Toward a Synthesis of Cellular Auditory Forebrain Functional Organization

  • Jeffery A. Winer
  • Christoph E. Schreiner


There is no global theory of auditory forebrain function since the facts available cannot support such an edifice. New technologies, some outlined in the previous chapters, have broadened the issues of functional organization and elevated the discussion to more global perspectives. In the following we are not attempting to provide a global synthesis. We rather address some questions preliminary to such a theory with the explicit view from the cellular level.


Auditory Cortex Inferior Colliculus GABAergic Neuron Basilar Membrane Cochlear Nucleus 
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.



anterior auditory field


auditory cortex


primary auditory cortex


gamma aminobutyric acid


inferior colliculus


medial geniculate body





This work was supported by United States Public Health Service grants R01 DC02260-16 (C.E.S.) and DC02319-30 (J.A.W.).


  1. Arcelli P, Frassoni C, Regondi MC, De Biasi, and Spreafico R (1997) GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? Brain Research Bulletin 42:27–37.PubMedCrossRefGoogle Scholar
  2. Atencio CA, Sharpee TO, and Schreiner CE (2009) Hierarchical computation in the canonical auditory cortical circuit. Proceedings of the National Academy of Sciences of the United States of America 106:21894–21899.PubMedCrossRefGoogle Scholar
  3. Atencio CA and Schreiner CE (2010a) Columnar connectivity and laminar processing in cat primary auditory cortex. Public Library of Science One 5:e9521.PubMedGoogle Scholar
  4. Atencio CA and Schreiner CE (2010b) Laminar diversity of dynamic sound processing in cat primary auditory cortex. Journal of Neurophysiology 103:192–205.PubMedCrossRefGoogle Scholar
  5. Bar-Yosef O and Nelken I (2007) The effects of background noise on the neural responses to natural sounds in cat primary auditory cortex. Frontiers in Computational Neuroscience 1:1:3, doi: 10.3389/neuro.3310/3003.2007.Google Scholar
  6. Briggs F and Callaway EM (2001) Layer-specific input to distinct cell types in layer 6 of monkey primary visual cortex. Journal of Neuroscience 21:3600–3608.PubMedGoogle Scholar
  7. Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. Journal of Neuroscience 3:2350–2364.PubMedGoogle Scholar
  8. Casseday JH, Schreiner CE, and Winer JA (2005) The inferior colliculus: past, present, and future. In: Winer JA and Schreiner CE (eds). The Inferior Colliculus. Springer, New York, pp. 626–640.CrossRefGoogle Scholar
  9. Cipolloni PB and Pandya DN (1991) Golgi, histochemical, and immunocytochemical analyses of the neurons of auditory-related cortices of the rhesus monkey. Experimental Neurology 114:104–122.PubMedCrossRefGoogle Scholar
  10. Clascá F, Llamas A, and Reinoso-Suárez F (2000) Cortical connections of the insular and adjacent parieto-temporal fields in the cat. Cerebral Cortex 10:371–399.PubMedCrossRefGoogle Scholar
  11. Crabtree JW, Collingridge GL, and Issac JTR (1998) A new intrathalamic pathway linking modality-related nuclei in the dorsal thalamus. Nature Neuroscience 1:389–394.PubMedCrossRefGoogle Scholar
  12. Crabtree JW, Spear PD, McCall MA, Tong L, Jones KR, and Kornguth SE (1986) Dose-response analysis of effects of antibodies to large ganglion cells on the cat’s retinogeniculate pathways. Journal of Neuroscience 6:1199–1210.PubMedGoogle Scholar
  13. Crook JM, Kisvárday ZF, and Eysel UT (1997) GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity. Visual Neuroscience 14:141–158.PubMedCrossRefGoogle Scholar
