Descending Connections of Auditory Cortex to the Midbrain and Brain Stem

Chapter

Abstract

Descending pathways in the brain have been known, since the end of the nineteenth century (Held 1891) but their significance was unappreciated due to the focus on ascending pathways and the unsuitability of the tract tracing methods then available to reveal these projections. Renewed interest was triggered by the discovery of the olivocochlear bundle (Rasmussen 1946, 1953), and interest surged as the magnitude of the descending pathways emerged (Bourassa et al. 1997; Winer 2006). The auditory cortex (AC) projects to a wide range of subcortical targets in the auditory pathway (Winer 2006; Winer and Lee 2007). By far, the projections to the auditory thalamus and midbrain are the largest and the projections to subcollicular nuclei such as nucleus sagulum, the paraleminscal regions, superior olivary complex (SOC), cochlear nuclear complex (CNC), and pontine nuclei (PN) were not appreciated until recently (Feliciano and Potashner 1995; Weedman and Ryugo 1996; Doucet et al. 2002; Doucet et al. 2003; Meltzer and Ryugo 2006; Perales et al. 2006). The AC also projects to subcortical forebrain structures such as the amygdala (Romanski and LeDoux 1993), the basal ganglia, and premotor structures including the striatum (Beneyto and Prieto 2001), superior colliculus (Paula-Barbosa and Sousa-Pinto 1973), and central gray (Winer et al. 1998), suggesting that the AC has an important role not only in sensory processing of audition, but also in motor behavior, autonomic function, and state dependent changes (Winer 2006).

Abbreviations

AI

primary auditory cortex

AC

auditory cortex

BDA

biotinylated dextran amines

BF

best frequency

CNC

cochlear nuclear complex

CNIC

central of the inferior colliculus

DCN

dorsal cochlear nucleus

DCIC

dorsal cortex of the inferior colliculus

DNLL

dorsal nucleus of the lateral lemniscus

DSCF

Doppler-shifted constant frequency

ECIC

external cortex of the inferior colliculus

ES

electrical stimulation

GABA

g-aminobutyric acid

IC

inferior colliculus

ICH

inner hair cell

LOC

lateral olivocochlear bundle

LSO

lateral superior olive

MGB

medial geniculate body

MOC

medial olivocochlear bundle

NB

nucleus basalis

NLL

nuclei of the lateral lemniscus

OHC

outer hair cell

PHA-L

Phaseolus vulgaris-leucoagglutinin

PN

pontine nuclei

SOC

superior olivary complex

SPO

superior paraolivary nucleus

VCN

ventral cochlear nucleus

VNLL

ventral nucleus of the lateral lemniscus

VNTB

ventral nucleus of the trapezoid body

Notes

Acknowledgments

Supported by grants from the Spanish MEC (BFU2009-07286), EU (EUI2009-04083) and JCYL-UE (GR221) to MSM to Manuel S. Malmierca, and NIH grants DC00232 and DC04395 and a Life Sciences Research Award from the Office for Science and Medicine, NSW, to David K. Ryugo. We are grateful to our colleagues whose work made this review possible.

