Regulation of Inhibitory Synapse Function in the Developing Auditory CNS

  • Dan H. Sanes
  • Emma C. Sarro
  • Anne E. Takesian
  • Chiye Aoki
  • Vibhakar C. Kotak


Auditory processing requires a balanced participation of synaptic inhibition and excitation. This balance is achieved during development, in part, through the refinement of inhibitory connections and the regulation of inhibitory functional properties. Here, we make the case that spontaneous and experience-driven activity contributes to these maturational events in the auditory brainstem and cortex. Using brain slice preparations, we selectively assessed the physiology and plasticity of central inhibitory transmission. Together, the results demonstrate that inhibitory synapse function is regulated at every central location examined. The sites of regulation involve presynaptic factors such as transmitter synthesis and release properties, as well as postsynaptic factors such as receptor subunit kinetics, KCC2 function, and long-term depression. We propose that reduced inhibitory strength following disuse is due to delayed development, and this may contribute the enhanced excitability.


Hearing Loss Inferior Colliculus GABAB Receptor Cochlear Nucleus Inhibitory Synapse 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



NIH DC006864 (DHS and VCK), DC008920 (AET), DC009729 (ECS), and NS41091, EY13145, P30 EY13079, DA009618-09 (CA)


  1. Adelsberger H, Garaschuk O, Konnerth A (2005) Cortical calcium waves in resting newborn mice. Nat Neurosci 8:988–990PubMedGoogle Scholar
  2. Aponte JE, Kotak VC, Sanes DH (1996) Decreased synaptic inhibition leads to dendritic hypertrophy prior to the onset of hearing. Auditory Neurosci 2:235–240Google Scholar
  3. Argence M, Saez I, Sassu R, Vassias I, Vidal PP, de Waele C (2006) Modulation of inhibitory and excitatory synaptic transmission in rat inferior colliculus after unilateral cochleectomy: an in situ and immunofluorescence study. Neuroscience 141:1193–1207PubMedGoogle Scholar
  4. Amin J, Weiss DS (1993) GABAA receptor needs two homologous domains of the beta-subunit for activation by GABA but not by pentobarbital. Nature 366:565–569PubMedGoogle Scholar
  5. Asako M, Holt AG, Griffith RD, Buras ED, Altschuler RA (2005) Deafness-related decreases in glycine-immunoreactive labeling in the rat cochlear nucleus. J Neurosci Res 81:102–109PubMedGoogle Scholar
  6. Backus KH, Deitmer JW, Friauf E (1998) Glycine-activated currents are changed by coincident membrane depolarization in developing rat auditory brainstem neurones. J Physiol (Lond) 507:783–794Google Scholar
  7. Balakrishnan V, Becker M, Löhrke S, Nothwang HG, Güresir E, Friauf E (2003) Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci 23:4134–4145PubMedGoogle Scholar
  8. Banay-Schwartz M, Lajtha A, Palkovits M (1989) Changes with aging in the levels of amino acids in rat CNS structural elements I. Glutamate and related amino acids. Neurochem Res 14:555–562PubMedGoogle Scholar
  9. Barnes EM Jr (1996) Use-dependent regulation of GABAA receptors. Int Rev Neurobiol 39:53–76PubMedGoogle Scholar
  10. Baumann SW, Baur R, Sigel E (2002) Forced subunit assembly in α1β2γ2 GABAA receptors. J Biol Chem 277:46020–46025PubMedGoogle Scholar
  11. Blaesse P, Guillemin I, Schindler J, Schweizer M, Delpire E, Khiroug L, Friauf E, Nothwang HG (2006) Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J Neurosci 26:10407–10419PubMedGoogle Scholar
  12. Bauer CA, Brozoski TJ, Holder TM, Caspary DM (2000) Effects of chronic salicylate on GABAergic activity in rat inferior colliculus. Hear Res 147:175–182PubMedGoogle Scholar
  13. Beutner D, Moser T (2001) The presynaptic function of mouse cochlear inner hair cells during development of hearing. J Neurosci 21:4593–4599PubMedGoogle Scholar
  14. Bledsoe SC Jr, Nagase S, Miller JM, Altschuler RA (1995) Deafness-induced plasticity in the mature central auditory system. NeuroReport 7:225–229PubMedGoogle Scholar
  15. Bock GR, Webster WR (1974) Spontaneous activity of single units in the inferior colliculus of anesthetized cats. Brain Res 76:150–154PubMedGoogle Scholar