  14. Crook JM, Kisvárday ZF, and Eysel UT (1998) Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques. European Journal of Neuroscience 10:2056–2075.PubMedCrossRefGoogle Scholar
  15. Colavita F (1979) Temporal pattern discrimination in cats with insular-temporal lesions. Physiology & Behavior 18:513–521.CrossRefGoogle Scholar
  16. Colavita FB (1974) Insular-temporal lesions and vibrotactile temporal pattern discrimination in cats. Physiology & Behavior 12:215–218.CrossRefGoogle Scholar
  17. Colwell S (1975) Thalamocortical-corticothalamic reciprocity: a combined anterograde-retrograde tracer technique. Brain Research 92:443–449.PubMedCrossRefGoogle Scholar
  18. Davis KA (2002) Evidence of a functionally segregated pathway from dorsal cochlear nucleus to inferior colliculus. Journal of Neurophysiology 87:1824–1835.PubMedGoogle Scholar
  19. Diamond IT (1973) The evolution of the tectal-pulvinar system in mammals: structural and behavioural studies of the visual system. Symposia of the Zoological Society of London 33:205–233.Google Scholar
  20. Edeline JM (2003) The thalamo-cortical auditory receptive fields: regulation by the states of vigilance, learning and the neuromodulatory systems. Experimental Brain Research 153:554–572.CrossRefGoogle Scholar
  21. Eggermont JJ (1998) Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. Journal of Neurophysiology 80:2743–2764.PubMedGoogle Scholar
  22. Emri Z, Antal K, and Crunelli V (2003) The impacts of corticothalamic feedback on the output dynamics of a thalamocortical neurone model: the role of synapse location and metabotropic glutamate receptors. Neuroscience 117:229–239.PubMedCrossRefGoogle Scholar
  23. Emson PC (1983) Chemical Neuroanatomy, Raven Press, New York.Google Scholar
  24. Fitzpatrick DC, Olsen JF, and Suga N (1998) Connections among functional areas in the mustached bat auditory cortex. Journal of Comparative Neurology 391:366–396.PubMedCrossRefGoogle Scholar
  25. Fritz JB, Elhilai M, and Shamma SA (2007) Auditory attention - focusing the searchlight on sound. Current Opinions in Neurobiology 17:437–455.CrossRefGoogle Scholar
  26. Fukuda T, Kosaka T, Singer W, and Galuske RA (2006) Gap junctions among dendrites of cortical GABAergic neurons establish a dense and widespread intercolumnar network. Journal of Neuroscience 26:3454–3464.CrossRefGoogle Scholar
  27. Hackett TA, Preuss TM, and Kaas JH (2001) Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. Journal of Comparative Neurology 441:197–222.PubMedCrossRefGoogle Scholar
  28. Hallman EL, Schofield BR, and Lin C-S (1988) Dendritic morphology and axon collaterals of corticotectal, corticopontine, and callosal neurons in layer V of primary visual cortex of the hooded rat. Journal of Comparative Neurology 272:149–160.PubMedCrossRefGoogle Scholar
  29. Hsieh CY, Chen Y, Leslie FM, and Metherate R (2002) Postnatal development of NR2A and NR2B mRNA expression in rat auditory cortex and thalamus. Journal of the Association for Research in Otolaryngology 3:479–487.PubMedCrossRefGoogle Scholar
  30. Huang CL, Larue DT, and Winer JA (1999) GABAergic organization of the cat medial geniculate body. Journal of Comparative Neurology 415:368–392.PubMedCrossRefGoogle Scholar
  31. Huang CL and Winer JA (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. Journal of Comparative Neurology 427:302–331.PubMedCrossRefGoogle Scholar
  32. Imaizumi K, Lee CC, Linden JF, Winer JA, and Schreiner CE (2005) The anterior field of auditory cortex: neurophysiological and neuroanatomical organization. In: König R, Heil P, Budinger E, and Scheich H (eds). The Auditory Cortex. A Synthesis of Human and Animal Research. Lawrence Erlbaum Associates, New York, pp. 95–110.Google Scholar