References

  1. Andersen RA, Snyder RL, and Merzenich MM (1980) The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical fields of the cat. Journal of Comparative Neurology 191:479–494.PubMedCrossRefGoogle Scholar
  2. Bajo VM and Moore DR (2005) Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. Journal of Comparative Neurology 486:101–116.PubMedCrossRefGoogle Scholar
  3. Bajo VM, Nodal FR, Bizley JK, Moore DR, and King AJ (2007) The ferret auditory cortex: descending projections to the inferior colliculus. Cerebral Cortex 17:475–491.PubMedCrossRefGoogle Scholar
  4. Bajo VM, Rouiller EM, Welker E, Clarke S, Villa AEP, de Ribaupierre Y, and de Ribaupierre F (1995) Morphology and spatial distribution of corticothalamic terminals originating from the cat auditory cortex. Hearing Research 83:161–174.PubMedCrossRefGoogle Scholar
  5. Bajo VM, Nodal FR, Moore DR, King AJ (2010) The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nature Neuroscience 13:253–260.Google Scholar
  6. Bakin JS and Weinberger NM (1990) Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Research 536:271–286.PubMedCrossRefGoogle Scholar
  7. Bakin JS, Weinberger NM (1996) Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proceedings of the National Academy of Sciences of the United States of America 93:11219–11224.PubMedCrossRefGoogle Scholar
  8. Bao S, Chang EF, Woods J, and Merzenich MM (2004) Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nature Neuroscience 7:974–981.PubMedCrossRefGoogle Scholar
  9. Bartlett EL and Smith PH (1999) Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. Journal of Neurophysiology 81:1999–2016.PubMedGoogle Scholar
  10. Bartlett EL, Stark JM, Guillery RW, and Smith PH (2000) Comparison of the fine structure of cortical and collicular terminals in the rat medial geniculate body. Neuroscience 100:811–828.PubMedCrossRefGoogle Scholar
  11. Beneyto M and Prieto JJ (2001) Connections of the auditory cortex with the claustrum and the endopiriform nucleus in the cat. Brain Research Bulletin 54:485–498.PubMedCrossRefGoogle Scholar
  12. Beneyto M, Winer JA, Larue DT, and Prieto JJ (1998) Auditory connections and neurochemistry of the sagulum. Journal of Comparative Neurology 401:329–351.PubMedCrossRefGoogle Scholar
  13. Beyerl BD (1978) Afferent projections to the central nucleus of the inferior colliculus in the rat. Brain Research 145:209–223.PubMedCrossRefGoogle Scholar
  14. Bourassa J, Pinault D, and Deschênes M (1997) Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. European Journal of Neuroscience 7:19–30.CrossRefGoogle Scholar
  15. Brodal P (1972) The corticopontine projection in the cat. The projection from the auditory cortex. Archives Italianes de Biologie 110:119–144.Google Scholar
  16. Brownell WE, Bader CR, Bertrand D, and de Ribaupierre Y (1985) Evoked mechanical responses of isolated cochlear outer hair cells. Science 227:194–196.PubMedCrossRefGoogle Scholar
  17. Budinger E, Heil P, and Scheich H (2000) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. European Journal of Neuroscience 12:2452–2474.PubMedCrossRefGoogle Scholar
  18. Caicedo A and Herbert H (1993) Topography of descending projections from the inferior colliculus to auditory brainstem nuclei in the rat. Journal of Comparative Neurology 328:377–392.PubMedCrossRefGoogle Scholar
  19. Casseday JH, Jones DR, and Diamond IT (1979) Projections from cortex to tectum in the tree shrew, Tupaia glis. Journal of Comparative Neurology 185:253–291.PubMedCrossRefGoogle Scholar
  20. Coleman JR and Clerici WJ (1987) Sources of projections to subdivisions of the inferior colliculus in the rat. Journal of Comparative Neurology 262:215–226.PubMedCrossRefGoogle Scholar
  21. Coomes DL and Schofield BR (2004) Projections from the auditory cortex to the superior olivary complex in guinea pigs. European Journal of Neuroscience 19:2188–2200.PubMedCrossRefGoogle Scholar
