Comparative posthearing development of inhibitory inputs to the lateral superior olive in gerbils and mice

Journal of Neurophysiology

Volumn 106, Issue 3, 2011, Pages 1443-1453

  Walcher, Jan ^a   Hassfurth, Benjamin ^a   Grothe, Benedikt ^a   Koch, Ursula ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Auditory brain stem; Development; Glycine receptor; Inhibition; Synaptic

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; GERBIL; HEARING; NERVOUS SYSTEM CONDUCTANCE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; STIMULUS RESPONSE; SUPERIOR OLIVARY NUCLEUS; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; WHOLE CELL;

ANIMALS; ANIMALS, NEWBORN; GERBILLINAE; HEARING; INHIBITORY POSTSYNAPTIC POTENTIALS; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; NEURAL INHIBITION; OLIVARY NUCLEUS;

EID: 80052602387     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01087.2010     Document Type: Article

References (61)

1. Adam TJ, Finlayson PG, Schwarz DW. Membrane properties of principal neurons of the lateral superior olive. J Neurophysiol 86: 922-934, 2001.
2. Adam TJ, Schwarz DW, Finlayson PG. Firing properties of chopper and delay neurons in the lateral superior olive of the rat. Exp Brain Res 124: 489-502, 1999.
3. Awatramani GB, Turecek R, Trussell LO. Inhibitory control at a synaptic relay. J Neurosci 24: 2643-2647, 2004.
4. Awatramani GB, Turecek R, Trussell LO. Staggered development of GABAergic and glycinergic transmission in the MNTB. J Neurophysiol 93: 819-828, 2005.
5. Barnes-Davies M, Barker MC, Osmani F, Forsythe ID. Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19: 325-333, 2004.
6. Beato M. The time course of transmitter at glycinergic synapses onto motoneurons. J Neurosci 28: 7412-7425, 2008.
7. Boudreau JC, Tsuchitani C. Binaural interaction in the cat superior olive S segment. J Neurophysiol 31: 442-454, 1968.
8. Boudreau JC, Tsuchitani C. Cat superior olive S-segment cell discharge to tonal stimulation. Contrib Sens Physiol 4: 143-213, 1970.
9. Bradaia A, Schlichter R, Trouslard J. Role of glial and neuronal glycine transporters in the control of glycinergic and glutamatergic synaptic transmission in lamina X of the rat spinal cord. J Physiol 559: 169-186, 2004.
10. Cathala L, Holderith NB, Nusser Z, DiGregorio DA, Cull-Candy SG. Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat Neurosci 8: 1310-1318, 2005.
11. Clements JD. Variance-mean analysis: a simple and reliable approach for investigating synaptic transmission and modulation. J Neurosci Methods 130: 115-125, 2003.
12. Glowatzki E, Fuchs PA. Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288: 2366-2368, 2000.
13. Hassfurth B, Magnusson AK, Grothe B, Koch U. Sensory deprivation regulates the development of the hyperpolarization-activated current in auditory brainstem neurons. Eur J Neurosci 30: 1227-1238, 2009.
14. Huffman KJ, Cramer KS. EphA4 misexpression alters tonotopic projections in the auditory brainstem. Dev Neurobiol 67: 1655-1668, 2007.
15. Joris PX, Yin TC. Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J Neurophysiol 73: 1043-1062, 1995.
16. Kaiser A, Alexandrova O, Grothe B. Urocortin-expressing olivocochlear neurons exhibit tonotopic and developmental changes in the auditory brainstem and in the innervation of the cochlea. J Comp Neurol 519: 2758-2778, 2011.
17. Kakazu Y, Akaike N, Komiyama S, Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19: 2843, 1999.
18. Kandler K, Clause A, Noh J. Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci 12: 711-717, 2009.
19. Kandler K, Friauf E. Development of electrical membrane properties and discharge characteristics of superior olivary complex neurons in fetal and postnatal rats. Eur J Neurosci 7: 1773-1790, 1995.
20. Kandler K, Gillespie DC. Developmental refinement of inhibitory soundlocalization circuits. Trends Neurosci 28: 290-296, 2005.
21. Kapfer C, Seidl AH, Schweizer H, Grothe B. Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci 5: 247-253, 2002.
22. Kavanagh GL, Kelly JB. Midline and lateral field sound localization in the ferret (Mustela putorius): contribution of the superior olivary complex. J Neurophysiol 67: 1643-1658, 1992.
23. Kim G, Kandler K. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6: 282-290, 2003.
24. Kim G, Kandler K. Synaptic changes underlying the strengthening of GABA/ glycinergic connections in the developing lateral superior olive. Neuroscience 171: 924-933, 2010.
25. Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rubsamen R. Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23: 9199-9207, 2003.
26. Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rubsamen R. The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154: 160-170, 2008.
27. Kotak VC, Korada S, Schwartz IR, Sanes DH. A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18: 4646-4655, 1998.
28. Kros CJ. How to build an inner hair cell: challenges for regeneration. Hear Res 227: 3-10, 2007.