  33. Imig TJ and Adrián HO (1977) Binaural columns in the primary auditory field (A1) of cat auditory cortex. Brain Research 138:241–257.PubMedCrossRefGoogle Scholar
  34. Imig TJ and Brugge JF (1978) Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat. Journal of Comparative Neurology 182:637–660.PubMedCrossRefGoogle Scholar
  35. Jenkins WM and Merzenich MM (1984) Role of cat primary auditory cortex for sound-localization behavior. Journal of Neurophysiology 52:819–847.PubMedGoogle Scholar
  36. Jones EG and Hendry SHC (1986) Colocalization of GABA and neuropeptides in neocortical neurons. Trends in Neurosciences 9:71–76.CrossRefGoogle Scholar
  37. Josephson EM and Morest DK (1998) A quantitative profile of the synapses on the stellate cell body and axon in the cochlear nucleus of the chinchilla. Journal of Neurocytology 27:841–864.PubMedCrossRefGoogle Scholar
  38. Kaas JH (1983) What, if anything is SI? Organization of first somatosensory area of cortex. Physiological Reviews 63:206–231.PubMedGoogle Scholar
  39. Kaas JH (1997) Topographic maps are fundamental to sensory processing. Brain Research Bulletin 44:107–112.PubMedCrossRefGoogle Scholar
  40. Kelly JB and Glazier SJ (1978) Auditory cortex lesions and discrimination of spatial location by the rat. Brain Research 145:315–321.PubMedCrossRefGoogle Scholar
  41. Kilgard MP and Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–1718.PubMedCrossRefGoogle Scholar
  42. King AJ (1997) Signal selection by cortical feedback. Current Biology 7:R85–R88.PubMedCrossRefGoogle Scholar
  43. King AJ and Nelken I (2009) Unraveling the principles of auditory cortical processing: can we learn from the visual system?. Nature Neuroscience 12:698–701.PubMedCrossRefGoogle Scholar
  44. Ko S, Zhao MG, Toyoda H, Qiu CS, and Zhuo M (2005) Altered behavioral responses to noxious stimuli and fear in glutamate receptor 5 (GluR5)- or GluR6-deficient mice. Journal of Neuroscience 25:977–984.PubMedCrossRefGoogle Scholar
  45. Kulesza RJ, Viñuela A, Saldaña E, and Berrebi AS (2002) Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hearing Research 168:12–24.PubMedCrossRefGoogle Scholar
  46. Kurt S, Crook JM, Ohl FW, Scheich H, and Schulze H (2006) Differential effects of iontophoretic in vivo application of GABAA-antagonists bicuculline and gabazine in sensory cortex. Hearing Research 212:224–235.PubMedCrossRefGoogle Scholar
  47. Lee CC, Schreiner CE, Imaizumi K, and Winer JA (2004) Tonotopic and heterotopic projection systems in physiologically defined auditory cortex. Neuroscience 128:871–887.PubMedCrossRefGoogle Scholar
  48. Lee CC and Winer JA (2005) Principles governing auditory forebrain connections. Cerebral Cortex 15:1804–1814.PubMedCrossRefGoogle Scholar
  49. LeVay S and Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Research 113:1–19.PubMedCrossRefGoogle Scholar
  50. Lübke J, Markram H, Frotscher M, and Sakmann B (1996) Frequency and dendritic distribution of autapses established by layer 5 pyramidal neurons in the developing rat neocortex: comparison with synaptic innervation of adjacent neurons of the same class. Journal of Neuroscience 16:3209–3218.PubMedGoogle Scholar
  51. Lund JS (1990) Excitatory and inhibitory circuiting and laminar mapping strategies in the primary visual cortex of the monkey. In: Edelman GM, Gall WE, and Cowan WM (eds). Signal and Sense: Local and Global Order in Perceptual Maps. Wiley-Liss, New York, pp. 51–82.Google Scholar