  22. Coomes DL, Schofield RM, and Schofield BR (2005) Unilateral and bilateral projections from cortical cells to the inferior colliculus in guinea pigs. Brain Research 1042:62–72.PubMedCrossRefGoogle Scholar
  23. Coomes-Peterson D and Schofield BR (2007) Projections from auditory cortex contact ascending pathways that originate in the superior olive and inferior colliculus. Hearing Research 232:67–77.PubMedCrossRefGoogle Scholar
  24. Darrow KN, Maison SF, and Liberman MC (2006) Cochlear efferent feedback balances interaural sensitivity. Nature Neuroscience 9:1474–1476.Google Scholar
  25. Deschênes MM, Veinante P, and Zhang ZW (1998) The organization of corticothalamic projections: reciprocity versus parity. Brain Research Brain Research Review 28:286–308.CrossRefGoogle Scholar
  26. Dewson JH, III (1968) Some relationships to stimulus discrimination in noise. Journal of Neurophysiology 31:122–130.PubMedGoogle Scholar
  27. Dolan DF and Nuttall AL (1988) Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. Journal of the Acoustical Society of America 83:1081–1086.PubMedCrossRefGoogle Scholar
  28. Doucet JR, Molavi DL, and Ryugo DK (2003) The source of corticocollicular and corticobulbar projections in area Te1 of the rat. Experimental Brain Research 153:461–466.CrossRefGoogle Scholar
  29. Doucet JR, Rose L, and Ryugo DK (2002) The cellular origin of corticofugal projections to the superior olivary complex in the rat. Brain Research 925:28–41.PubMedCrossRefGoogle Scholar
  30. Faye-Lund H (1985) The neocortical projection to the inferior colliculus in the albino rat. Anatomy & Embryology (Berlin) 173:53–70.CrossRefGoogle Scholar
  31. Feliciano M and Potashner SJ (1995) Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus. Journal of Neurochemistry 65:1348–1357.PubMedCrossRefGoogle Scholar
  32. Feliciano M, Saldaña E, and Mugnaini E (1995). Direct projections from the rat primary auditory neocortex to nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei. Auditory Neuroscience 1:287–308.Google Scholar
  33. Fitzpatrick KA and Imig TJ (1978) Projections of auditory cortex upon the thalamus and midbrain in the owl monkey. Journal of Comparative Neurology 177:537–556.CrossRefGoogle Scholar
  34. Games KD and Winer JA (1988) Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hearing Research 34:1–25.PubMedCrossRefGoogle Scholar
  35. Gao E and Suga N (1998) Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proceedings of the National Academy of Sciences of the United States of America. 95:12663–12670.PubMedCrossRefGoogle Scholar
  36. Gao E and Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: role of the corticofugal system. Proceedings of the National Academy of Sciences of the United States of America 97:8081–8086.PubMedCrossRefGoogle Scholar
  37. Groff JA and Liberman MC (2003) Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. Journal of Neurophysiology 90:3178–3200.PubMedCrossRefGoogle Scholar
  38. Haas M, Coomes D, Kuwabara N, and Schofield BR (2003) Laminar distribution and projection patterns of corticocollicular cells in guinea pig auditory cortex. Association for Research in Otolaryngology Abstracts 26 :817.Google Scholar
  39. He J (2003a) Corticofugal modulation on both ON and OFF responses in the nonlemniscal auditory thalamus of the guinea pig. Journal of Neurophysiology 89:367–381.PubMedCrossRefGoogle Scholar
  40. He J (2003b) Corticofugal modulation of the auditory thalamus. Experimental Brain Research 153:579–590.CrossRefGoogle Scholar
  41. He J, Yu YQ, Xiong Y, Hashikawa T, and Chan YS (2002) Modulatory effect of cortical activation on the lemniscal auditory thalamus of the Guinea pig. Journal of Neurophysiology 88:1040–1050.PubMedCrossRefGoogle Scholar
