Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Anatomy and Physiology of the Mammalian Auditory System

Living reference work entry
DOI: https://doi.org/10.1007/978-1-4614-7320-6_286-1

An auditory system is found in all classes of vertebrates, including fish, amphibians, reptiles and birds, and mammals. Although there are important similarities across classes, the system has evolved differently in the different groups. Even within the class of mammals, there are notable specializations, especially in echolocating mammals such as cetaceans and bats. Because one major objective in hearing research is to understand the structure and physiology of the human auditory system, this entry is restricted to an overview of the general plan of organization of the mammalian system. Insights gained from research in animals should aid in identifying the causes of hearing impairments in humans and represent an important step toward developing effective treatments.

The specific auditory stimulus consists of pressure waves arriving at the ear within a certain frequency range. This audible frequency range varies among species (e.g., humans, 0.02–20 kHz; rat, 0.25 to 70 kHz; mouse, 2–70...

Keywords

Glycine NMDA Kelly Acetylcholinesterase Corti 
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Notes

Acknowledgments

I am most thankful and indebted to Dr. Nell Cant for her suggestions and constructive criticisms on a previous version of the manuscript.

Financial support was provided by Spanish MINECO (BFU2009-07286) and EU (EUI2009-04083, in the framework of the ERA-NET Network of European Funding for Neuroscience Research).

References

  1. Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol 183:519–538PubMedGoogle Scholar
  2. Adams JC (1983) Cytology of periolivary cells and the organization of their projections in the cat. J Comp Neurol 215:2752–2789Google Scholar
  3. Aitkin LM, Dickhaus H, Schult W, Zimmermann M (1978) External nucleus of inferior colliculus, auditory and spinal somatosensory afferents and their interactions. J Neurophysiol 41:837–847PubMedGoogle Scholar
  4. Anderson LA, Malmierca MS, Wallace MN, Palmer AR (2006) Evidence for a direct, short latency projection from the dorsal cochlear nucleus to the auditory thalamus in the guinea pig. Eur J Neurosci 24:491–498PubMedGoogle Scholar
  5. Banks MI, Smith PH (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12:2819–2837PubMedGoogle Scholar
  6. Bartlett EL, Smith PH (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. J Neurophysiol 81:1999–2016PubMedGoogle Scholar
  7. Bartlett EL, Stark JM, Guillery RW, Smith PH (2000) Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 100:811–828PubMedGoogle Scholar
  8. Blaesse P, Ehrhardt S, Friauf E, Nothwang HG (2005) Developmental pattern of three vesicular glutamate transporters in the rat superior olivary complex. Cell Tissue Res 320:33–50PubMedGoogle Scholar
  9. Brawer JR, Morest DK, Kane EC (1974) The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155:251–300PubMedGoogle Scholar
  10. Brodal A (1981) Neurological anatomy in relation to clinical medicine, 3rd edn. Oxford University Press, OxfordGoogle Scholar
  11. Brown MC, Levine JL (2008) Dendrites of medial olivocochlear neurons in mouse. Neuroscience 154:147–159PubMedCentralPubMedGoogle Scholar
  12. Brown MC, Liberman MC, Benson TE, Ryugo DK (1988) Brainstem branches from olivocochlear axons in cats and rodents. J Comp Neurol 278:591–603PubMedGoogle Scholar
  13. Burton H, Jones EG (1976) The posterior thalamic region and its cortical projection in New World and Old World monkeys. J Comp Neurol 168:249–301PubMedGoogle Scholar