29. Leao KE, Leao RN, Sun H, Fyffe REW, Walmsley B. Hyperpolarizationactivated currents are differentially expressed in mice brainstem auditory nuclei. J Physiol 576: 849-864, 2006.
30. Leao RN, Oleskevich S, Sun H, Bautista M, Fyffe RE, Walmsley B. Differences in glycinergic mIPSCs in the auditory brain stem of normal and congenitally deaf neonatal mice. J Neurophysiol 91: 1006-1012, 2004.
31. Li P, Rudolph U, Huntsman MM. Long-term sensory deprivation selectively rearranges functional inhibitory circuits in mouse barrel cortex. Proc Natl Acad Sci U S A 106: 12156-12161, 2009.
32. Lu T, Rubio ME, Trussell LO. Glycinergic transmission shaped by the corelease of GABA in a mammalian auditory synapse. Neuron 57: 524-535, 2008.
33. Lynch JW. Native glycine receptor subtypes and their physiological roles. Neuropharmacology 56: 303-309, 2009.
34. Magnusson AK, Kapfer C, Grothe B, Koch U. Maturation of glycinergic inhibition in the gerbil medial superior olive after hearing onset. J Physiol 568: 497-512, 2005.
35. Miko IJ, Nakamura PA, Henkemeyer M, Cramer KS. Auditory brainstem neural activation patterns are altered in EphA4-and ephrin-B2-deficient mice. J Comp Neurol 505: 669-681, 2007.
36. Moore MJ, Caspary DM. Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3: 237-242, 1983.
37. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7: 17-23, 2004.
38. Noh J, Seal RP, Garver JA, Edwards RH, Kandler K. Glutamate co-release at GABA/glycinergic synapses is crucial for the refinement of an inhibitory map. Nat Neurosci 13: 232-238, 2010.
39. Oleskevich S, Youssoufian M, Walmsley B. Presynaptic plasticity at two giant auditory synapses in normal and deaf mice. J Physiol 560: 709-719, 2004.
40. Park TJ, Grothe B, Pollak GD, Schuller G, Koch U. Neural delays shape selectivity to interaural intensity differences in the lateral superior olive. J Neurosci 16: 6554-6566, 1996.
41. Piechotta K, Weth F, Harvey RJ, Friauf E. Localization of rat glycine receptor alpha1 and alpha2 subunit transcripts in the developing auditory brainstem. J Comp Neurol 438: 336-352, 2001.
42. Sanes DH. The development of synaptic function and integration in the central auditory system. J Neurosci 13: 2627-2637, 1993.
43. Sanes DH, Friauf E. Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147: 46-58, 2000.
44. Sanes DH, Merickel M, Rubel EW. Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J Comp Neurol 279: 436-444, 1989.
45. Sanes DH, Rubel EW. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8: 682-700, 1988.
46. Sanes DH, Siverls V. Development and specificity of inhibitory terminal arborizations in the central nervous system. J Neurobiol 22: 837-854, 1991.
47. Sanes DH, Takacs C. Activity-dependent refinement of inhibitory connections. Eur J Neurosci 5: 570-574, 1993.
48. Schofield CM, Huguenard JR. GABA affinity shapes IPSCs in thalamic nuclei. J Neurosci 27: 7954-7962, 2007.
49. Smith PH, Joris PX, Carney LH, Yin TC. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304: 387-407, 1991.
50. Sonntag M, Englitz B, Kopp-Scheinpflug C, Rubsamen R. Early postnatal development of spontaneous and acoustically evoked discharge activity of principal cells of the medial nucleus of the trapezoid body: an in vivo study in mice. J Neurosci 29: 9510-9520, 2009.
51. Sterenborg JC, Pilati N, Sheridan CJ, Uchitel OD, Forsythe ID, Barnes-Davies M. Lateral olivocochlear (LOC) neurons of the mouse LSO receive excitatory and inhibitory synaptic inputs with slower kinetics than LSO principal neurons. Hear Res 270: 119-126, 2010.
52. Stuart GJ, Redman SJ. Voltage dependence of Ia reciprocal inhibitory currents in cat spinal motoneurones. J Physiol 420: 111-125, 1990.
53. Taschenberger H, von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20: 9162-9173, 2000.
54. Tollin DJ. The lateral superior olive: a functional role in sound source localization. Neuroscientist 9: 127-143, 2003.
55. Tollin DJ, Yin TCT. Interaural phase and level difference sensitivity in low-frequency neurons in the lateral superior olive. J Neurosci 25: 10648-10657, 2005.
56. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE. The origin of spontaneous activity in the developing auditory system. Nature 450: 50-55, 2007.
57. Wall MJ, Robert A, Howe JR, Usowicz MM. The speeding of EPSC kinetics during maturation of a central synapse. Eur J Neurosci 15: 785-797, 2002.
58. Wang Y, Manis PB. Short-term synaptic depression and recovery at the mature mammalian endbulb of Held synapse in mice. J Neurophysiol 100: 1255-1264, 2008.
59. Werthat F, Alexandrova O, Grothe B, Koch U. Experience-dependent refinement of the inhibitory axons projecting to the medial superior olive. Dev Neurobiol 68: 1454-1462, 2008.
60. Willott JF, Turner JG, Carlson S, Ding D, Seegers Bross L, Falls WA. The BALB/c mouse as an animal model for progressive sensorineural hearing loss. Hear Res 115: 162-174, 1998.
61. Youssoufian M, Couchman K, Shivdasani MN, Paolini AG, Walmsley B. Maturation of auditory brainstem projections and calyces in the congenitally deaf (dn/dn) mouse. J Comp Neurol 506: 442-451, 2008.