  42. Held H (1891) Die centralen Bahnen des Nervus acusticus bei der Katze. Archiv für Anatomie und Physiologie. Anatomische Abteilung 15:271–290.Google Scholar
  43. Hefti BJ and Smith PH (2000) Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABAA blockade. Journal of Neurophysiology 83:2626–2638.PubMedGoogle Scholar
  44. Herbert H, Aschoff A, and Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. Journal of Comparative Neurology 304:103–122.PubMedCrossRefGoogle Scholar
  45. Huffman RF and Henson OW J. (1990). The descending auditory pathway and acousticomotor systems, connections with the inferior colliculus. Brain Research Brain Research Reviews 15:295–323.PubMedCrossRefGoogle Scholar
  46. Irvine DRF, Rajan R, and Brown M (2001) Injury- and use-related plasticity in adult auditory cortex. Audiology & Neurootology 6:192–195.CrossRefGoogle Scholar
  47. Irvine DRF, Rajan R, and Smith S (2003) Effects of restricted cochlear lesions in adult cats on the frequency organization of the inferior colliculus. Journal of Comparative Neurology 467:354–374.PubMedCrossRefGoogle Scholar
  48. Irvine DRF and Wright BA (2005) Plasticity of spectral processing. International Review of Neurobiology 70:435–472.PubMedCrossRefGoogle Scholar
  49. Jacomme AV, Nodal FR, Bajo VM Manunta Y, Edeline J-M, Babalian A, and Rouiller EM (2003) The projection from auditory cortex to cochlear nucleus in guinea pigs: an in vivo anatomical and in vitro electrophysiological study. Experimental Brain Research 153:467–476.CrossRefGoogle Scholar
  50. Jones EG (2002) Thalamic organization and function after Cajal. Progress in Brain Research 136:333–357.PubMedCrossRefGoogle Scholar
  51. Kamke MR, Brown M, and Irvine DRF (2005) Basal forebrain cholinergic input is not essential for lesion-induced plasticity in mature auditory cortex. Neuron 48:675–686.PubMedCrossRefGoogle Scholar
  52. Kamke MR, Brown M, and Irvine DRF (2003) Plasticity in the tonotopic organization of the medial geniculate body in adult cats following restricted unilateral cochlear lesions. Journal of Comparative Neurology 459:355–367.PubMedCrossRefGoogle Scholar
  53. Kawamura K and Chiba M (1979) Cortical neurons projecting to the pontine nuclei in the cat. An experimental study with the horseradish peroxidase technique. Experimental Brain Research 35:269–285.Google Scholar
  54. Kilgard MP and Merzenich MM (1998) Plasticity of temporal information processing in the primary auditory cortex. Nature Neuroscience 1:727–731.PubMedCrossRefGoogle Scholar
  55. Kuypers HGJM and Lawrence DG (1967) Cortical projections to the red nucleus and the brain stem in the Rhesus monkey. Brain Research 4:151–188.PubMedCrossRefGoogle Scholar
  56. Llano DA and Sherman SM (2008) Evidence for nonreciprocal organization of the mouse auditory thalamocortical-corticothalamic projection systems. Journal of Comparative Neurology 507:1209–1227.PubMedCrossRefGoogle Scholar
  57. Ma X and Suga N (2001) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proceedings of the National Academy of Sciences of the United States of America 98:14060–14065PubMedCrossRefGoogle Scholar
  58. Ma X and Suga N (2003) Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. Journal of Neurophysiology 89:90–103.PubMedCrossRefGoogle Scholar
  59. Ma X and Suga N (2004) Lateral inhibition for center-surround reorganization of the frequency map of bat auditory cortex. Journal of Neurophysiology 92:3192–3199.PubMedCrossRefGoogle Scholar
  60. Ma X and Suga N (2007) Multiparametric corticofugal modulation of collicular duration-tuned neurons: modulation in the amplitude domain. Journal of Neurophysiology 97:3722–3730.PubMedCrossRefGoogle Scholar
  61. Malmierca E and Núñez A (1998) Corticofugal action on somatosensory response properties of rat nucleus gracilis cells. Brain Research 810:172–180.PubMedCrossRefGoogle Scholar