  14. Caicedo A, Herbert H (1993) Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. J Comp Neurol 328:377–392PubMedGoogle Scholar
  15. Cant NB, Benson CG (2003) Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei. Brain Res Bull 60:457–474PubMedGoogle Scholar
  16. Cant NB, Benson CG (2006) Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex. J Comp Neurol 495:511–528PubMedCentralPubMedGoogle Scholar
  17. Cant NB, Benson CG (2007) Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculatus. J Comp Neurol 503:432–453PubMedGoogle Scholar
  18. Casseday JH, Fremouw T, Covey E (2002) The inferior colliculus, a hub for the central audiotory system. In: Oertel D, Popper AN, Fay RR (eds) Springer handbook of auditory research. Springer, New YorkGoogle Scholar
  19. Cotillon N, Nafati M, Edeline JM (1999) Characteristics of reliable tone-evoke oscillations in the rat thalamo-cortical auditory system. Hear Res 142:113–130Google Scholar
  20. Covey E, Casseday JH (1991) The monoaural nuclei of the lateral lemniscus in an echolocating bat, parallel pathways for analyzing temporal features of sound. J Neurosci 11:3456–3470PubMedGoogle Scholar
  21. Dehmel S, Kopp-Scheinpflug C, Dörrscheidt GJ, Rübsamen R (2002) Electrophysiological characterization of the superior paraolivary nucleus in the Mongolian gerbil. Hear Res 172:18–36PubMedGoogle Scholar
  22. Doron NN, Ledoux JE (1999) Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat. J Comp Neurol 412:383–409PubMedGoogle Scholar
  23. Doucet JR, Ryugo DK (1997) Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J Comp Neurol 385:245–264PubMedGoogle Scholar
  24. Doucet JR, Ross AT, Gillespie MB, Ryugo DK (1999) Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus. J Comp Neurol 408:515–531PubMedGoogle Scholar
  25. Doucet JR, Molavi DL, Ryugo DK (2003) The source of corticocollicular and corticobulbar projections in area Te1 of the rat. Exp Brain Res 4:461–466Google Scholar
  26. Echteler SM, Fay RR, Popper AN (1994) Structure of the mammalian cochlea. In: Fay RR, Popper AN (eds) Comparative hearing, mammals. Springer, Berlin, pp 134–171Google Scholar
  27. Eggermont JJ (2001) Between sound and perception, reviewing the search for a neural code. Hear Res 157:1–42PubMedGoogle Scholar
  28. Fay RR (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay Associates, WinnetkaGoogle Scholar
  29. Fay RR, Popper AN (1994) Comparative hearing in mammals. In: Fay RR and Popper AN (Eds), Springer handbook of auditory research. Springer, New YorkGoogle Scholar
  30. Faye-Lund H (1985) The neocortical projection to the inferior colliculus in the albino rat. Anat Embryol (Berl) 173:53–70Google Scholar
  31. Faye-Lund H, Osen KK (1985) Anatomic of the inferior colliculus in rat. Anat Embryol 175:35–52Google Scholar
  32. Feliciano M, Potashner SJ (1995) Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem 65:1348–1357PubMedGoogle Scholar
  33. Friauf E (1993) Transient appearance of calbindin-D28k-positive neurons in the superior olivary complex of developing rats. J Comp Neurol 334:59–74Google Scholar
  34. Games KD, Winer JA (1988) Layer V in rat auditory cortex, projections to the inferior colliculus and contralateral cortex. Hear Res 34:1–25PubMedGoogle Scholar
  35. Guinan JJ, Norris BE, Guinan SS (1972) Single auditory units in the superior olivary complex, II. Locations of unit categories and tonotopic organization. Int J Neurosci 4:147–166Google Scholar
  36. Hefti BJ, Smith PH (2000) Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABA(A)blockade. J Neurophysiol 83:2626–2638PubMedGoogle Scholar