  52. Lund JS, Griffiths S, Rumberger A, and Levitt JB (2001) Inhibitory synapse cover on the somata of excitatory neurons in macaque monkey visual cortex. Cerebral Cortex 11:783–795.PubMedCrossRefGoogle Scholar
  53. Malmierca MS, Rees A, and Le Beau FEN (1997) Ascending projections to the medial geniculate body from physiologically identified loci in the inferior colliculus. In: Syka J (ed). Acoustical Signal Processing in the Central Auditory System. Plenum, New York, pp. 295–302.Google Scholar
  54. Martinez LM, Wang Q, Reid RC, Pillai C, Alonso J-M, Sommer FT, and Hirsch JA (2005) Receptive field varies with layer in the primary visual cortex. Nature Neuroscience 8:372–379.PubMedCrossRefGoogle Scholar
  55. McMullen NT and de Venecia RK (1993) Thalamocortical patches in auditory neocortex. Brain Research 620:317–322.PubMedCrossRefGoogle Scholar
  56. Middlebrooks JC and Zook JM (1983) Intrinsic organization of the cat’s medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex. Journal of Neuroscience 3:203–225.PubMedGoogle Scholar
  57. Miller KD, Pinto DJ, and Simons DJ (2001a) Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex. Current Opinion in Neurobiology 11:488–497.PubMedCrossRefGoogle Scholar
  58. Miller LM, Escabí MA, Read HL, and Schreiner CE (2001b) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151–160.PubMedCrossRefGoogle Scholar
  59. Miller LM, Escabí MA, Read HL, and Schreiner CE (2002) Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. Journal of Neurophysiology 87:516–527.PubMedGoogle Scholar
  60. Miller LM, Escabí MA, and Schreiner CE (2001c) Feature selectivity and interneuronal cooperation in the thalamocortical system. Journal of Neuroscience 21:8136–8144.PubMedGoogle Scholar
  61. Miller LM and Schreiner CE (2000) Stimulus based state control in the thalamocortical system. Journal of Neuroscience 20:7011–7016.PubMedGoogle Scholar
  62. Montero VM and Zempel J (1985) Evidence for two types of GABA-containing interneurons in the A-laminae of the cat lateral geniculate nucleus: a double-label HRP and GABA-immunocytochemical study. Experimental Brain Research 60:603–609.Google Scholar
  63. Morel A and Kaas JH (1992) Subdivisions and connections of auditory cortex in owl monkeys. Journal of Comparative Neurology 318:27–63.PubMedCrossRefGoogle Scholar
  64. Morosan P, Rademacher J, Schleicher A, Amunts K, Schormann T, and Zilles K (2001) Human primary auditory cortex: cytoarchitectonic subdivisions and mapping into a spatial reference system. NeuroImage 13:694–701.CrossRefGoogle Scholar
  65. Müller CM (1988) Distribution of GABAergic perikarya and terminals in the centers of the higher auditory pathway of the chicken. Cell and Tissue Research 252:99–106.PubMedCrossRefGoogle Scholar
  66. Ohki K, Cheung S, Ch’ng YH, Kara P, Fabene PF, and Reid RC (2005) Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature 433:597–603.PubMedCrossRefGoogle Scholar
  67. Oliver DL, Winer JA, Beckius GE, and Saint Marie RL (1994) Morphology of GABAergic cells and axon terminals in the cat inferior colliculus. Journal of Comparative Neurology 340:27–42.PubMedCrossRefGoogle Scholar
  68. Olsen JF and Suga N (1991) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. Journal of Neurophysiology 65:1254–1274.PubMedGoogle Scholar
  69. Palmer LA, Rosenquist AC, and Tusa RJ (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. Journal of Comparative Neurology 177:237–256.PubMedCrossRefGoogle Scholar
  70. Perales M, Winer JA, and Prieto JJ (2006) Focal projections of cat auditory cortex to the pontine nuclei. Journal of Comparative Neurology 497:959–980.PubMedCrossRefGoogle Scholar