  62. Malmierca MS (2003) The structure and physiology of the rat auditory system: an overview. International Review of Neurobiology 56:147–211.PubMedCrossRefGoogle Scholar
  63. Malmierca MS and Merchán M (2004) The auditory system. In: Paxinos G (ed) The Rat Nervous System. Academic Press, San Diego, pp. 997–1082.Google Scholar
  64. Malmierca MS, Le Beau FEN, and Rees A (1996) The topographical organization of descending projections from the central nucleus of the inferior colliculus in guinea pig. Hearing Research 93:167–180.PubMedCrossRefGoogle Scholar
  65. 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). Acoustic Signal Processing in the Central Auditory System. Plenum Press, New York, pp. 295–302.Google Scholar
  66. Massopust LC Jr and Ordy JM (1962) Auditory organization of the inferior colliculi in the cat. Experimental Neurology 6:465–477.PubMedCrossRefGoogle Scholar
  67. Meltzer NE and Ryugo DK (2006) Projections from auditory cortex to cochlear nucleus: a comparative analysis of rat and mouse. Anatomical Record Advances in Integrative Anatomy and Evolutionary Biology 288:397–408.CrossRefGoogle Scholar
  68. Mettler FA (1935) Corticofugal fiber connections of the cortex of Macaca mulatta. The temporal region. Journal of Comparative Neurology 63:25–47.CrossRefGoogle Scholar
  69. Mitani A, Shimokouchi M, and Nomura S (1983) Effects of stimulation of the primary auditory cortex upon colliculogeniculate neurons in the inferior colliculus of the cat. Neuroscience Letters 42:185–189.PubMedCrossRefGoogle Scholar
  70. Monconduit L, López-Ávila A, Molat JL, Chalus M, and Villanueva L (2006) Corticofugal output from the primary somatosensory cortex selectively modulates innocuous and noxious inputs in the rat spinothalamic system. Journal of Neuroscience 26:8441–8450.PubMedCrossRefGoogle Scholar
  71. Montero VM (1983). Ultrastructural identification of axon terminals from the thalamic reticular nucleus in the medial geniculate body of the rat: an EM autoradiographic study. Experimental Brain Research 51:338–342.CrossRefGoogle Scholar
  72. Morest DK and Oliver DL (1984) The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. Journal of Comparative Neurology 222:209–236.PubMedCrossRefGoogle Scholar
  73. Moriizumi T and Hattori T (1991) Pyramidal cells in rat temporoauditory cortex project to both striatum and inferior colliculus. Brain Research Bulletin 27:141–144.PubMedCrossRefGoogle Scholar
  74. Mulders WHAM and Robertson D (2000) Evidence for direct cortical innervation of medial olivocochlear neurones in rats. Hearing Research 144:65–72.PubMedCrossRefGoogle Scholar
  75. Mulders WHAM and Robertson D (2006) Gentamicin abolishes all cochlear effects of electrical stimulation of the inferior colliculus. Experimental Brain Research 174:35–44.CrossRefGoogle Scholar
  76. Nakamoto KT, Jones SJ, and Palmer AR (2008) Descending projections from auditory cortex modulate sensitivity in the midbrain to cues for spatial position. Journal of Neurophysiology 99:2347–2356.PubMedCrossRefGoogle Scholar
  77. Ohlrogge M, Doucet JR, and Ryugo DK (2001) Projections of the pontine nuclei to the cochlear nucleus in rats. Journal of Comparative Neurology 436:290–303.PubMedCrossRefGoogle Scholar
  78. Ojima H, Honda CN, and Jones EG (1992) Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cerebral Cortex 2:197–216.PubMedCrossRefGoogle Scholar
  79. Oliver DL, Ostapoff E-M, and Beckius GE (1999) Direct innervation of identified tectothalamic neurons in the inferior colliculus by axons from the cochlear nucleus. Neuroscience 93:643–658.PubMedCrossRefGoogle Scholar
  80. Paula-Barbosa MM and Sousa-Pinto A (1973) Auditory cortical projections to the superior colliculus in the cat. Brain Research 50:47–61.PubMedCrossRefGoogle Scholar