  37. Hefti BJ, Smith PH (2003) Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex. J Assoc Res Otolaryngol 4:106–121PubMedCentralPubMedGoogle Scholar
  38. Held H (1893) Die centralem Bahnen des Nervus acusticus bei der. Katz Arch Anat Abtheil 15:190–271Google Scholar
  39. Helfert RH, Aschoff A (1997) Superior olivary complex and nuclei of the lateral lemniscus. In: Ehret G, Romand R (eds) Anatomical and functional aspects of the cochlear nucleus. Oxford University Press, Oxford, pp 193–257Google Scholar
  40. Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 304:103–122PubMedGoogle Scholar
  41. Irvine DRF (1992) Physiology of the auditory brainstem. In: Popper AN, Fay RR (eds) Springer handbook of auditory pathway, neurophysiology. Springer, New York, pp 153–231Google Scholar
  42. Ito T, Oliver DL (2012) Patterns of synaptic organization send different messages to the thalamus. Front Neural Circuits 6:48. doi:103389/fncir201200048PubMedCentralPubMedGoogle Scholar
  43. Jones EG (2003) Chemically defined parallel pathways in the monkey auditory system. Ann N Y Acad Sci 999:218–233PubMedGoogle Scholar
  44. Jones EG (2007) The thalamus, vol II, 2nd edn. Cambridge University Press, Cambridge, pp 875–923Google Scholar
  45. Joris PX, Smith PH, Yin TCT (1998) Coincidence detection in the auditory system, 50 years after Jeffress. Neuron 21:1235–1238PubMedGoogle Scholar
  46. Kaas JH, Hackett TA (1998) Subdivisions of auditory cortex and levels of processing in primates. Audiol Neurootol 3:73–85PubMedGoogle Scholar
  47. Kasper EM, Larkman AU, Lubke J, Blakemore C (1994) Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets. J Comp Neurol 339:459–474PubMedGoogle Scholar
  48. Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69:416–431PubMedGoogle Scholar
  49. Kelly JB, Caspary DM (2005) Pharmacology of the inferior colliculus. In: Winer JA, Schreiner C (eds) The inferior colliculus. Springer, New York, pp 248–281Google Scholar
  50. King AJ, Jiang ZD, Moore DR (1998) Auditory brainstem projections to the ferret superior colliculus: anatomical contribution to the neural coding of sound azimuth. J Comp Neurol 390:342–365PubMedGoogle Scholar
  51. Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rübsamen R (2008) The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154:60–170Google Scholar
  52. Kulesza RJ Jr, Spirou GA, Berrebi AS (2003) Physiological response properties of neurons in the superior paraolivary nucleus of the rat. J Neurophysiol 89:2299–2312PubMedGoogle Scholar
  53. LeBeau FEN, Malmierca MS, Rees A (2001) Iontophoresis in vivo demonstrates a key role for GABAA- and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci 21:7303–7312PubMedGoogle Scholar
  54. Lee CC, Winer JA (2005) Principles governing auditory cortex connections. Cereb Cortex 15:1804–1814PubMedGoogle Scholar
  55. Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea, quantitative analysis with light and electron microscopy. J Comp Neurol 301:443–460PubMedGoogle Scholar
  56. Llano DA, Sherman SM (2008) Evidence for nonreciprocal organization of the mouse auditory thalamocortical-corticothalamic projection systems. J Comp Neurol 507:1209–1227PubMedGoogle Scholar
  57. Llano DA, Sherman SM (2009) Differences in intrinsic properties and local network connectivity of identified layer 5 and layer 6 adult mouse auditory corticothalamic neurons support a dual corticothalamic projection hypothesis. Cereb Cortex 19:2810–2826PubMedCentralPubMedGoogle Scholar
  58. Loftus B, Malmierca MS, Oliver DL (2008) The Cytoarchitecture of the inferior colliculus revisited: a common organization of the lateral cortex in rat and cat. Neuroscience 154:196–205PubMedCentralPubMedGoogle Scholar
