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CANADIAN ASSOCIATION OF NEUROSCIENCE REVIEW: Development and Plasticity of the Auditory Cortex

Published online by Cambridge University Press:  02 December 2014

Jun Yan
Jun Yan*
Affiliation:
Department of Physiology and Biophysics, Neuroscience Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada
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Abstract:

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The functions of the cerebral cortex are predominantly established during the critical period of development. One obvious developmental feature is its division into different functional areas that systematically represent different environmental information. This is the result of interactions between intrinsic (genetic) factors and extrinsic (environmental) factors. Following this critical period, the cerebral cortex attains its adult form but it will continue to adapt to environmental changes. Thus, the cerebral cortex is constantly adapting to the environment (plasticity) from its embryonic stages to the last minute of life. This review details important factors that contribute to the development and plasticity of the auditory cortex. The instructive role of thalamocortical innervation, the regulatory role of cholinergic projection of the basal forebrain and the potential role of the corticofugal modulation are presented.

Résumé:

RÉSUMÉ:

Les fonctions du cortex cérébral sont établies en grande partie pendant une période critique du développement. Sa division en différentes zones fonctionnelles, qui représentent systématiquement différentes informations environnementales, résulte d’interactions entre des facteurs intrinsèques (génétiques) et des facteurs extrinsèques (environnementaux). Après cette période critique, le cortex cérébral atteint sa forme adulte. Il va cependant continuer à s’adapter aux changements environnementaux. Ainsi, le cortex cérébral est en adaptation constante à l’environnement (la plasticité), de la phase embryonnaire jusqu’aux derniers instants de la vie. Cette revue décrit en détail les facteurs importants qui contribuent au développement et à la plasticité du cortex auditif. Le rôle informatif de l’innervation thalamocorticale, le rôle régulateur des projections cholinergiques du cerveau antérieur et le rôle potentiel de la modulation corticofuge sont présentés.

Type
Research Article
Information
Canadian Journal of Neurological Sciences , Volume 30 , Issue 3 , August 2003 , pp. 189 - 200
Copyright
Copyright © The Canadian Journal of Neurological 2003

References

1. Dreher, B, Burke, W, Calford, MB. Cortical plasticity revealed by circumscribed retinal lesions or artificial scotomas. Prog Brain Res 2001;134:217–246.Google Scholar
2. Eggermont, JJ. Representation of spectral and temporal sound features in three cortical fields of the cat. Similarities outweigh differences. J Neurophysiol 1998;80:2743–2764.CrossRefGoogle ScholarPubMed
3. Stiebler, I, Neulist, R, Fichtel, I, Ehret, G. The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J Comp Physiol [A] 1997;181(6):559–571.Google Scholar
4. Fox, K, Glazewski, S, Schulze, S. Plasticity and stability of somatosensory maps in thalamus and cortex. Curr Opin Neurobiol 2000;10(4):494–497.Google Scholar
5. Phillips, DP, Judge, PW, Kelly, JB. Primary auditory cortex in the ferret (Mustela putorius): neural response properties and topographic organization. Brain Res 1988;443(1–2):281–294.Google Scholar
6. Suga, N. Multi-function theory for cortical processing of auditory information: implications of single-unit and lesion data for future research. J Comp Physiol [A] 1994;175:135–144.CrossRefGoogle ScholarPubMed
7. Irvine, DR, Rajan, R. Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning. Clin Exp Pharmacol Physiol 1996;23(10–11):939–947.Google Scholar