  16. Bormann J, Hamill OP, Sakmann B (1987) Mechanism of anion permeation through channels gated by glycine and γ-aminobutyric acid in mouse cultured spinal neurones. J Physiol (Lond) 385:243–286Google Scholar
  17. Brandt A, Striessnig J, Moser T (2003) CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J Neurosci 23:10832–10840PubMedGoogle Scholar
  18. Brückner S, Rübsamen R (1995) Binaural response characteristics in isofrequency sheets of the gerbil inferior colliculus. Hear Res 86:1–14PubMedGoogle Scholar
  19. Buras ED, Holt AG, Griffith RD, Asako M, Altschuler RA (2006) Changes in glycine immunoreactivity in the rat superior olivary complex following deafness. J Comp Neurol 494:179–189PubMedGoogle Scholar
  20. Burrone J, Murthy VN (2003) Synaptic gain control and homeostatsis. Curr Opinion Neurobiol 13:560–567Google Scholar
  21. Calford MB, Rajan R, Irvine DR (1993) Rapid changes in the frequency tuning of neurons in cat auditory cortex resulting from pure-tone-induced temporary threshold shift. Neuroscience 55:953–964PubMedGoogle Scholar
  22. Caspary DM, Raza A, Lawhorn Armour BA, Pippin J, Arneric SP (1990) Immunocytochemical and neurochemical evidence for age-related loss of GABA in the inferior colliculus: implications for neural presbycusis. J Neurosci 10:2363–2372PubMedGoogle Scholar
  23. Caspary DM, Holder TM, Hughes LF, Milbrandt JC, McKernan RM, Naritoku DK (1999) Age-related changes in GABA(A) receptor subunit composition and function in rat auditory system. Neuroscience 93:307–312PubMedGoogle Scholar
  24. Caspary DM, Schatteman TA, Hughes LF (2005) Age-related changes in the inhibitory response properties of dorsal cochlear nucleus output neurons: role of inhibitory inputs. J Neurosci 25:10952–10959PubMedGoogle Scholar
  25. Caspary DM, Milbrandt JC, Helfert RH (1995) Central auditory aging: GABA changes in the inferior colliculus. Exp Gerontol 30:349-360.PubMedGoogle Scholar
  26. Caspary DM, Ling L, Turner JG, Hughes LF (2008) Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. J Exp Biol 211:1781–1791PubMedGoogle Scholar
  27. Chagnac-Amitai Y, Connors BW (1989) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J Neurophysiol 61:747–758PubMedGoogle Scholar
  28. Chandrasekaran AR, Plas DT, Gonzalez E, Crair MC (2005) Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J Neurosci 25:6929–6938PubMedGoogle Scholar
  29. Chang EH, Kotak VC, Sanes DH (2003) Long-term depression of synaptic inhibition is expressed postsynaptically in the developing auditory system. J Neurophysiol 90:1479–1488PubMedGoogle Scholar
  30. Chen QC, Jen PH (2000) Bicuculline application affects discharge patterns, rate-intensity functions, and frequency tuning characteristics of bat auditory cortical neurons. Hear Res 150:161–174PubMedGoogle Scholar
  31. Chih B, Engelman H, Scheiffele P (2005) Control of excitatory and inhibitory synapse formation by neuroligins. Science 307:1324–1328PubMedGoogle Scholar
  32. Clayton GH, Owens GC, Wolff JS, Smith RL (1998) Ontogeny of cation-Cl cotransporter expression in rat neocortex. Brain Res Dev Brain Res 109:281–292PubMedGoogle Scholar
  33. Connolly CN, Wooltorton JR, Smart TG, Moss SJ (1996) Subcellular localization of gamma-aminobutyric acid type A receptors is determined by receptor beta subunits. Proc Natl Acad Sci USA 93:9899–9904PubMedGoogle Scholar
  34. Cook RD, Hung TY, Miller RL, Smith DW, Tucci DL (2002) Effects of conductive hearing loss on auditory nerve activity in gerbil. Hear Res 164:127–137PubMedGoogle Scholar
  35. Cruikshank SI, Rose HJ, Metherate R (2002) Auditory thalamocrotical synaptic transmission in vitro. J Neurophysiol 87:361–384PubMedGoogle Scholar
  36. Delpire E, Rauchman MI, Beier DR, Hebert SC, Gullans SR (1994) Molecular cloning and chromosome localization of a putative basolateral Na(+)-K(+)-2Cl(-) cotransporter from mouse inner medullary collecting duct (mIMCD-3) cells. J Biol Chem 269:25677–25683PubMedGoogle Scholar