  59. Lorente de Nó R (1981) The primary acoustic nuclei. Raven Press, New YorkGoogle Scholar
  60. Lu E, Llano DA, Sherman SM (2009) Different distributions of calbindin and calretinin immunostaining across the medial and dorsal divisions of the mouse medial geniculate body. Hear Res 257:16–23PubMedCentralPubMedGoogle Scholar
  61. Malmierca MS (2003) The structure and physiology of the rat auditory system: an overview. Int Rev Neurobiol 56:147–211PubMedGoogle Scholar
  62. Malmierca MS, Hackett TA (2010) Structural organization of the ascending auditory pathway. In: Moore DR (ed) The Oxford handbook of auditory science: the auditory brain. Oxford University Press, New York, pp 9–41Google Scholar
  63. Malmierca MS, Ryugo DK (2011) Descending connections of auditory cortex to the midbrain and brainstem. In: Winer JA, Schreiner CE (eds) The auditory cortex. Springer, New York, pp 189–208Google Scholar
  64. Malmierca MS, Ryugo DK (2012) Auditory system. In: Watson C, Paxinos G, Puelles L (eds) The mouse nervous system. Academic, Amsterdam, pp 607–645Google Scholar
  65. Malmierca MS, Blackstad TW, Osen KK, Karagülle T, Molowny RL (1993) The central nucleus of the inferior colliculus in rat, a Golgi and computer reconstruction study of neuronal and laminar structure. J Comp Neurol 333:1–27PubMedGoogle Scholar
  66. Malmierca MS, Rees A, LeBeau FEN, Bajaalie JG (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol 357:124–144PubMedGoogle Scholar
  67. Malmierca MS, LeBeau FEN, Rees A (1996) The topographical organization of descending projections from the central nucleus of the inferior colliculus in guinea pig. Hear Res 93:167–180PubMedGoogle Scholar
  68. Malmierca MS, Leergard TB, Bajo VM, Bjaalie JG (1998) Anatomic evidence of a 3-D mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in cat. J Neurosci 19:10603–10618Google Scholar
  69. Malmierca MS, Merchán M, Henkel CK, Oliver DL (2002) Direct projections from the dorsal cochlear nucleus to the auditory thalamus in rat. J Neurosci 22:10891–10897PubMedGoogle Scholar
  70. Malmierca MS, Saint Marie RL, Merchan MA, Oliver DL (2005) Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus: two patterns of convergence. Neuroscience 136:883–894PubMedGoogle Scholar
  71. Malmierca MS, Izquierdo MA, Cristaudo S, Hernández O, Pérez-González D, Covey E, Oliver DL (2008) A discontinuous tonotopic organization in the inferior colliculus of the rat. J Neurosci 28:4767–4776PubMedCentralPubMedGoogle Scholar
  72. Malmierca MS, Cristaudo S, Pérez-González D, Covey E (2009) Stimulus-specific adaptation in the inferior colliculus of the anesthetized rat. J Neurosci 29:5483–5493PubMedCentralPubMedGoogle Scholar
  73. Meltzer NE, Ryugo DK (2006) Projections from auditory cortex to cochlear nucleus: a comparative analysis of rat and mouse. Anat Rec A Discov Mol Cell Evol Biol 288:397–408PubMedCentralPubMedGoogle Scholar
  74. Merchán M, Aguilar LA, Lopez-Poveda EA, Malmierca MS (2005) The inferior colliculus of the rat: quantitative immunocytochemical study of GABA and glycine. Neuroscience 136:907–925PubMedGoogle Scholar
  75. Moore JK, Osen KK (1979) The human cochlear nuclei. In: Creutzfeld O, Scheich H, Schreiner C (eds) Exp Brain Res, Suppementum II, pp 36–44Google Scholar
  76. Morest DK (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 Res 9:288–311PubMedGoogle Scholar
  77. Mugnaini E, Osen KK, Dahl A-L, Friedrich VL Jr, Korte G (1980a) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. J Neurocytol 9:537–570PubMedGoogle Scholar
  78. Mugnaini E, Warr WB, Osen KK (1980b) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J Comp Neurol 191:581–606PubMedGoogle Scholar