8. Scheich, H, Stark, H, Zuschratter, W, Ohl, FW, Simonis, CE. Some functions of primary auditory cortex in learning and memory formation. Adv Neurol 1997;73:179–193.Google Scholar
9. Weinberger, NM. Physiological Memory in Primary Auditory Cortex: Characteristics and Mechanisms. Neurobiol Learn Mem 1998;70:226–251.CrossRefGoogle ScholarPubMed
10. Edeline, JM. Learning-induced physiological plasticity in the thalamo-cortical sensory systems: a critical evaluation of receptive field plasticity, map changes and their potential mechanisms. Prog Neurobiol 1999;57(2):165–224.CrossRefGoogle ScholarPubMed
11. Kilgard, MP, Pandya, PK, Engineer, ND, Moucha, R. Cortical network reorganization guided by sensory input features. Biol Cybern 2002;87(5–6):333–343.CrossRefGoogle ScholarPubMed
12. Rauschecker, JP. Cortical map plasticity in animals and humans. Prog Brain Res 2002;138:73–88.Google Scholar
13. Suga, N, Xiao, Z, Ma, X, Ji, W. Plasticity and corticofugal modulation for hearing in adult animals. Neuron 2002;36(1):9–18.Google Scholar
14. Rubenstein, JL. Intrinsic and extrinsic control of cortical development. Novartis Found Symp 2000;228:67–75.Google Scholar
15. Rubenstein, JL, Rakic, P. Genetic control of cortical development. Cereb Cortex 1999;9:521–523.Google Scholar
16. Chapman, B, Godecke, I, Bonhoeffer, T. Development of orientation preference in the mammalian visual cortex. J Neurobiol 1999;41:18–24.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
17. Bakin, JS, Weinberger, NM. Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res 1990;536:271–286.CrossRefGoogle ScholarPubMed
18. Hohmann, CF, Berger-Sweeney, J. Cholinergic regulation of cortical development and plasticity: New twist to an old story. Perspect Dev Neurobiol 1998; 5:401–425.Google Scholar
19. Suga, N, Yan, J, Zhang, Y. Cortical maps for hearing and egocentric selection for self-organization. Trends Cognit Sci 1997;1:1–14.CrossRefGoogle ScholarPubMed
20. Berard, N, Pizzorusso, T, Maffei, L. Critical period during sensory development. Curr Opin Neurobiol 2000;10:138–145.Google Scholar
21. Eggermont, JJ. Differential maturation rates for response parameters in cat primary auditory cortex. Auditory Neurosci 1996;2:30–327.Google Scholar
22. Harwerth, RS, Smith, EL 3rd, Duncan, GC, Crawford, ML, von Noorden, GK. Multiple sensitive periods in the development of the primate visual system. Science 1986;232:235–238.CrossRefGoogle ScholarPubMed
23. Molnar, Z, Lopez-Bendito, G, Small, J, Partridge, LD, Blakemore, C, Wilson, MC. Normal development of embryonic thalamocortical connectivity in the absence of evoked synaptic activity. J Neurosci 2002;22(23):10313–10323.CrossRefGoogle ScholarPubMed
24. Crandall, JE, Caviness, VS Jr. Thalamocortical connections in newborn mice. J Comp Neurol 1984;228:542–556.Google Scholar
25. Erzurumlu, RS, Jhaveri, S. Emergence of connectivity in the embryonic rat parietal cortex. Cereb Cortex 1992;2(4):336–352.CrossRefGoogle ScholarPubMed
26. Miyashita-Lin, EM, Hevner, R, Wassarman, KM, Martinez, S, Rubenstein, JL. Early neocortical regionalization in the absence of thalamic innervation. Science 1999;285:906–909.Google Scholar
27. Nakagawa, Y, Johnson, JE, O’Leary, DD. Graded and areal expression patterns of regulatory genes and cadherins in embryonic neocortex independent of thalamocortical input. J Neurosci 1999;19:10877–10885.Google Scholar
28. O’Leary, DD, Nakagawa, Y. Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 2002;12:14–25.CrossRefGoogle ScholarPubMed
29. Yuste, R, Sur, M. Development and plasticity of the cerebral cortex:from molecules and maps. J Neurobiol 1999;41:1–6.Google Scholar
30. Harrison, RV, Nagasawa, A, Smith, DW, Stanton, S, Mount, RJ. Reorganization of auditory cortex after neonatal high frequency cochlear hearing loss. Hear Res 1991;54(1):11–19.CrossRefGoogle ScholarPubMed
31. Harrison, RV, Stanton, SG, Ibrahim, D, Nagasawa, A, Mount, RJ. Neonatal cochlear hearing loss results in developmental abnormalities of the central auditory pathways. Acta Otolaryngol 1993;113(3):296–302.CrossRefGoogle ScholarPubMed