  37. DeFazio RA, Keros S, Quick MW, Hablitz JJ (2000) Potassium-couple chloride cotransport controls intracellular chloride in rat neocortical pyramidal neurons. J Neurosci 20:8069-8076.PubMedGoogle Scholar
  38. Ehrlich I, Lohrke S, Friauf E (1999) Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent Cl regulation. J Physiol 520:121–137PubMedGoogle Scholar
  39. Ene FA, Kalmbach A, Kandler K (2007) Metabotropic glutamate receptors in the lateral superior olive activate TRP-like channels: age- and experience-dependent regulation. J Neurophysiol 97:3365–3375PubMedGoogle Scholar
  40. Ene FA, Kullmann PH, Gillespie DC, Kandler K (2003) Glutamatergic calcium responses in the developing lateral superior olive: receptor types and their specific activation by synaptic activity patterns. J Neurophysiol 90:2581–2591PubMedGoogle Scholar
  41. Farrant M, Kaila K (2007) The cellular, molecular and ionic basis of GABA(A) receptor signalling. Prog Brain Res 160:59–87PubMedGoogle Scholar
  42. Firzlaff U, Schuller G (2001) Motion processing in the auditory cortex of the rufous horseshoe bat: role of GABAergic inhibition. Eur J NeuroSci 14:1687–1701PubMedGoogle Scholar
  43. Fitzgerald KK, Sanes DH (2001) The development of stimulus coding in the auditory system. In: Jahn E, Santos-Sacchi J (eds) Physiology of the Ear, 2nd edn. San Diego, Singular PublishingGoogle Scholar
  44. Foeller E, Vater M, Kössl M (2001) Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2:279–296PubMedGoogle Scholar
  45. Fritschy JM, Brünig I (2003) Formation and plasticity of GABAergic synapses: physiological mechanisms and pathophysiological implications. Pharmacol Ther 98:299–323PubMedGoogle Scholar
  46. Franklin SR, Brunso-Bechtold JK, Henkel CK (2008) Bilateral cochlear ablation in postnatal rat disrupts development of banded pattern of projections from the dorsal nucleus of the lateral lemniscus to the inferior colliculus. Neurosci 154:346–354Google Scholar
  47. Gabriele ML, Brunso-Bechtold JK, Henkel CK (2000a) Development of afferent patterns in the inferior colliculus of the rat: projection from the dorsal nucleus of the lateral lemniscus. J Comp Neur 416:368–382PubMedGoogle Scholar
  48. Gabriele ML, Brunso-Bechtold JK, Henkel CK (2000b) Plasticity in the development of afferent patterns in the inferior colliculus of the rat after unilateral cochlear ablation. J Neurosci 20:6939–6949PubMedGoogle Scholar
  49. Garaschuk O, Linn J, Eilers J, Konnerth A (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3:452–9PubMedGoogle Scholar
  50. Gillespie DC, Kim G, Kandler K (2005) Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci 8:332–338PubMedGoogle Scholar
  51. Gleich O, Hamann I, Klump GM, Kittel M, Strutz J (2003) Boosting GABA improves impaired auditory temporal resolution in the gerbil. NeuroReport 14:1877–1880PubMedGoogle Scholar
  52. Heynen AJ, Yoon BJ, Liu CH, Chung HJ, Huganir RL, Bear MF (2003) Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci 6:854–862PubMedGoogle Scholar
  53. Holt AG, Asako M, Lomax CA, MacDonald JW, Tong L, Lomax MI, Altschuler RA (2005) Deafness-related plasticity in the inferior colliculus: gene expression profiling following removal of peripheral activity. J Neurochem 93:1069–1086PubMedGoogle Scholar
  54. Horikawa J, Hosokawa Y, Kubota M, Nasu M, Taniguchi I (1996) Optical imaging of spatiotemporal patterns of glutamatergic excitation and GABAergic inhibition in the guinea-pig auditory cortex in vivo. J Physiol 497:629–638PubMedGoogle Scholar
  55. Hübner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001) Disruption of KCC2 reveals an essential role of K–Cl cotransport already in early synaptic inhibition. Neuron 30:515–524PubMedGoogle Scholar
  56. Jones TA, Leake PA, Snyder RL, Stakhovskaya O, Bonham B (2007) Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J Neurophysiol 98:1898–1908PubMedGoogle Scholar
  57. Kakazu Y, Akaike N, Komiyama S, Nabekura J (1999) Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19:2843–2851PubMedGoogle Scholar
