Journal of Neurophysiology, 76(4), 2137–2156.PubMedGoogle Scholar
  27. Joris, P. X., & Yin, T. C. (1995). Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences.[erratum appears in Journal of Neurophysiology 1995 Jun;73(6):followi]. Journal of Neurophysiology, 73(3), 1043–1062.PubMedGoogle Scholar
  28. Kaczmarek, L. K. (2012). Gradients and modulation of K(+) channels optimize temporal accuracy in networks of auditory neurons. PLoS Computational Biology, 8(3), e1002424.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kaczmarek, L. K. (2013). Slack, Slick and sodium-activated potassium channels. International Scholarly Research Notices Neuroscience, 2013, 354262, 1–14.Google Scholar
  30. Kanemasa, T., Gan, L., Perney, T. M., Wang, L. Y., & Kaczmarek, L. K. (1995). Electrophysiological and pharmacological characterization of a mammalian Shaw channel expressed in NIH 3T3 fibroblasts. Journal of Neurophysiology, 74(1), 207–217.PubMedGoogle Scholar
  31. Kullmann, L., Schluter, T., Wagner, H., & Nothwang, H. G. (2013). Evolutionary conservation of Kv3.1 in the barn owl Tyto alba. Brain, Behavior and Evolution, 81(3), 187–193.CrossRefPubMedGoogle Scholar
  32. Labro, A. J., Priest, M. F., Lacroix, J. J., Snyders, D. J., & Bezanilla, F. (2015). Kv3.1 uses a timely resurgent K(+) current to secure action potential repolarization. Nature Communications, 6, 10173.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Leao, R. N., Berntson, A., Forsythe, I. D., & Walmsley, B. (2004). Reduced low-voltage activated K+ conductances and enhanced central excitability in a congenitally deaf (dn/dn) mouse. The Journal of Physiology, 559(Pt 1), 25–33.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Li, W., Kaczmarek, L. K., & Perney, T. M. (2001). Localization of two high-threshold potassium channel subunits in the rat central auditory system. The Journal of Comparative Neurology, 437(2), 196–218.CrossRefPubMedGoogle Scholar
  35. Liu, S. J., & Kaczmarek, L. K. (1998a). The expression of two splice variants of the Kv3.1 potassium channel gene is regulated by different signaling pathways. The Journal of Neuroscience, 18(8), 2881–2890.PubMedGoogle Scholar
  36. Liu, S. Q., & Kaczmarek, L. K. (1998b). Depolarization selectively increases the expression of the Kv3.1 potassium channel in developing inferior colliculus neurons. The Journal of Neuroscience, 18(21), 8758–8769.PubMedGoogle Scholar
  37. Liu, S. Q., & Kaczmarek, L. K. (2005). Aminoglycosides block the Kv3.1 potassium channel and reduce the ability of inferior colliculus neurons to fire at high frequencies. Journal of Neurobiology, 62(4), 439–452.CrossRefPubMedGoogle Scholar
  38. Lu, Y., Monsivais, P., Tempel, B. L., & Rubel, E. W. (2004). Activity-dependent regulation of the potassium channel subunits Kv1.1 and Kv3.1. The Journal of Comparative Neurology, 470(1), 93–106.CrossRefPubMedGoogle Scholar
  39. Luneau, C. J., Williams, J. B., Marshall, J., Levitan, E. S., et al. (1991). Alternative splicing contributes to K+ channel diversity in the mammalian central nervous system. Proceedings of the National Academy of Sciences of the USA, 88(9), 3932–3936.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Macica, C. M., & Kaczmarek, L. K. (2001). Casein kinase 2 determines the voltage dependence of the Kv3.1 channel in auditory neurons and transfected cells. The Journal of Neuroscience, 21(4), 1160–1168.PubMedGoogle Scholar
  41. Macica, C. M., von Hehn, C. A., Wang, L. Y., Ho, C. S., et al. (2003). Modulation of the kv3.1b potassium channel isoform adjusts the fidelity of the firing pattern of auditory neurons. The Journal of Neuroscience, 23(4), 1133–1141.PubMedGoogle Scholar
  42. Middlebrooks, J. C., Nick, H. S., Subramony, S. H., Advincula, J., et al. (2013). Mutation in the kv3.3 voltage-gated potassium channel causing spinocerebellar ataxia 13 disrupts sound-localization mechanisms. PloS ONE, 8(10), e76749.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Misonou, H., Mohapatra, D. P., Park, E. W., Leung, V., et al. (2004). Regulation of ion channel localization and phosphorylation by neuronal activity. Nature Neuroscience, 7(7), 711–718.CrossRefPubMedGoogle Scholar