  71. Persico AM, Calia AE, Puglisi-Allegra S, Ventura R, Lucchese F, and Keller F (2000) Serotonin depletion and barrel cortex development: impact of growth impairment vs. serotonin effects on thalamocortical endings. Cerebral Cortex 10:181–191.PubMedCrossRefGoogle Scholar
  72. Peruzzi D, Bartlett E, Smith PH, and Oliver DL (1997) A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. Journal of Neuroscience 17:3766–3777.PubMedGoogle Scholar
  73. Peters A, Palay SL, and Webster H (1991) The Fine Structure of the Nervous System. The Neurons and their Supporting Cells. Oxford University Press, New York.Google Scholar
  74. Prieto JJ, Peterson BA, and Winer JA (1994) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). Journal of Comparative Neurology 344:349–382.PubMedCrossRefGoogle Scholar
  75. Prieto JJ and Winer JA (1999) Layer VI in cat primary auditory cortex (AI): Golgi study and sublaminar origins of projection neurons. Journal of Comparative Neurology 404:332–358.PubMedCrossRefGoogle Scholar
  76. Przybyszewski AW (1998) Does top-down processing help us to see? Current Biology 8:R135-R139.PubMedCrossRefGoogle Scholar
  77. Read HL, Winer JA, and Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proceedings of the National Academy of Sciences of the United States of America 98:8042–8047.PubMedCrossRefGoogle Scholar
  78. Reale RA and Imig TJ (1980) Tonotopic organization in auditory cortex of the cat. Journal of Comparative Neurology 192:265–291.PubMedCrossRefGoogle Scholar
  79. Rouiller EM, Rodrigues-Dagaeff C, Simm GM, de Ribaupierre Y, Villa AEP, and de Ribaupierre F (1989) Functional organization of the medial division of the medial geniculate body of the cat: tonotopic organization, spatial distribution of response properties and cortical connections. Hearing Research 39:127–146.PubMedCrossRefGoogle Scholar
  80. Schofield BR and Coomes DL (2004) Projections from the auditory cortex to the superior olivary complex in guinea pigs. European Journal of Neuroscience 19:2188–2200.PubMedCrossRefGoogle Scholar
  81. Schreiner CE (1995) Order and disorder in auditory cortical maps. Current Opinion in Neurobiology 5:489–496.PubMedCrossRefGoogle Scholar
  82. Sherman SM (2004) Interneurons and triadic circuitry of the thalamus. Trends in Neurosciences 27:670–675.PubMedCrossRefGoogle Scholar
  83. Shi C-J and Cassell MD (1997) Cortical, thalamic, and amygdaloid projections of rat temporal cortex. Journal of Comparative Neurology 382:153–175.PubMedCrossRefGoogle Scholar
  84. Smith DE and Moskowitz N (1979) Ultrastructure of layer IV of the primary auditory cortex of the squirrel monkey. Neuroscience 4:349–359.PubMedCrossRefGoogle Scholar
  85. Spreafico R, Frassoni C, Arcelli P, and De Biasi S (1994) GABAergic interneurons in the somatosensory thalamus of the guinea-pig: a light and ultrastructural immunocytochemical investigation. Neuroscience 59:961–973.PubMedCrossRefGoogle Scholar
  86. Steriade M (1996) Arousal: Revisiting the reticular activating system. Science 272:225–226.PubMedCrossRefGoogle Scholar
  87. Steriade M and Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37:563–576.PubMedCrossRefGoogle Scholar
  88. Storm-Mathisen J (1972) Glutamate decarboxylase in the rat hippocampal region after lesions of the afferent fibre systems: evidence that enzyme is localized in intrinsic neurons. Brain Research 40:215–235.PubMedCrossRefGoogle Scholar
  89. Striedter GF (2002) Brain homology and function: An uneasy alliance. Brain Research Bulletin 57:239–242.PubMedCrossRefGoogle Scholar