  58. Kanaka C, Ohno K, Okabe A, Kuriyama K, Itoh T, Fukuda A, Sato K (2001) The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1, 2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 104:933–946PubMedGoogle Scholar
  59. Kandler K, Clause A, Noh J (2009) Tonotopic reorganization of developing auditory brainstem circuits. Nat Neurosci 12:711–717PubMedGoogle Scholar
  60. Kapfer C, Seidl AH, Schweizer H, Grothe B (2002) Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons. Nat Neurosci 5:247–253PubMedGoogle Scholar
  61. Kazaku I, Akaike N, Komiyama S, Nabekura J (1999) Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19:2843–2851.PubMedGoogle Scholar
  62. Kil J, Kageyama GH, Semple MN, Kitzes LM (1995) Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil. J Comp Neurol 353:317–340PubMedGoogle Scholar
  63. Kilman V, van Rossum MC, Turrigiano GG (2002) Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J Neurosci 22:1328–1337PubMedGoogle Scholar
  64. Kim G, Kandler K (2003) Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6:282–290PubMedGoogle Scholar
  65. Kimura M, Eggermont JJ (1999) Effects of acute pure tone induced hearing loss on response properties in three auditory cortical fields in cat. Hear Res 135:146–162PubMedGoogle Scholar
  66. Kitzes LM, Kageyama GH, Semple MN, Kil J (1995) Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 353:341–363PubMedGoogle Scholar
  67. Kitzes LM, Semple MN (1985) Single-unit responses in the inferior colliculus: effects of neonatal unilateral cochlear ablation. J Neurophysiol 53:1483–1500PubMedGoogle Scholar
  68. Klinke R, Kral A, Heid S, Tillein J, Hartmann R (1999) Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation. Science 285:1729–1733PubMedGoogle Scholar
  69. Koerber KC, Pfeiffer RR, Warr WB, Kiang NY (1966) Spontaneous spike discharges from single units in the cochlear nucleus after destruction of the cochlea. Exp Neurol 16:119–130PubMedGoogle Scholar
  70. Komatsu Y (1994) Age-dependent long-term potentiation of inhibitory synaptic transmission in rat visual cortex. J Neurosci 14:6488–6499PubMedGoogle Scholar
  71. Korada S, Schwartz IL (1999) Development of GABA, glycine and their receptors in the auditory brainstem of gerbil: a light and electron microscopic study. J Comp Neurol 409:664–681PubMedGoogle Scholar
  72. Kotak VC, Sanes DH (1995) Synaptically evoked prolonged depolarizations in the developing auditory system. J Neurophysiol 74:1611–1620PubMedGoogle Scholar
  73. Kotak VC, Sanes DH (1996) Developmental influence of glycinergic inhibition: Regulation of NMDA- mediated EPSPs. J Neurosci 16:1836–1843PubMedGoogle Scholar
  74. Kotak VC, Korada S, Schwartz IR, Sanes DH (1998) A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18:4646–4655PubMedGoogle Scholar
  75. Kotak VK, Sanes DH (2000) Long-Lasting Inhibitory Synaptic Depression is Age- and Calcium-Dependent. J Neurosci 20:5820–5826PubMedGoogle Scholar
  76. Kotak VC, DiMattina C, Sanes DH (2001) GABAB and Trk receptor signaling mediates long-lasting inhibitory synaptic depression. J Neurophysiol 86:536–540PubMedGoogle Scholar
  77. Kotak VC, Sanes DH (2002) Postsynaptic kinase signaling underlies inhibitory synaptic plasticity. J Neurobiol 53:36–43PubMedGoogle Scholar
  78. Kotak VC, Fujisawa S, Lee FA, Karthikeyan O, Aoki C, Sanes DH (2005) Hearing loss raises excitability in the auditory cortex. J Neurosci 25:3908–3918PubMedGoogle Scholar
  79. Kotak VC, Sadahiro M, Fall CP (2007) Developmental expression of endogenous oscillations and waves in the auditory cortex involves calcium, gap junctions, and GABA. Neurosci 146:1629–1639Google Scholar
  80. Kotak VC, Takesian AE, Sanes DH (2008) Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb Cortex 18:2098–2108PubMedGoogle Scholar
  81. Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2000) Congenital auditory deprivation reduces synaptic activity within the auditoy cortex in a layer specific manner. Cereb Cortex 10:714–726PubMedGoogle Scholar
  82. Kral A, Tillein J, Peter Hubka P, Schiemann D, Heid S, Hartmann R (2009) Spatiotemporal patterns of cortical activity with bilateral cochlear implants in congenital deafness. J Neurosci 29:811–827PubMedGoogle Scholar
