摘要
在上行听觉通路中,下丘(inferior colliculus, IC)接收并整合众多来自于低位脑干的听觉核团,IC的内在投射,对侧IC的连合投射,以及来自听皮层的兴奋性和抑制性输入。所有这些投射联系使得IC成为皮层下听信息的时相和空间整合的一个重要中枢。本研究在自由声场条件下,通过电生理记录,局部电刺激和离子电泳技术,在昆明小鼠中研究了局部电刺激一侧IC(简称为ICES)如何对另一侧IC(简称为ICMdu)声信号强度域的加工进行调制,并探讨了与双侧IC间相互作用有关的生物学意义和可能的功能作用途径。所获得的主要研究结果如下:
1.在实时的ICES局部电刺激条件下,记录到50个ICMdu神经元在电刺激前后对声刺激的完整的强度-放电率函数(rate-amplitude function, RAF)。根据被刺激侧神经元(ICES)与被调制侧神经元(ICMdu)J的最佳频率差(best frequency, BF)将ICMdu神经元分为两类,其中26个ICMdu神经元的BF差≤2kHz,称为双侧对应频率层神经元(bilateral corresponding frequency laminea, BCFL);另外24个ICMdu(?)经元的BF差>2kHz,称为双侧非对应频率层神经元(bilateral non-corresponding frequency laminea, BNCFL)。ICES局部电刺激时,14.0%ICMdu神经元的声反应被易化,这部分受兴奋性调制的ICMdu神经元均位于BCFL;而86.0%ICMdu神经元的声反应被抑制,受抑制性调制的ICMdu神经元广泛分布于BCFL(38.0%)和BNCFL(48.0%)中。双侧IC间的相互作用可增加受兴奋性调制的ICMdu神经元的放电率拓宽神经元反应的动态范围(dynamic range, DR)并减小RAF的斜率,从而获得对声刺激强度更广泛的响应范围。相反,双侧IC间相互作用减少受抑制性调制的ICMdu神经元的放电率和DR,并增加RAF的斜率,使得神经元对声刺激强度的敏感性被锐化。而且BCFL神经元所受到的抑制性调制作用的程度显著强于BNCFL神经元。
2.实验获得了70个受双侧IC间调制的ICMdu神经元,局部电刺激一侧IC对对侧IC的声反应的影响表现为广泛的抑制(87.1%)和集中或局灶性(foucus)兴奋(12.9%),且受抑制性和兴奋性调制的两组神经元在IC中的分布并无明显的拓扑分界。这一调制作用的影响在较低声刺激强度下表现的更为明显,且依赖于声电刺激间间隔。在最佳声电刺激间隔下,受抑制性调制的IC神经元的反应幅度最小而反应潜伏期最长,而受兴奋性调制的IC神经元则表现出相反的效应。一侧IC的局部电刺激可以压抑或是易化对侧IC神经元的RAF,且双侧IC交互电刺激的结果显示这一调制作用在双侧IC间既可以是相互的,也可能是单侧的。局部电刺激同样可引起IC神经元的BF,最小阈值(minimum threshold, MT),反应潜伏期和DR的改变,这一变化平均可持续约150分钟。双侧IC间相互作用对这些参数的调制程度取决于刺激侧IC神经元与被调制IC神经元间BF差。对受抑制性和兴奋性调制的神经元分别离子电泳注射荷包牡丹碱(bicuculline, Bic)和犬尿酸(kynurenic acid, KA)后,由局部电刺激所致的双侧IC间抑制性和兴奋性调制作用的影响可全部或部分被解除。表明双侧IC间的相互作用主要由GABA能受体和谷氨酸能受体介导。
3.双侧IC间的调制作用通过集中的点对点兴奋性投射来增强IC神经元的声反应并获得对声刺激的更好的强度响应,或通过更为广泛分布的抑制性锐化IC神经元的强度敏感性来影响IC对声信号强度域的加工。双侧IC间少部分集中的兴奋性调制和大多数广泛的抑制性调制作用,有可能分别参与了IC神经元双耳听觉特性的形成,如EE(excitation-excitation)和El (excitation-inhibition)神经元的形成;这种不平衡的兴奋和抑制性投射的分布可能在动物听声辨位和保证单侧优势中起着重要的作用。双侧IC间相互作用对IC神经元强度信号加工的调制作用可能建立在双侧IC的声调拓扑组构基础之上,并参与了IC听经验依赖的可塑性。
以上结果和发现提示,双侧IC间的相互作用为IC声信号的加工提供了一种可调的且可塑的调制模式。
In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commisure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examined bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, focal electrical stimulation and ionophoresis. The responses of IC neurons (abbreviated as ICMdu neurons) of mice(Mus musculus, Km) were recorded before, during and after the electrical stimulating of contralateral IC neurons (abbreviated as ICES neurons). The possible biological significance and neural pathways underlying the bilateral collicular interaction were discussed.