32. Stanton, SG, Harrison, RV. Neonatal auditory augmentation modifies cochleotopic mapping in primary auditory cortex of the cat. Auditory Neurosci 1996;2:97–107.Google Scholar
33. Zhang, LI, Bao, S, Merzenich, MM. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 2001;4(11):1123–1130.Google Scholar
34. Zhang, LI, Bao, S, Merzenich, MM. Disruption of primary auditory cortex by synchronous auditory inputs during a critical period. Proc Natl Acad Sci USA 2002;99(4):2309–2314.Google Scholar
35. Wiesel, TN, Hubel, DH. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 1963;26:1003–1017.Google Scholar
36. Stanton, SG, Harrison, RV. Projections from the medial geniculate body to primary auditory cortex in neonatally deafened cats. J Comp Neurol 2000;426(1):117–129.Google Scholar
37. Harrison, RV, Ibrahim, D, Mount, RJ. Plasticity of tonotopic maps in auditory midbrain following partial cochlear damage in the developing chinchilla. Exp Brain Res 1998;123(4):449–460.Google Scholar
38. Poon, PW, Chen, X, Postnatal exposure to tones alters the tuning characteristics of inferior collicular neurons in the rat. Brain Res 1992;586:391–394.Google Scholar
39. Gao, W, Pallas, SL. Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J Neurosci 1999;19(18):7940–7950.Google Scholar
40. Sharma, J, Angelucci, A, Sur, M. Induction of visual orientation modules in auditory cortex. Nature 2000;404(6780):841–847.Google Scholar
41. Robertson, RT, Gallardo, KA, Claytor, KJ, et al. Neonatal treatment with 192 IgG-saporin produces long-term forebrain cholinergic deficits and reduces dendritic branching and spine density of neocortical pyramidal neurons. Cereb Cortex 1998;58(2):142–155.Google Scholar
42. Zhu, XO, de Permentier, PJ, Waite, PM. Cholinergic depletion by IgG192-saporin retards development of rat barrel cortex. Brain Res Dev Brain Res 2002;136(1):1–16.Google Scholar
43. Mesulam, MM, Mufson, EJ, Levey, AI, Wainer, BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 1983;214(2):170–197.Google Scholar
44. Mesulam, MM, Mufson, EJ, Wainer, BH, Levey, AI. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983;10:1186–1201.Google Scholar
45. Houser, CR, Crawford, GD, Salvaterra, PM, Voughn, JE. Immunocytochemical localization of cholineacetyltransferase in rat cerebral cortex: a study of cholinergic neurons and synapses. J Comp Neurol 1985;243:17–34.Google Scholar
46. Kitt, CA, Hohmann, CF, Coyle, JT, Price, DL. Cholinergic innervation of mouse forebrain structures. J Comp Neurol 1994;341:117–129.Google Scholar
47. Mechawar, N, Descarries, L. The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study. Neurosci 2001;108(4):555–567.Google Scholar
48. Hohmann, CF, Ebner, FF. Development of cholinergic markers in mouse forebrain. I. Choline acetyltransferase enzyme activity and acetylcholinesterase histochemistry. Brain Res 1985;355(2):225–241.Google Scholar
49. Kristt, DA. Development of neocortical circuitry: histochemical localization of acetylcholinesterase in relation to the cell layers of rat somatosensory cortex. J Comp Neurol 1979;186(1):1–15.Google Scholar
50. Thal, LJ, Gilbertson, E, Armstrong, DM, Gage, FH. Development of the basal forebrain cholinergic system: phenotype expression prior to target innervation. Neurobiol Aging 1992;13(1):67–72.Google Scholar
51. Virgili, M, Contestabile, A, Barnabei, O. Postnatal maturation of cholinergic markers in forebrain regions of C57BL/6 mice. Brain Res Dev Brain Res 1991;63(1–2):281–285.Google Scholar
52. Zahalka, EA, Seidler, FJ, Lappi, SE, Yanai, J, Slotkin, TA. Differential development of cholinergic nerve terminal markers in rat brain regions: implications for nerve terminal density, impulse activity and specific gene expression. Brain Res 1993;601(1–2):221–229.CrossRefGoogle ScholarPubMed