  81. 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
  82. Perrot X, Ryvlin P, Isnard J, Guénot M, Catenoix H, Fischer C, Mauguière F, and Collet L (2006) Evidence for corticofugal modulation of peripheral auditory activity in humans. Cerebral Cortex 16:941–948.PubMedCrossRefGoogle Scholar
  83. 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
  84. Pickles, JO (1988) An Introduction to the Physiology of Hearing. Academic Press, Orlando.Google Scholar
  85. Popelár J, Erre JP, Syka J, and Aran JM (2001) Effects of contralateral acoustical stimulation on three measures of cochlear function in the guinea pig. Hearing Research 152:128–138.PubMedCrossRefGoogle Scholar
  86. Polley DB, Heiser MA, Blake DT, Schreiner CE, Merzenich MM (2004) Associative learning shapes the neural code for stimulus magnitude in primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America 101:16351–16356.PubMedCrossRefGoogle Scholar
  87. Potashner SJ, Dymczyk L, and Deangelis MM (1988) D-aspartate uptake and release in the guinea pig spinal cord after partial ablation of the cerebral cortex. Journal of Neurochemistry 50:103–111.PubMedCrossRefGoogle Scholar
  88. Rajan R (1990) Electrical stimulation of the inferior colliculus at low rates protects the cochlea from auditory desensitization. Brain Research 506:192–204.PubMedCrossRefGoogle Scholar
  89. Rajan R and Irvine DRF (1998a) Absence of plasticity of the frequency map in dorsal cochlear nucleus of adult cats after unilateral partial cochlear lesions. Journal of Comparative Neurology 399:35–46.PubMedCrossRefGoogle Scholar
  90. Rajan R and Irvine DRF (1998b) Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiology & Neurootology 3:123–144.CrossRefGoogle Scholar
  91. Rasmussen GL (1946) The olivary peduncle and other fiber projections of the superior olivary complex. Journal of Comparative Neurology 99:61–74.CrossRefGoogle Scholar
  92. Rasmussen GL (1953) Further observations of the efferent cochlear bundle. Journal of Comparative Neurology 99:61–74.PubMedCrossRefGoogle Scholar
  93. Recanzone GH, Schreiner CE, and Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. Journal of Neuroscience 13:87–103.PubMedGoogle Scholar
  94. Romanski LM, Clugnet MC, Bordi F, and LeDoux JE (1993) Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behavioral Neuroscience 107:444–450.PubMedCrossRefGoogle Scholar
  95. Romanski LM and LeDoux JE (1993) Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cerebral Cortex 3:515–532.PubMedCrossRefGoogle Scholar
  96. Rouiller EM and Welker E (1991) Morphology of corticothalamic terminals arising from the auditory cortex of the rat: a Phaseolus vulgaris-leucoagglutinin (PHA-L) tracing study. Hearing Research 56:179–190.PubMedCrossRefGoogle Scholar
  97. Ryugo DK and Weinberger NM (1976) Corticofugal modulation of the medial geniculate body. Experimental Neurology 51:377–391.PubMedCrossRefGoogle Scholar
  98. Sakai M and Suga N (2001) Plasticity of the cochleotopic (frequency) map in specialized and nonspecialized auditory cortices. Proceedings of the National Academy of Sciences of the United States of America 98:3507–3512.PubMedCrossRefGoogle Scholar
  99. Sakai M and Suga N (2002) Centripetal and centrifugal reorganizations of frequency map of auditory cortex in gerbils. Proceedings of the National Academy of Sciences of the United States of America 99:7108–7112.PubMedCrossRefGoogle Scholar
  100. Saldaña E, Feliciano M, and Mugnaini E (1996) Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. Journal of Comparative Neurology 371:15–40.PubMedCrossRefGoogle Scholar
  101. Schofield BR (2002) Ascending and descending projections from the superior olivary complex in guinea pigs: different cells project to the cochlear nucleus and the inferior colliculus. Journal of Comparative Neurology 453:217–225.PubMedCrossRefGoogle Scholar