  83. Leao RN, Berntson A, Forsythe ID, Walmsley B (2004a) Reduced low-voltage activated K+ conductances and enhanced central excitability in a congenitally deaf (dn/dn) mouse. J Physiol 559:25–33PubMedGoogle Scholar
  84. Leao RN, Oleskevich S, Sun H, Bautista M, Fyffe RE, Walmsley B (2004b) Differences in glycinergic mIPSCs in the auditory brain stem of normal and congenitally deaf neonatal mice. J Neurophysiol 91:1006–1012PubMedGoogle Scholar
  85. Lee DS, Lee JS, Oh SH, Kim SK, Kim JW, Chung JK, Lee MC, Kim CS (2001) Cross-modal plasticity and cochlear implants. Nature 409:149–150PubMedGoogle Scholar
  86. Leventhal AG, Youngchang W, Mingliang Pu, Yifeng Z, Yuanye M (2003) GABA and its agonists improved visual cortical function in senescent monkeys. Science 300:812-815.PubMedGoogle Scholar
  87. Levinson JN, Chery N, Huang K, Wong TP, Gerrow K, Kang R, Prange O, Wang YT, El-Husseini A (2005) Neuroligins mediate excitatory and inhibitory synapse formation: involvement of PSD-95 and neurexin-1beta in neuroligin-induced synaptic specificity. J Biol Chem 280:17312–17319PubMedGoogle Scholar
  88. Li MX, Jia M, Jiang H, Dunlap V, Nelson PG (2001) Opposing actions of protein kinase A and C mediate Hebbian synaptic plasticity. Nat Neurosci 4:871–872PubMedGoogle Scholar
  89. Ling LL, Hughes LF, Caspary DM (2005) Age-related loss of the GABA synthetic enzyme glutamic acid decarboxylase in rat primary auditory cortex. Neuroscience 132:1103–1113PubMedGoogle Scholar
  90. Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14:1486–1495PubMedGoogle Scholar
  91. Lu J, Karadhed M, Delpire E (1999) Developmental regulation of the neuronal-specific isoform of K–Cl cotranspoter KCC2 in postnatal rat brains. J Neurobiol 39:558–568PubMedGoogle Scholar
  92. Maffei A, Nelson SB, Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7:1353–1359PubMedGoogle Scholar
  93. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443:81–84PubMedGoogle Scholar
  94. Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563–574PubMedGoogle Scholar
  95. McCarthy MM, Auger AP, Perrot-Sinal TS (2002) Getting excited about GABA differences in the brain. Trends Neurosci 25:307–312PubMedGoogle Scholar
  96. McAlpine D, Martin RL, Mossop JE, Moore DR (1997) Response properties of neurones in the inferior colliculus of the monaurally-deafened ferret to acoustic stimulation of the intact ear. J Neurophysiol 78:767–779PubMedGoogle Scholar
  97. McFadden SL, Walsh EJ, McGee J (1996) Onset and development of auditory brainstem responses in the Mongolian gerbil (Meriones unguiculatus). Hear Res 100:68–79PubMedGoogle Scholar
  98. McKernan RM, Whiting PJ (1996) Which GABAA-receptor subtypes really occur in the brain? Trends Neuroscience 19:139–143Google Scholar
  99. Milbrandt JC, Albin RL, Caspary DM (1994) Age-related decrease in GABAB receptor binding in the Fischer 344 rat inferior colliculus. Neurobiol Aging 15:699–703PubMedGoogle Scholar
  100. Milbrandt JC, Hunter C, Caspary DM (1997) Alterations of GABAA receptor subunit mRNA levels in the aging Fischer 344 rat inferior colliculus. J Comp Neurol 379:455–465PubMedGoogle Scholar
  101. Möhler H (2006) GABAA receptor diversity and pharmacology. Cell Tissue Res 326:505–516PubMedGoogle Scholar
  102. Moore DR (1992) Trophic influences of excitatory and inhibitory synapses on neurones in the auditory brain stem. Neuro Report 3:269–272Google Scholar
  103. Moore MJ, Caspary DM (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J Neurosci 3:237–42PubMedGoogle Scholar
  104. Moore CM, Vollmer M, Leake PA, Snyder RL, Rebscher SJ (2002) The effects of chronic intracochlear electrical stimulation on inferior colliculus spatial representation in adult deafened cats. Hear Res 164:82–96PubMedGoogle Scholar
  105. Morishita W, Sastry BR (1991) Chelation of postsynaptic Ca2+ facilitates long-term potentiation of hippocampal IPSPs. NeuroReport 2:533–6PubMedGoogle Scholar
  106. Mossop JE, Wilson MJ, Caspary DM, Moore DR (2000) Down-regulation of inhibition following unilateral deafening. Hear Res 147:183–187PubMedGoogle Scholar