53. Hohmann, CF, Brooks, AR, Coyle, JT. Neonatal lesions of the basal forebrain cholinergic neurons result in abnormal cortical development. Brain Res 1988;470(2):253–264.Google Scholar
54. Hohmann, CF, Kwiterovich, KK, Oster-Granite, ML, Coyle, JT. Newborn basal forebrain lesions disrupt cortical cytodifferentiation as visualized by rapid Golgi staining. Cereb Cortex 1991;1(2):143–157.Google Scholar
55. Torres, EM, Perry, TA, Blockland, A, et al. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neurosci 1994;63(1):95–122.Google Scholar
56. Robertson, RT, Mostamand, F, Kageyama, GH, Gallardo, KA, Yu, J. Primary auditory cortex in the rat: transient expression of acetylcholinesterase activity in developing geniculocortical projections. Brain Res Dev Brain Res 1991;58(1):81–95.CrossRefGoogle ScholarPubMed
57. Eggermont, JJ, Komiya, H. Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood. Hear Res 2000;142(1–2):89–101.Google Scholar
58. Robertson, D, Irvine, DR. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J Comp Neurol 1989;282(3):456–471.Google Scholar
59. Rajan, R, Irvine, DR, Wise, LZ, Heil, P. Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochlea in primary auditory cortex. J Comp Neurol 1993;338(1):17–49.Google Scholar
60. Pantev, C, Oostenveld, R, Engelien, A, et al. Increased auditory cortical representation in musicians. Nature 1998;392:811–814.Google Scholar
61. Monaghan, P, Metcalfe, NB, Ruxton, GD. Does practice shape the brain? Nature 1998;394(6692):434.Google Scholar
62. Recanzone, GH, Schreiner, CE, Merzenich, MM. Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 1993;13(1):87–103.Google Scholar
63. Gao, E, Suga, N. Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci USA 1998;95:12663–12670.Google Scholar
64. Bakin, JS, Lepan, B, Weinberger, NM. Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality. Brain Res 1992;577:226–235.Google Scholar
65. Edeline, J-M, Weinberger, NM. Receptive field plasticity in the auditory cortex during frequency discrimination training: selective returning independent of task difficulty. Behav Neurosci 1993;107:82–103.CrossRefGoogle Scholar
66. Edeline, J-M, Pham, P, Weinberger, NM. Rapid development of learning-induced receptive field plasticity in the auditory cortex. Behav Neurosci 1993;107:539–557.Google Scholar
67. Weinberger, NM, Javid, R, Lepan, B. Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc Natl Acad Sci USA 1993;90:2394–2398.Google Scholar
68. Edeline, J-M, Dutrieux, G, Neuenschwander, EI, Massioui, N. Multiunit changes in hippocampus and medial geniculate body in free-behaving rats during acquisition and retention of a conditioned response to a tone. Behav Neural Biol 1988;50:61–79.Google Scholar
69. Edeline, J-M, Weinberger, NM. Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behav Neurosci 1992;106:81–105.Google Scholar
70. Feldman, DE, Knudsen, EI. Pharmacological specialization of learned auditory responses in the inferior colliculus of the barn owl. J Neurosci 1998;18(8):3073–3087.Google Scholar
71. McKernan, MG, Shinnick-Gallagher, P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 1997;390:607–611.Google Scholar
72. Rogan, MT, Staubli, UV, LeDoux, JE. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997;390:604–607.Google Scholar
73. Armstrong, DD. Rett syndrome neuropathology review 2000. Brain Dev 2001;23(Suppl 1):S72–S76.Google Scholar
74. Frolich, L. The cholinergic pathology in Alzheimer’s disease--discrepancies between clinical experience and pathophysiologi-cal findings. J Neural Transm 2002;109(7–8):1003–1013.Google Scholar
75. Gallagher, M, Colombo, PJ. Aging: the cholinergic hypothesis of cognitive decline. Curr Opin Neurobiol 1995;5:161–168.CrossRefGoogle ScholarPubMed
76. Pirch, JH, Turco, K, Rucker, HK. A role for acetylcholine in conditioning-related responses of rat frontal cortex neurons: microiontophoretic evidence. Brain Res 1992;586(1):19–26.CrossRefGoogle ScholarPubMed