  79. Oertel D (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61:497–519PubMedGoogle Scholar
  80. Oertel D, Young ED (2004) What's a cerebellar circuit doing in the auditory system? Trends Neurosci 27:104–110PubMedGoogle Scholar
  81. Oertel D, Wu SH, Garb MW, Dizack C (1990) Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J Comp Neurol 295:136–154PubMedGoogle Scholar
  82. Oliver DL, Morest DK (1984) The central nucleus of the inferior colliculus in the cat. J Comp Neurol 222:237–264PubMedGoogle Scholar
  83. Oliver DL, Ostapoff EM, Beckius GE (1999) Direct innervation of identified tectothalamic neurons in the inferior colliculus by axons from the cochlear nucleus. Neuroscience 93:643–658PubMedGoogle Scholar
  84. Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–483PubMedGoogle Scholar
  85. Osen KK, Mugnaini E, Dahl AL, Christiansen AH (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei. A reappraisal with emphasis on the cochlear granule cell system. Arch Ital Biol 122:169–212PubMedGoogle Scholar
  86. Osen KK, Ottersen OP, Størm-Mathisen J (1990) Colocalization of glicine-like and GABA-like inmunoreactivities, a semiquantitative study of individual neurons in the dorsal cochlear nucleus of cat. In: Ottersen OP, Størm-Mathissen J (eds) Glycine neurotransmission. Wiley, Chichester, pp 417–451Google Scholar
  87. Ota Y, Oliver DL, Dolan DF (2004) Frequency-specific effects on cochlear responses during activation of the inferior colliculus in the Guinea pig. J Neurophysiol 91:2185–2193PubMedGoogle Scholar
  88. Palombi PS, Caspary DM (1996) Responses of young and aged Fischer 344 rat inferior colliculus neurons to binaural tonal stimuli. Hear Res 100:59–67PubMedGoogle Scholar
  89. Peruzzi D, Bartlett E, Smith PH, Oliver DL (1997) A monosynaptic GABAergic input from the inferior colliculus to the medial geniculate body in rat. J Neurosci 17:3766–3777PubMedGoogle Scholar
  90. Rajan R (1990) Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization. Brain Res 506:192–204PubMedGoogle Scholar
  91. Rasmussen GL (1946) The olivary peduncle and other fiber projections of the superior olivary complex. J Comp Neurol 99:61–74Google Scholar
  92. Rietzel HJ, Friauf E (1998) Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390:20–40PubMedGoogle Scholar
  93. Riquelme R, Saldaña E, Osen KK, Ottersen OP, Merchán MA (2001) Colocalization of GABA and Glycine in the ventral nucleus of the lateral lemniscus in rat, an in situ hybridization and semiquantitative inmunocytochemical study. J Comp Neurol 432:409–424PubMedGoogle Scholar
  94. Rubio ME, Juiz JM (2004) Differential distribution of synaptic endings containing glutamate, glycine, and GABA in the rat dorsal cochlear nucleus. J Comp Neurol 477:253–272PubMedGoogle Scholar
  95. Rubio ME, Gudsnuk KA, Smith Y, Ryugo DK (2008) Revealing the molecular layer of the primate dorsal cochlear nucleus. Neuroscience 154:99–113PubMedCentralPubMedGoogle Scholar
  96. Ryugo DK, Parks TN (2003) Primary innervation of the avian and mammalian cochlear nucleus. Brain Res Bull 60:435–456PubMedGoogle Scholar
  97. Safieddine S, Eybalin M (1992) Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalins, and calcitonin gene-related peptide within efferent olivocochlear neurons in rats and guinea-pigs. Eur J Neurosci 4:981–992PubMedGoogle Scholar
  98. Safieddine S, Prior AM, Eybalin M (1997) Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig. Eur J Neurosci 9:356–367PubMedGoogle Scholar
  99. Saldaña E, Merchán MA (1992) Intrinsic and commissural connections of the rat inferior colliculus. J Comp Neurol 319:417–437PubMedGoogle Scholar