  107. Müller CM, Scheich H (1988) Contribution of GABAergic inhibition to the response characteristics of auditory units in the avian forebrain. J Neurophysiol 59:1673–1689PubMedGoogle Scholar
  108. Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H (2004) Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7:17–23PubMedGoogle Scholar
  109. Nishimaki T, Jang IS, Ishibashi H, Yamaguchi J, Nabekura J (2007) Reduction of metabotropic glutamate receptor-mediated heterosynaptic inhibition of developing MNTB-LSO inhibitory synapses. Eur J NeuroSci 26:323–330PubMedGoogle Scholar
  110. Norena AJ, Eggermont JJ (2003) Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear Res 183:137–153PubMedGoogle Scholar
  111. Norena AJ, Tomita M, Eggermont JJ (2003) Neural changes in cat auditory cortex after a transient pure-tone trauma. J Neurophysiol 90:2387–2401PubMedGoogle Scholar
  112. Nusser Z, Cull-Candy S, Farrant M (1997) Differences in synaptic GABAA receptor number underlie variation in GABA mini amplitude. Neuron 19:697–709PubMedGoogle Scholar
  113. Nusser Z, Hajos N, Somogyi P, Mody I (1998) Increased number of synaptic GABAA receptors underlies potentiation at hippocampal inhibitory synapses. Nature 395:172–177PubMedGoogle Scholar
  114. Oda Y, Charpier S, Murayama Y, Suma C, Korn H (1995) Long-term potentiation of glycinergic inhibitory synaptic transmission. J Neurophysiol 74:1056–1074PubMedGoogle Scholar
  115. Oda Y, Kawasaki K, Morita M, Korn H, Matsui H (1998) Inhibitory long-term potentiation underlies auditory conditioning of goldfish escape behavior. Nature 394(6689):182–185PubMedGoogle Scholar
  116. Oleskevich S, Walmsley B (2002) Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J Physiol 540:447–455PubMedGoogle Scholar
  117. Oswald AM, Schiff ML, Reyes AD (2006) Synaptic mechanisms underlying auditory processing. Curr Opin Neurobiol 16:371–376PubMedGoogle Scholar
  118. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414–6423PubMedGoogle Scholar
  119. Payne JA (1997) Functional characterization of the neuronal-specific K–Cl cotransporter: implications for [K+]o regulation. Am J Physiol 273:C1516–C1525PubMedGoogle Scholar
  120. Payne JA, Stevenson TJ, Donaldson LF (1996) Molecular characterization of a putative K–Cl cotransporter in rat brain. J Biol Chem 27:16245–16252Google Scholar
  121. Payne JA, Rivera C, Voipio J, Kaila K (2003) Cation-chloride co-transporters in neuronal communication, development, and trauma. Trends Neurosci 26:199–206PubMedGoogle Scholar
  122. Paysan J, Kossel A, Bolz J, Fritschy JM (1997) Area-specific regulation of gamma-aminobutyric acid type A receptor subtypes by thalamic afferents in developing rat neocortex. Proc Natl Acad Sci 94:6995-7000.PubMedGoogle Scholar
  123. Plotkin MD, Snyder EY, Hebert SC, Delpire E (1997) Expression of the Na–K–2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA’s excitatory role in immature brain. J Neurobiol 33:781–795PubMedGoogle Scholar
  124. Pollak GD, Burger RM, Park TJ, Klug A, Bauer EE (2002) Roles of inhibition for transforming binaural properties in the brainstem auditory system. Hear Res 168:60–78PubMedGoogle Scholar
  125. Pollak GD, Burger RM, Klug A (2003) Dissecting the circuitry of the auditory system. Trends Neurosci 26:33–39PubMedGoogle Scholar
  126. Raggio MW, Schreiner CE (1999) Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III. Activation patterns in short- and long-term deafness. J Neurophysiol 82:3506–3526PubMedGoogle Scholar
  127. Raggio MW, Schreiner CE (2003) Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation: IV. Activation pattern for sinusoidal stimulation. J Neurophysiol 89:3190–3204PubMedGoogle Scholar
  128. Rajan R (1998) Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1:138–143PubMedGoogle Scholar
  129. Rajan R (2001) Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. Cereb Cortex 11:171–182PubMedGoogle Scholar
  130. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl cotransporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397:251–255PubMedGoogle Scholar