77. Metherate, R, Ashe, JH, Weinberger, NM. Acetylcholine modifies neuronal acoustic rate-level functions in guinea pig auditory cortex by an action at muscarinic receptors. Synapse 1990;6:364–368.Google Scholar
78. Metherate, R, Ashe, JH. Nucleus basalis stimulation facilitates thalamocortical synaptic transmission in the rat auditory cortex. Synapse 1993;14:132–143.Google Scholar
79. Edeline, J-M, Hars, B, Maho, C, Hennevin, E. Transient and prolonged facilitation of tone-evoked responses induced by basal forebrain stimulations in the rat auditory cortex. Exp Brain Res 1994;97:373–386.CrossRefGoogle ScholarPubMed
80. Hars, B, Maho, C, Edeline, J-M, Hennevin, E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neurosci 1993;56(1):61–74.Google Scholar
81. Ashe, JH, McKenna, TM, Weinberger, NM. Cholinergic modulation of frequency receptive fields in auditory cortex: II. Frequency-specific effects of anticholinesterases provide evidence for a modulatory action of endogenous ACh. Synapse 1989;4:44–54.Google Scholar
82. McKenna, TM, Ashe, JH, Weinberger, NM. Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency-specific effects of muscarinic agonists. Synapse 1989;4:30–43.Google Scholar
83. Metherate, R, Weinberger, NM. Acetylcholine produces stimulus- specific receptive field alterations in cat auditory cortex. Brain Res 1989;480:372–377.Google Scholar
84. Bandrowski, AE, Moore, SI. Ashe, JH. Cholinergic synaptic potentials in the superagranular layers of auditory cortex. Synapse 2001;41:118–130.CrossRefGoogle ScholarPubMed
85. Ji, W, Gao, E, Suga, N. Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J Neurophysiol 2001;86:211–225.CrossRefGoogle ScholarPubMed
86. Thiel, CM, Friston, KJ, Dolan, RJ. Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron 2002;35(3):567–574.Google Scholar
87. Bjordahl, TS, Dimyan, MA, Weinberger, NM. Induction of long- term receptive field plasticity in the auditory cortex of the waking guinea pig by stimulation of the nucleus basalis. Behav Neurosci 1998;112(3):1–13.Google Scholar
88. Dimyan, MA, Weinberger, NM. Basal forebrain stimulation induces discriminative receptive field plasticity in the auditory cortex. Behav Neurosci 1999;113(4):691–702.Google Scholar
89. Kilgard, MP, Merzenich, MM. Cortical map reorganization enabled by nucleus basalis activity. Science 1998;279:1714–1718.Google Scholar
90. McLin, DE 3rd, Miasnikov, AA, Weinberger, NM. Induction of behavioral associative memory by stimulation of the nucleus basalis. Proc Natl Acad Sci USA 2002;99(6):4002–4007.Google Scholar
91. Miasnikov, AA, McLin, DE 3rd, Weinberger, NM. Muscarinic dependence of nucleus basalis induced conditioned receptive field plasticity. Neuroreport 2001;12(7):1537–1542.Google Scholar
92. Aramakis, VB, Metherate, R. Nicotine selectively enhances NMDA receptor-mediated synaptic transmission during postnatal development in sensory neocortex. J Neurosci 1998;18(20):8485–8495.Google Scholar
93. Gu, Q, Singer, W. Effects of intracortical infusion of anticholinergic drugs on neuronal plasticity in kitten striate cortex. Eur J Neurosci 1993;5(5):475–485.Google Scholar
94. Brown, JH, Taylor, P. Muscarinic receptor agonists and antagonists. In: Hardman, JG, Limbrid, LE, (Eds). The Pharmacological Basis of Therapeutic, ed 9, New York: McGraw-Hill, 1996;141–160.Google Scholar
95. Wess, J, Buhl, T, Lambrecht, G, Mutschler, E. Cholinergic receptors. In: Emmett, J, (Ed). Comprehensive Medicinal Chemistry, Vol. 3, Oxford:Pergamon, 1990;423–491.Google Scholar
96. Bakin, JS, Weinberger, NM. Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci USA 1996;93(20):11219–11224.CrossRefGoogle ScholarPubMed
97. Krnjevic, K. Central cholinergic mechanisms and function. Prog Brain Res 1993;98:285–292.CrossRefGoogle ScholarPubMed
98. Saar, D, Grossman, Y, Barkai, E. Long-lasting cholinergic modulation underlies rule learning in rats. J Neurosci 2001;21(4):1385–1392.Google Scholar