  44. Morest, D. K. (1968). The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle. Brain Research, 9(2), 288–311.CrossRefPubMedGoogle Scholar
  45. Mossbridge, J. A., Fitzgerald, M. B., O’Connor, E. S., & Wright, B. A. (2006). Perceptual-learning evidence for separate processing of asynchrony and order tasks. The Journal of Neuroscience, 26(49), 12708–12716.CrossRefPubMedGoogle Scholar
  46. Munte, T. F., Kohlmetz, C., Nager, W., & Altenmuller, E. (2001). Neuroperception: Superior auditory spatial tuning in conductors. Nature, 409(6820), 580.CrossRefPubMedGoogle Scholar
  47. Nager, W., Kohlmetz, C., Altenmuller, E., Rodriguez-Fornells, A., & Munte, T. F. (2003). The fate of sounds in conductors’ brains: an ERP study. Cognitive Brain Research, 17(1), 83–93.CrossRefPubMedGoogle Scholar
  48. Parameshwaran, S., Carr, C. E., & Perney, T. M. (2001). Expression of the Kv3.1 potassium channel in the avian auditory brainstem. The Journal of Neuroscience, 21(2), 485–494.PubMedGoogle Scholar
  49. Perney, T. M., & Kaczmarek, L. K. (1997). Localization of a high threshold potassium channel in the rat cochlear nucleus. The Journal of Comparative Neurology, 386(2), 178–202.CrossRefPubMedGoogle Scholar
  50. Perney, T. M., Marshall, J., Martin, K. A., Hockfield, S., & Kaczmarek, L. K. (1992). Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. Journal of Neurophysiology, 68(3), 756–766.PubMedGoogle Scholar
  51. Polley, D. B., Steinberg, E. E., & Merzenich, M. M. (2006). Perceptual learning directs auditory cortical map reorganization through top-down influences. The Journal of Neuroscience, 26(18), 4970–4982.CrossRefPubMedGoogle Scholar
  52. Richter, J. D., Bassell, G. J., & Klann, E. (2015). Dysregulation and restoration of translational homeostasis in fragile X syndrome. Nature Reviews Neuroscience, 16(10), 595–605.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Rosato-Siri, M. D., Zambello, E., Mutinelli, C., Garbati, N., et al. (2015). A novel modulator of Kv3 potassium channels regulates the firing of parvalbumin-positive cortical interneurons. The Journal of Pharmacology and Experimental Therapeutics, 354(3), 251–260.CrossRefPubMedGoogle Scholar
  54. Rubel, E. W., Hyson, R. L., & Durham, D. (1990). Afferent regulation of neurons in the brain stem auditory system. Journal of Neurobiology, 21(1), 169–196.CrossRefPubMedGoogle Scholar
  55. Rudy, B., & McBain, C. J. (2001). Kv3 channels: Voltage-gated K+ channels designed for high-frequency repetitive firing. Trends in Neurosciences, 24(9), 517–526.CrossRefPubMedGoogle Scholar
  56. Sakaba, T., & Neher, E. (2003). Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. The Journal of Neuroscience, 23(3), 837–846.PubMedGoogle Scholar
  57. Santi, C. M., Ferreira, G., Yang, B., Gazula, V. R., Butler, A., Wei, A., Kaczmarek, L. K., & Salkoff, L. (2006). Opposite regulation of Slick and Slack K+ channels by neuromodulators. The Journal of Neuroscience, 26(19), 5059–5068.CrossRefPubMedGoogle Scholar
  58. Schneggenburger, R., & Forsythe, I. D. (2006). The calyx of Held. Cell and Tissue Research, 326(2), 311–337.CrossRefPubMedGoogle Scholar
  59. Smith, P. H., Joris, P. X., & Yin, T. C. (1998). Anatomy and physiology of principal cells of the medial nucleus of the trapezoid body (MNTB) of the cat. Journal of Neurophysiology, 79(6), 3127–3142.PubMedGoogle Scholar
  60. Song, P., & Kaczmarek, L. K. (2006). Modulation of Kv3.1b potassium channel phosphorylation in auditory neurons by conventional and novel protein kinase C isozymes. The Journal of Biological Chemistry, 281(22), 15582–15591.CrossRefPubMedGoogle Scholar
  61. Song, P., Yang, Y., Barnes-Davies, M., Bhattacharjee, A., Hamann, M., et al. (2005). Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nature Neuroscience, 8(10), 1335–1342.CrossRefPubMedGoogle Scholar
  62. Spirou, G. A., Brownell, W. E., & Zidanic, M. (1990). Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. Journal of Neurophysiology, 63(5), 1169–1190.PubMedGoogle Scholar