  102. Schofield BR and Coomes DL (2005) Auditory cortical projections to the cochlear nucleus in guinea pigs. Hearing Research 199:89–102.PubMedCrossRefGoogle Scholar
  103. Schofield BR and Coomes DL (2006) Pathways from auditory cortex to the cochlear nucleus in guinea pigs. Hearing Research 216–217:81–89.PubMedCrossRefGoogle Scholar
  104. Schofield BR, Coomes DL, and Schofield RM (2006) Cells in auditory cortex that project to the cochlear nucleus in guinea pigs. Journal of the Association for Research in Otolaryngology 7:95–109.PubMedCrossRefGoogle Scholar
  105. Schuller G, Covey E, and Casseday JH (1991) Auditory pontine grey: connections and response properties in the horseshoe bat. European Journal of Neuroscience 3:648–662.PubMedCrossRefGoogle Scholar
  106. Seluakumaran K, Mulders WH, and Robertson D (2008) Effects of medial olivocochlear efferent stimulation on the activity of neurons in the auditory midbrain. Experimental Brain Research 186:161–174.CrossRefGoogle Scholar
  107. Shi CJ and Cassell MD (1997) Cortical, thalamic, and amygdaloid projections of rat temporal cortex. Journal of Comparative Neurology 382:153–175.PubMedCrossRefGoogle Scholar
  108. Spangler KM and Warr WB (1991). The descending auditory system. In: Altschuler R, Hoffman DW, Bobbin RP and Clopton BM (eds) The Neurobiology of Hearing. Volume. II, Raven Press, New York. pp. 27–45.Google Scholar
  109. Suga N (2008) Role of corticofugal feedback in hearing. Journal of Comparative Physiology A 194:169–183.CrossRefGoogle Scholar
  110. Suga N, Gao E, Zhang Y, Ma X, and Olsen JF (2000) The corticofugal system for hearing: recent progress. Proceedings of the National Academy of Sciences of the United States of America 97:11807–11814.PubMedCrossRefGoogle Scholar
  111. Suga N and Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nature Reviews Neuroscience 4:783–794.PubMedCrossRefGoogle Scholar
  112. Suga N, Xiao Z, Ma X, and Ji W (2002) Plasticity and corticofugal modulation for hearing in adult animals. Neuron 36:9–18.PubMedCrossRefGoogle Scholar
  113. Thompson AM (2005) Descending connections of the auditory midbrain. In: Winer JA and Schreiner CE (eds), The Inferior Colliculus. Springer, New York. pp. 182–199.CrossRefGoogle Scholar
  114. Thompson WH (1900) Degenerations resulting from lesions of the cortex of the temporal lobe. Journal of Anatomy and Physiology 35:147–165.Google Scholar
  115. Towe AL and Jabbur SJ (1961) Cortical inhibition of neurons in dorsal column nuclei of cat. Journal of Neurophysiology 24:488–498.PubMedGoogle Scholar
  116. Veinante P, Jacquin MF, and Deschênes M (2000) Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat. Journal of Comparative Neurology 420:233–243.PubMedCrossRefGoogle Scholar
  117. Vetter DE, Saldaña E, and 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. Hearing Research 70:173–186.PubMedCrossRefGoogle Scholar
  118. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, and Fay RR (eds). The Mammalian Auditory Pathway, Neuroanatomy. Volume 2, Springer Handbook of Auditory Research. Springer, Berlin, pp. 410–448.Google Scholar
  119. Warr WB, Guinan JJ Jr, and White JS (1986) Organization of the efferent fibers: the lateral and medial olivocochlear systems. In: Altschuler RA, Hoffman DW, and Bobbin RP (eds). Neurobiology of Hearing, The Cochlea. Raven Press, New York, pp. 333–348.Google Scholar
  120. Watanabe T, Yanagisawa K, Kanzaki J, and Katsuki Y (1966) Cortical efferent flow influencing unit responses of medial geniculate body to sound stimulation. Experimental Brain Research 2:302–317.CrossRefGoogle Scholar
  121. 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
  122. Weinberger NM (1998) Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiology of Learning and Memory 70:226–251.PubMedCrossRefGoogle Scholar