99. Rouse, ST, Hamilton, SE, Potter, LT, Nathanson, NM, Conn PJ. Muscarinic-induced modulation of potassium conductances is unchanged in mouse hippocampal pyramidal cells that lack functional M1 receptors. Neurosci Lett 2000;278(1–2):61–64.Google Scholar
100. Haj-Dahmane, S, Andrade, R. Ionic mechanism of the slow afterdepolarization induced by muscarinic receptor activation in rat prefrontal cortex. J Neurophysiol 1998;80(3):1197–1210.Google Scholar
101. Levey, AI. Immunological localization of M1-M5 muscarinicacetylcholine receptors in peripheral tissues and brain. Life Sci 1993;52:441–448.CrossRefGoogle Scholar
102. Levey, AI, Kitt, CA, Simonds, WF, Price, DL, Brann, MR. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 1991;11:3218–3226.Google Scholar
103. Rotter, T. The molecular basis of muscarinic receptor diversity. Trends Neurosci 1989;12:148–151.Google Scholar
104. Gordon, JA, Stryker, MP. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J Neurosci 1996;16(10):3274–3286.Google Scholar
105. Gu, Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neurosci 2002;111(4):815–835.Google Scholar
106. Hohmann, CF, Potter, ED, Levey, AI. Development of muscarinic receptor subtypes in the forebrain of the mouse. J Comp Neurol 1995;358(1):88–101.Google Scholar
107. Tan, XX, Costa, LG. Postnatal development of muscarinic receptor-stimulated phosphoinositide metabolism in mouse cerebral cortex: sensitivity to ethanol. Brain Res Dev Brain Res 1995;86(1–2):348–353.Google Scholar
108. Zhang, Y, Suga, N, Yan, J. Corticofugal modulation of frequency-processing in bats auditory system. Nature 1997;387:900–903.Google Scholar
109. Yan, J, Ehret, G. Corticofugal modulation of midbrain sound pro-cessing in the house mouse. Eur J Neurosci 2002;16(1):119–128.CrossRefGoogle Scholar
110. Yan, W, Suga, N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat Neurosci 1998;1:54–58.Google Scholar
111. Suga, N, O’Neill, WE. Neural axis representing target range in the auditory cortex of the mustache bat. Science 1979;206(4416):351–353.Google Scholar
112. Yan, J, Suga, N. The midbrain creates and the thalamus sharpens echo-delay tuning for the cortical representation of target-distance information in the mustached bat. Hear Res 1996;93(1–2):102–110.CrossRefGoogle ScholarPubMed
113. Yan, J, Suga, N. Corticofugal modulation of time-domain processing of biosonar information in bats. Science 1996;273:1100–1103.Google Scholar
114. Sakai, M, Suga, N. Centripetal and centrifugal reorganizations of frequency map of auditory cortex in gerbils. Proc Natl Acad Sci USA 2002;99(10):7108–7112.Google Scholar
115. Yan, J, Ehret, G. Corticofugal reorganization of midbrain tonotopic map in mice. Neuroreport 2001;12(15):3313–3316.Google Scholar
116. Auladell, C, Perez-Sust, P, Super, H, Soriano, E. The early development of thalamocortical and corticothalamic projections in the mouse. Anat Embryol 2000;201(3):169–179.Google Scholar
117. Winer, JA. 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. New York: Springer-Verlag, 1992:222–409.CrossRefGoogle Scholar
118. Andersen, RA, Synder, RL, Merzenich, MM, The topographic organization of corticocollicular projections from physiologically identified loci in the AI, AII, and anterior auditory cortical field of the cat. J Comp Neurol 1980;191:479–494.Google Scholar
119. Herbert, H, Aschoff, A, Ostwald, J. Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol 1991;304:103–122.Google Scholar
120. Saldana, E, Feliciano, M, Mugnaini, E. Distribution of descending projections from primary auditory neocortex to inferior colliculus mimics the topography of intracollicular projections. J Comp Neurol 1996;371:15–40.Google Scholar
121. Rutkowski, RG, Than, K., Weinberger, NM, Evidence for area of frequency representation encoding acquired stimulus importance in rat primary auditory cortex. Program No. 80.3. 2002 Abstract Viewer/Itinerary Planner. Washington, DC:Society for Neuroscience, 2002. Online.Google Scholar