  63. Steinert, J. R., Kopp-Scheinpflug, C., Baker, C., Challiss, R. A., et al. (2008). Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron, 60(4), 642–656.CrossRefPubMedGoogle Scholar
  64. Strumbos, J. G., Polley, D. B., & Kaczmarek, L. K. (2010a). Specific and rapid effects of acoustic stimulation on the tonotopic distribution of Kv3.1b potassium channels in the adult rat. Neuroscience, 167(3), 567–572.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Strumbos, J. G., Brown, M. R., Kronengold, J., Polley, D. B., & Kaczmarek, L. K. (2010b). Fragile X mental retardation protein is required for rapid experience-dependent regulation of the potassium channel Kv3.1b. The Journal of Neuroscience, 30(31), 10263–10271.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sung, M. J., Ahn, H. S., Hahn, S. J., & Choi, B. H. (2008). Open channel block of Kv3.1 currents by fluoxetine. Journal of Pharmacological Sciences, 106(1), 38–45.CrossRefPubMedGoogle Scholar
  67. Taschenberger, H., & von Gersdorff, H. (2000). Fine-tuning an auditory synapse for speed and fidelity: Developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. The Journal of Neuroscience, 20(24), 9162–9173.PubMedGoogle Scholar
  68. Taskin, B., von Schoubye, N. L., Sheykhzade, M., Bastlund, J. F., et al. (2015). Biophysical characterization of KV3.1 potassium channel activating compounds. European Journal of Pharmacology, 758, 164–170.CrossRefPubMedGoogle Scholar
  69. Tong, H., Steinert, J. R., Robinson, S. W., Chernova, T., et al. (2010). Regulation of Kv channel expression and neuronal excitability in rat medial nucleus of the trapezoid body maintained in organotypic culture. The Journal of Physiology, 588(Pt 9), 1451–1468.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Trussell, L. O. (1999). Synaptic mechanisms for coding timing in auditory neurons. Annual Review of Physiology, 61, 477–496.CrossRefPubMedGoogle Scholar
  71. von Hehn, C. A., Bhattacharjee, A., & Kaczmarek, L. K. (2004). Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. The Journal of Neuroscience, 24(8), 1936–1940.CrossRefGoogle Scholar
  72. Wang, L. Y., & Kaczmarek, L. K. (1998). High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature, 394(6691), 384–388.CrossRefPubMedGoogle Scholar
  73. Wang, L. Y., Gan, L., Forsythe, I. D., & Kaczmarek, L. K. (1998). Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. The Journal of Physiology, 509(Pt 1), 183–194.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Wang, Y., Sakano, H., Beebe, K., Brown, M. R., et al. (2014). Intense and specialized dendritic localization of the fragile X mental retardation protein in binaural brainstem neurons: A comparative study in the alligator, chicken, gerbil, and human. The Journal of Comparative Neurology, 522(9), 2107–2128.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Winklhofer, M., Matthias, K., Seifert, G., Stocker, M., et al. (2003). Analysis of phosphorylation-dependent modulation of Kv1.1 potassium channels. Neuropharmacology, 44(6), 829–842.CrossRefPubMedGoogle Scholar
  76. Yang, B., Desai, R., & Kaczmarek, L. K. (2007). Slack and Slick K(Na) channels regulate the accuracy of timing of auditory neurons. The Journal of Neuroscience, 27(10), 2617–2627.CrossRefPubMedGoogle Scholar
  77. Yokoyama, S., Imoto, K., Kawamura, T., Higashida, H., et al. (1989). Potassium channels from NG108-15 neuroblastoma-glioma hybrid cells: Primary structure and functional expression from cDNAs. FEBS Letters, 259(1), 37–42.CrossRefPubMedGoogle Scholar
  78. Zhang, Y., & Kaczmarek, L. K. (2016). Kv3.3 potassium channels and spinocerebellar ataxia. The Journal of Physiology, 594(16), 4677–4684.CrossRefPubMedGoogle Scholar
  79. Zhang, Y., Zhang, X. F., Fleming, M. R., Amiri, A., et al. (2016). Kv3.3 channels bind Hax-1 and Arp2/3 to assemble a stable local actin network that regulates channel gating. Cell, 165(2), 434–448.CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Departments of Pharmacology and Cellular and Molecular PhysiologyYale University School of MedicineNew HavenUSA

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