  90. Suga N (1978) Specialization of the auditory system for reception and processing of species-specific sounds. Federation of the American Society for Experimental Biology Proceedings 37:2342–2354.Google Scholar
  91. Szentágothai J (1975) The “module-concept” in cerebral cortex architecture. Brain Research 95:475–496.PubMedCrossRefGoogle Scholar
  92. Tusa RJ, Palmer LA, and Rosenquist AC (1981) Multiple cortical visual areas: visual field topography in the cat. In: Woolsey CN (ed). Cortical Sensory Organization, volume 2, Multiple Visual Areas. Humana Press, Clifton, pp. 1–31.Google Scholar
  93. Wakatsuki H, Gomi H, Kudoh M, Kimura S, Takahashi K, Takeda M, and Shibuki K (1998) Layer-specific NO dependence of long-term potentiation and biased NO release in layer V in the rat auditory cortex. Journal of Physiology 513:71–81.PubMedCrossRefGoogle Scholar
  94. Warr WB (1982) Parallel ascending pathways from the cochlear nucleus: neuroanatomical evidence of functional specialization. In: Neff WD (ed). Contributions to Sensory Physiology. Academic Press, New York, pp. 1–38.Google Scholar
  95. Weedman DL and Ryugo DK (1996) Projections from auditory cortex to the cochlear nucleus in rats: synapses on granule cell dendrites. Journal of Comparative Neurology 371:311–324.PubMedCrossRefGoogle Scholar
  96. Weinberg RJ (1997) Are topographic maps fundamental to sensory processing? Brain Research Bulletin 44:113–116.PubMedCrossRefGoogle Scholar
  97. Weinberger NM (1998) Tuning the brain by learning and by stimulation of the nucleus basalis. Trends in Cognitive Sciences 2:271–273.CrossRefPubMedGoogle Scholar
  98. Wenstrup JJ (2005) The tectothalamic system. In: Winer JA and Schreiner CE (eds). The Inferior Colliculus. Springer, New York, pp. 200–230.CrossRefGoogle Scholar
  99. Wenstrup JJ, Larue DT, and Winer JA (1994) Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei. Journal of Comparative Neurology 346:207–236.PubMedCrossRefGoogle Scholar
  100. Wever EG (1978) The Reptile Ear. Its Structure and Function. Princeton University Press, Princeton.Google Scholar
  101. White EL, Amitai Y, and Gutnick MJ (1994) A comparison of synapses onto the somata of intrinsically bursting and regular spiking neurons in layer V of rat SmI cortex. Journal of Comparative Neurology 342:1–14.PubMedCrossRefGoogle Scholar
  102. Wild JM, Karten HJ, and Frost BJ (1993) Connections of the auditory forebrain in the pigeon (Columba livia). Journal of Comparative Neurology 337:32–62.PubMedCrossRefGoogle Scholar
  103. Windhorst U (1990) Activation of Renshaw cells. Progress in Neurobiology 35:135–179.PubMedCrossRefGoogle Scholar
  104. Winer JA (1984) Anatomy of layer IV in cat primary auditory cortex (AI). Journal of Comparative Neurology 224:535–567.PubMedCrossRefGoogle Scholar
  105. Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, and Fay RR (eds). Springer Handbook of Auditory Research, volume 1, The Mammalian Auditory Pathway: Neuroanatomy. Springer, New York, pp. 222–409.Google Scholar
  106. Winer JA (2005) Three systems of descending projections to the inferior colliculus. In: Winer JA and Schreiner CE (eds). The Inferior Colliculus. Springer, New York, pp. 231–247.CrossRefGoogle Scholar
  107. Winer JA (2006) Decoding the auditory corticofugal systems. Hearing Research 212:1–8.PubMedCrossRefGoogle Scholar
  108. Winer JA, Diehl JJ, and Larue DT (2001) Projections of auditory cortex to the medial geniculate body of the cat. Journal of Comparative Neurology 430:27–55.PubMedCrossRefGoogle Scholar