  100. Saldaña E, Feliciano M, Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 371:15–40PubMedGoogle Scholar
  101. Schofield BR (1995) Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. J Comp Neurol 360:135–149PubMedGoogle Scholar
  102. Schofield BR, Cant NB (1991) Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology. J Comp Neurol 314:645–670PubMedGoogle Scholar
  103. Schreiner CE, Langner G (1988) Coding of temporal patterns in the central auditory nervous system. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function. Wiley, New York, pp 337–340Google Scholar
  104. Schreiner CE, Langner G (1997) Laminar fine structure of frequency organization in auditory midbrain. Nature 388:383–386PubMedGoogle Scholar
  105. Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367–1395PubMedGoogle Scholar
  106. Sinex DG, Lopez DE, Warr WB (2001) Electrophysiological responses of cochlear root neurons. Hear Res 370:1–11Google Scholar
  107. Sivaramakrishnan S, Oliver DL (2001) Distinct K+ currents result in physiologically distinct cell types in the inferior colliculus of the rat. J Neurosci 21:2861–2877PubMedGoogle Scholar
  108. Slepecky NB (1996) Structure of the mammalian cochlea. In: Dallos P, Popper AN, Fay RR (eds) The cochlea, Springer handbook of auditory research. Springer, New York, pp 44–129Google Scholar
  109. Smith PH (1995) Structural and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J Neurophysiol 73:1653–1667PubMedGoogle Scholar
  110. Smith PH, Rhode WS (1989) Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J Comp Neurol 282:595–616PubMedGoogle Scholar
  111. Smith PH, Joris PX, Carney LH, Yin TCT (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304:387–407PubMedGoogle Scholar
  112. Sommer I, Lingenhöhl K, Friauf E (1993) Principal cells of the rat medial nucleus of the trapezoid body, an intracellular in vivo study of their physiology and morphology. Exp Brain Res 95:223–239PubMedGoogle Scholar
  113. Taranda J, Maison SF, Ballestero JA, Katz E, Savino J, Vetter DE, Boulter J, Liberman MC, Fuchs PA, Elgoyhen AB (2009) A point mutation in the hair cell nicotinic cholinergic receptor prolongs cochlear inhibition and enhances noise protection. PLoS Biol. doi: 101371/journalpbio1000018PubMedCentralPubMedGoogle Scholar
  114. Thompson AM, Schofield BR (2000) Afferent projections of the superior olivary complex. Microsc Res Tech 51:330–354PubMedGoogle Scholar
  115. Vetter DE, Mugnaini E (1992) Distribution and dendritic features of three groups of rat olivocochlear neurons. A study with two retrograde cholera toxin tracers. Anat Embryol 185:1–16PubMedGoogle Scholar
  116. Vetter DE, Saldaña E, Mugnaini E (1993) Input from the inferior colliculus to medial olivocochlear neurons in the rat, a double label study with PHA-L and cholera toxin. Hear Res 70:173–186PubMedGoogle Scholar
  117. Wallace MN, Harper MS (1997) Callosal connections of the ferret primary auditory cortex. Exp Brain Res 116:367–374PubMedGoogle Scholar
  118. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway, neuroanatomy. Springer, Berlin, pp 410–448Google Scholar
  119. Warr WB, Boche JB, Neely ST (1997) Efferent innervation of the inner hair cell region, origins and terminations of two lateral olivocochlear systems. Hear Res 108:89–111PubMedGoogle Scholar
  120. Weedman DL, Ryugo DK (1996a) Projections from auditory cortex to the cochlear nucleus in rats, synapses on granule cell dendrites. J Comp Neurol 371:311–324PubMedGoogle Scholar
  121. Weedman DL, Ryugo DK (1996b) Pyramidal cells in primary auditory cortex project to cochlear nucleus in rat. Brain Res 706:97–102PubMedGoogle Scholar