  131. Romand R (1992) Development of Auditory and Vestibular Systems 2. Elsevier, AmsterdamGoogle Scholar
  132. Russell FA, Moore DR (1995) Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal. J Comp Neurol 352:607–625PubMedGoogle Scholar
  133. Salvi RJ, Wang J, Ding D (2000) Auditory plasticity and hyperactivity following cochlear damage. Hear Res 147:261–274PubMedGoogle Scholar
  134. Sanes DH, Geary WA, Wooten GF, Rubel EW (1987) Quantitative distribution of the glycine receptor in the auditory brain stem of the gerbil. J Neurosci 7:3793–802PubMedGoogle Scholar
  135. Sanes DH, Rubel EW (1988) The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8:682–700PubMedGoogle Scholar
  136. Sanes DH, Siverls V (1991) Development and specificity of inhibitory terminal arborizations in the central nervous system. J Neurobiol 22:837–54PubMedGoogle Scholar
  137. Sanes DH, Chokshi P (1992) Glycinergic transmission influences the development of dendritic shape. Neuro Report 3:323–326Google Scholar
  138. Sanes DH, Markowitz S, Bernstein J, Wardlow J (1992) The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J Comp Neurol 321:637–644PubMedGoogle Scholar
  139. Sanes DH (1993) The development of synaptic function and integration in the central auditory system. J Neurosci 13:2627–37PubMedGoogle Scholar
  140. Sanes DH, Takács C (1993) Activity-dependent refinement of inhibitory connections. Eur J NeuroSci 5:570–574PubMedGoogle Scholar
  141. Sanes DH, Harris WA, Reh TA (2006) Development of the Nervous System, 2nd edn. Academic, San DiegoGoogle Scholar
  142. Sarro E, Kotak VC, Sanes DH, Aoki C (2008) Hearing loss alters the subcellular distribution of presynaptic GAD and postsynaptic GABAA receptors in the auditory cortex. Cereb Cortex 18:2855–2867PubMedGoogle Scholar
  143. Seki S, Eggermont JJ (2003) Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear Res 180:28–38PubMedGoogle Scholar
  144. Semple MN, Kitzes LM (1985) Single-unit responses in the inferior colliculus: different consequences of contralateral and ipsilateral auditory stimulation. J Neurophysiol 53:1467–1482PubMedGoogle Scholar
  145. Shepherd RK, Baxi JH, Hardie NA (1999) Response of inferior colliculus neurons to electrical stimulation of the auditory nerve in neonatally deafened cats. J Neurophysiol 82:1363–1380PubMedGoogle Scholar
  146. Snyder RL, Sinex DG, McGee JD, Walsh EW (2000) Acute spiral ganglion lesions change the tuning and tonotopic organziation of cat inferior colliculus neurons. Hear Res 147:200–220PubMedGoogle Scholar
  147. Suneja SK, Potashner SJ, Benson CG (1998) Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp Neurol 151:273–288PubMedGoogle Scholar
  148. Syka J (2002) Plastic changes in the central auditory system after hearing loss, restoration of function, and during learning. Physiol Rev 82:601-636.PubMedGoogle Scholar
  149. Szczepaniak WS, Moller AR (1995) Evidence of decreased GABAergic influence on temporal integration in the inferior colliculus following acute noise exposure: a study of evoked potentials in the rat. Neurosci Let 196:77–80Google Scholar
  150. Takesian AE, Kotak VC, Sanes DH (2007) Sensorineural hearing loss disrupts Inhibitory short-term plasticity in the developing auditory cortex. Assoc Res Otolaryngol 30Google Scholar
  151. Tan AY, Zhang LI, Merzenich MM, Schreiner CE (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630–643PubMedGoogle Scholar
  152. Tang AH, Chai Z, Wang SQ (2007) Dark rearing alters the short-term synaptic plasticity in visual cortex. Neurosci Lett 422:49–53PubMedGoogle Scholar
  153. Tehrani MH, Barnes EM Jr (1991) Agonist-dependent internalization of gamma-aminobutyric acid A/benzodiazepine receptors in chick cortical neurons. J Neurochem 57:1307–1312PubMedGoogle Scholar
  154. Thornton S, Semple MN, Sanes DH (1999) Development of auditory motion processing in the gerbil inferior colliculus. Eur J NeuroSci 11:1414–1420Google Scholar
  155. Tollin DJ (2003) The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–143PubMedGoogle Scholar