  109. Winer JA, Kelly JB, and Larue DT (1999a) Neural architecture of the rat medial geniculate body. Hearing Research 130:19–41.PubMedCrossRefGoogle Scholar
  110. Winer JA and Larue DT (1996) Evolution of GABAergic circuitry in the mammalian medial geniculate body. Proceedings of the National Academy of Sciences of the United States of America 93:3083–3087.PubMedCrossRefGoogle Scholar
  111. Winer JA, Larue DT, Diehl JJ, and Hefti BJ (1998) Auditory cortical projections to the cat inferior colliculus. Journal of Comparative Neurology 400:147–174.PubMedCrossRefGoogle Scholar
  112. Winer JA, Larue DT, and Huang CL (1999b) Two systems of giant axon terminals in the cat medial geniculate body: convergence of cortical and GABAergic inputs. Journal of Comparative Neurology 413:181–197.PubMedCrossRefGoogle Scholar
  113. Winer JA, Larue DT, and Pollak GD (1995) GABA and glycine in the central auditory system of the mustache bat: structural substrates for inhibitory neuronal organization. Journal of Comparative Neurology 355:317–353.PubMedCrossRefGoogle Scholar
  114. Winer JA, Lee CC, Imaizumi K and Schreiner CE (2005a) Challenges to a neuroanatomical theory of forebrain auditory plasticity. In: Syka J and Merzenich MM (eds). Plasticity of the Central Auditory System and Processing of Complex Acoustic Signals. Springer, New York, pp. 109–127.CrossRefGoogle Scholar
  115. Winer JA, Miller LM, Lee CC, and Schreiner CE (2005b) Auditory thalamocortical transformation: structure and function. Trends in Neurosciences 28:255–263.PubMedCrossRefGoogle Scholar
  116. Winer JA and Prieto JJ (2001) Layer V in cat primary auditory cortex (AI): cellular architecture and identification of projection neurons. Journal of Comparative Neurology 434:379–412.PubMedCrossRefGoogle Scholar
  117. Winer JA, Saint Marie RL, Larue DT and Oliver DL (1996) GABAergic feedforward projections from the inferior colliculus to the medial geniculate body. Proceedings of the National Academy of Sciences of the United States of America 93:8005–8010.PubMedCrossRefGoogle Scholar
  118. Winer JA, Sally SL, Larue DT and Kelly JB (1999c) Origins of medial geniculate body projections to physiologically defined regions of rat auditory cortex. Hearing Research 130:42–61.PubMedCrossRefGoogle Scholar
  119. Winer JA, Wenstrup JJ and Larue DT (1992) Patterns of GABAergic immunoreactivity define subdivisions of the mustached bat’s medial geniculate body. Journal of Comparative Neurology 319:172–190.PubMedCrossRefGoogle Scholar
  120. Yingcharoen K, Rinvik E, Storm-Mathisen J, and Ottersen OP (1989) GABA, glycine, glutamate, aspartate and taurine in the perihypoglossal nuclei: an immunocytochemical investigation with particular reference to the issue of amino acid colocalization. Experimental Brain Research 78:345–357.CrossRefGoogle Scholar
  121. Zhang Y and Suga N (2005) Corticofugal feedback for collicular plasticity evoked by electric stimulation of the inferior colliculus. Journal of Neurophysiology 94:2676–2682.PubMedCrossRefGoogle Scholar
  122. Zirrinpar A and Callaway EM (2006) Local connections of specific types of layer 6 neurons in the rat visual cortex. Journal of Neurophysiology 95:1751–1761.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Division of Neurobiology, Department of Molecular and Cell BiologyUniversity of California at BerkeleyBerkeleyUSA
  2. 2.Coleman Memorial Laboratory, Department of OtolaryngologyW.M. Keck Center for Integrative Neuroscience, University of California, School of MedicineSan FranciscoUSA

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