  122. Weedman DL, Pongstaporn T, Ryugo DK (1996) Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: mossy fiber endings and their targets. J Comp Neurol 369:345–360PubMedGoogle Scholar
  123. White JS, Warr WB (1983) The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219:203–214PubMedGoogle Scholar
  124. Wickesberg RE, Oertel D (1988) Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice. J Comp Neurol 268:389–399PubMedGoogle Scholar
  125. Winer JA (1985) The medial geniculate body of the cat. Adv Anat Embryol Cell Biol 86:1–97PubMedGoogle Scholar
  126. Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway, neuroanatomy. Springer, New York, pp 222–409Google Scholar
  127. Winer JA (2006) Decoding the auditory corticofugal systems. Hear Res 212:1–8PubMedGoogle Scholar
  128. Winer JA, Larue DT (1988) Anatomy of glutamic acid decarboxylase immunoreactive neurons and axons in the rat medial geniculate body. J Comp Neurol 278:47–68PubMedGoogle Scholar
  129. Winer JA, Lee CC (2007) The distributed auditory cortex. Hear Res 229:3–13PubMedCentralPubMedGoogle Scholar
  130. Winer JA, Morest DK (1983) The medial division of the medial geniculate body of the cat: implications for thalamic organization. J Neurosci 3:2629–2651PubMedGoogle Scholar
  131. Winer JA, Schreiner CE (2011) The auditory cortex. Springer, New YorkGoogle Scholar
  132. Winer JA, Kelly JB, Larue DT (1999) Neural architecture of the rat medial geniculate body. Hear Res 31:19–41Google Scholar
  133. Wu SH (1999) Physiological properties of neurons in the ventral nucleus of the lateral lemniscus of the rat, intrinsic membrane properties and synaptic responses. J Neurophysiol 81:2862–2874PubMedGoogle Scholar
  134. Ye Y, Machado DG, Kim DO (2000) Projection of the marginal shell of the anteroventral cochlear nucleus to olivocochlear neurons in the cat. J Comp Neurol 420:127–138PubMedGoogle Scholar
  135. Young ED, Davis KA (2002) Circuitry and function of the dorsal cochlear nucleus, chapter 5. In: Oertel D, Fay RR, Popper AN (eds) Springer handbook of auditory research. Integrative functions in the mammalian auditory pathway, vol 15. Springer, New York, pp 160–206Google Scholar
  136. Young ED, Shofner WP, White JA, Robert JM, Voigt HF (1988) Response properties of cochlear nucleus neurons in relationship to physiological mechanisms. In: Edelman GM, Gall WE, Cowan WM (eds) Auditory function, neurobiological bases of hearing. Wiley, New York, pp 277–312Google Scholar
  137. Yu XJ, Xu XX, He S, He J (2009) Change detection by thalamic reticular neurons. Nat Neurosci 12:1165–1170PubMedGoogle Scholar
  138. Zhang H, Kelly JB (2006a) Responses of neurons in the rat’s ventral nucleus of the lateral lemniscus to monaural and binaural tone bursts. J Neurophysiol 95:2501–2512PubMedGoogle Scholar
  139. Zhang H, Kelly JB (2006b) Responses of neurons in the rat’s ventral nucleus of the lateral lemniscus to amplitude-modulated tones. J Neurophysiol 96:2905–2914PubMedGoogle Scholar
  140. Zhang Y, Wu SH (2000) Long-term potentiation in the inferior colliculus studied in rat brain slice. Hear Res 1(47):92–103Google Scholar
  141. Zhao M, Wu SH (2001) Morphology and physiology of neurons in the ventral nucleus of the lateral lemniscus in rat brain slices. J Comp Neurol 433:255–271PubMedGoogle Scholar
  142. Zhou J, Shore S (2006) Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig. J Comp Neurol 495:100–112PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Cellular Biology and Pathology, Faculty of MedicineUniversity of SalamancaSalamancaSpain
  2. 2.Auditory Neuroscience LaboratoryInstitute for Neuroscience of Castilla y LéonSalamancaSpain