  123. White JS and Warr WB (1983) The dual origins of the olivocochlear bundle in the albino rat. Journal of Comparative Neurology 219:203–214.PubMedCrossRefGoogle Scholar
  124. 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
  125. Winer JA (2006) Decoding the auditory corticofugal systems. Hearing Research 212:1–8.PubMedCrossRefGoogle Scholar
  126. 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
  127. 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
  128. Winer JA and Lee CC (2007) The distributed auditory cortex. Hearing Research 229:3–13.PubMedCrossRefGoogle Scholar
  129. 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
  130. Wong D and Kelly JP (1981) Differentially projecting cells in individual layers of the auditory cortex: a double-labeling study. Brain Research 230:362–366.PubMedCrossRefGoogle Scholar
  131. Wu Y and Yan J (2007) Modulation of the receptive fields of midbrain neurons elicited by thalamic electrical stimulation through corticofugal feedback. Journal of Neuroscience 27:10651–10658.PubMedCrossRefGoogle Scholar
  132. Xiao Z and Suga N (2002) Modulation of cochlear hair cells by the auditory cortex in the mustached bat. Nature Neuroscience 5:57–63.PubMedCrossRefGoogle Scholar
  133. Xiao Z and Suga N (2005) Asymmetry in corticofugal modulation of frequency-tuning in mustached bat auditory system. Proceedings of the National Academy of Sciences of the United States of America 102:19162–19167.PubMedCrossRefGoogle Scholar
  134. Yan J and Ehret G (2001) Corticofugal reorganization of the midbrain tonotopic map in mice. Neuroreport 12:3313–3316.PubMedCrossRefGoogle Scholar
  135. Yan J and Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. European Journal of Neuroscience 16:119–128.PubMedCrossRefGoogle Scholar
  136. Yan J and Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273:1100–1103.PubMedCrossRefGoogle Scholar
  137. Yan J and Zhang Y (2005) Sound-guided shaping of the receptive field in the mouse auditory cortex by basal forebrain activation. European Journal of Neuroscience 21:563–576.PubMedCrossRefGoogle Scholar
  138. Yan J, Zhang Y, and Ehret G (2005) Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. Journal of Neurophysiology 93:71–83.PubMedCrossRefGoogle Scholar
  139. Yan W and Suga N (1998) Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nature Neuroscience 1:54–58.PubMedCrossRefGoogle Scholar
  140. Yu YQ, Xiong Y, Chan YS, and He J (2004) Corticofugal gating of auditory information in the thalamus: an in vivo intracellular recording study. Journal of Neuroscience 24:3060–3069.PubMedCrossRefGoogle Scholar
  141. Yu XJ, Xu XX, He S, and He J (2009) Change detection by thalamic reticular neurons. Nature Neuroscience 12:1165–1170.Google Scholar
  142. Zhang Y and Suga N (1997) Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. Journal of Neurophysiology 78:3489–3492.PubMedGoogle Scholar
  143. Zhang Y and Suga N (2000) Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. Journal of Neurophysiology 84:325–333.PubMedGoogle Scholar
  144. 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
  145. Zhang Y, Suga N, and Yan J (1997) Corticofugal modulation of frequency processing in bat auditory system. Nature 387:900–903.PubMedCrossRefGoogle Scholar
  146. Zheng J, Shen W, He DZ, Long KB, Madison LD, and Dallos P (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149–155.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Auditory Neurophysiology Unit, Laboratory for the Neurobiology of Hearing, Faculty of MedicineInstitute for Neuroscience of Castilla y León, and Dept Cell Biology and Pathology, Med School, University of SalamancaSalamancaSpain
  2. 2.Program for NeuroscienceGarvan Institute of Medical ResearchDarlinghurstAustralia

Personalised recommendations