  156. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50–55PubMedGoogle Scholar
  157. Tucci DL, Cant NB, Durham D (1999) Conductive hearing loss results in a decrease in central auditory system activity in the young gerbil. Laryngoscope 109:1359–1371PubMedGoogle Scholar
  158. Tucci DL, Cant NB, Durham D (2001) Effects of conductive hearing loss on gerbil central auditory system activity in silence. Hear Res 155:124–132PubMedGoogle Scholar
  159. Turrigiano G (2007) Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol 17:318–324PubMedGoogle Scholar
  160. Vale C, Sanes DH (2000) Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain. J Neurosci 20:1912–1921PubMedGoogle Scholar
  161. Vale C, Sanes DH (2002) The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus. Eur J NeuroSci 16:2394–2404PubMedGoogle Scholar
  162. Vale C, Schoorlemmer J, Sanes DH (2003) Deafness disrupts chloride transporter function and inhibitory synaptic transmission. J Neurosci 23:7516–7524PubMedGoogle Scholar
  163. Vale C, Juiz J, Moore D, Sanes DH (2004) Unilateral hearing loss produces greater loss of inhibition in the contralateral inferior colliculus. Eur J NeuroSci 20:2133–2140PubMedGoogle Scholar
  164. Vale C, Caminos E, Martinez-Galán JR, Juiz JM (2005) Expression and developmental regulation of the K+–Cl cotransporter KCC2 in the cochlear nucleus. Hear Res 206:107–115PubMedGoogle Scholar
  165. Wang J, Ding D, Salvi RJ (2002a) Functional reorganization in chinchilla inferior colliculus associated with chronic and acute cochlear damage. Hear Res 168:238–249PubMedGoogle Scholar
  166. Wang J, McFadden SL, Caspary D, Salvi R (2002b) Gamma-aminobutyric acid circuits shape response properties of auditory cortex neurons. Brain Res 19:219–231Google Scholar
  167. Wang J, Reichling DB, Kyrozis A, MacDermott AB (1994) Developmental loss of GABA- and glycine-induced depolarization and Ca2+ transients in embryonic rat dorsal horn neurons in culture. Eur J NeuroSci 6:1275–1280PubMedGoogle Scholar
  168. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442–446PubMedGoogle Scholar
  169. Wenthold RJ, Huie D, Altschuler RA, Reeks KA (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neurosci 22:897–912Google Scholar
  170. Wenthold RJ, Altschuler RA, Hampson DR (1990) Immunocytochemistry of neurotransmitter receptors. J Electron Microscop Tech 15:81–96Google Scholar
  171. Werthat F, Alexandrova O, Grothe B, Koch U (2008) Experience-dependent refinement of the inhibitory axons projecting to the medial superior olive. Dev Neurobiol 68:1454–1462PubMedGoogle Scholar
  172. Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28:1029–1040PubMedGoogle Scholar
  173. Williams JR, Sharp JW, Kumari VG, Wilson M, Payne JA (1999) The neuron-specific K-Cl cotransporter, KCC2. Antibody development and initial characterization of the protein. J Biol Chem 274:12656–12664PubMedGoogle Scholar
  174. Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The Distribution of 13 GABA, Receptor Subunit mRNAs in the Rat Brain. I. Telencephalon, Diencephalon, Mesencephalon. J Neurosci 12:1040–1062PubMedGoogle Scholar
  175. Woolf NK, Ryan AF (1984) The development of auditory function in the cochlea of the mongolian gerbil. Hear Res 13:277–283PubMedGoogle Scholar
  176. Woolf NK, Ryan AF (1985) Ontogeny of neural discharge patterns in the ventral cochlear nucleus of the mongolian gerbil. Dev Brain Res 17:131–147Google Scholar
  177. Wu SH, Kelly JB (1994) Physiological evidence for ipsilateral inhibition in the lateral superior olive: synaptic responses in mouse brain slice. Hear Res 73:57–64PubMedGoogle Scholar
  178. Wyatt RM, Balice-Gordon RJ (2003) Activity-dependent elimination of neuromuscular synapses. J Neurocytol 32:777–794PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Dan H. Sanes
    • 1
  • Emma C. Sarro
    • 1
  • Anne E. Takesian
    • 1
  • Chiye Aoki
    • 1
  • Vibhakar C. Kotak
    • 1
  1. 1.Center for Neural ScienceNew York UniversityNew YorkUSA

Personalised recommendations