1. Fifty ICMdu neurons were classified as two groups according to the best frequency (BF) difference between ICMdu and ICES neuron. For simplicity,26ICMdu neurons were called bilateral corresponding frequency lamina (BCFL) neurons only if the BF difference was within2kHz. Otherwise24ICMdu neurons were called bilateral non-corresponding frequency lamina (BNCFL) neurons. During focally electrical stimulation of the contralateral IC neurons,14.0%IC neurons were facilitated and located in BCFL while86.0%IC neurons were inhibited and widespreadly located in BCFL (38.0%) and BNCFL (48.0%). The facilitatory modulation of bilateral collicular interaction increased the number of impulses and dynamic ranges (DRs) of facilitated IC neurons but decreased the slope of their rate-amplitude functions (RAFs) for wider amplitude responses to sound stimulus. Otherwise, the inhibitory modulation of bilateral collicular interaction decreased the number of impulses and DR of inhibited IC neurons but increased the slopes of their RAFs for sharper sensitivity to sound amplitude. Moreover the degree of inhibitory modulation was greater in BCFL neurons than in BNCFL neurons.
2. Seventy ICMdu neurons were studied for bilateral collicular interaction. Focal electrical stimulation of ICES produces widespread inhibition (87.1%) and focused facilitation (12.9%) of responses of contralateral ICMdu neurons. This bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited ICmdu neurons but produces an opposite effect in the response of facilitated ICMdu neurons. This modulation effect is most effective at low sound amplitude and is dependent upon the time interval between the acoustic and electric stimuli. At the optimal inter-stimulus interval, the inhibited ICMdu neurons have the smallest response magnitude and the longest response latency during focal electrical stimulation while the opposite effects are observed for the facilitated ICMdu neurons. The focal electrical stimulation of ICES compresses or expands the RAF of contralateral ICMdu neurons to improve the sensitivity in the change or range of amplitude. This bilateral collicular interaction is found to be either reciprocal or unilateral by alternatively electical stimulating paires neurons in both IC. The focal electrical stimulation also produces a shift in a neuron's minimum threshold and dynamic range for as long as150minutes. The degree of bilateral collicular interaction is dependent upon the difference in BF between the electrically stimulated IC neurons and the affected IC neurons. The results suggest that bilateral collicular interaction is mainly to change the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Respective ionophoretic application of bicuculline and kynurenic acid to inhibited and facilitated neurons shows that bilateral collicular interaction induced by focal electrical stimulation can be eliminated or only partly abolished.
The role of bilateral collicular interaction in amplitude-domain signal processing is to mudulate the amplitude signal processing by sharpening the amplitude sensitivity through wide spread inhibition and by enhancing response of facilitated IC neurons for better amplitude responsiveness to tuned sound stimulus through the more focused point-to-point connections. The small proportion of bilateral collicular facilitatory interaction between neurons in BCFL observed in our study may be involved in the formation of binaural property of EE (excitation-excitation) neurons. Conversly, the large proportion of bilateral collicular inhibitory interaction between the neurons in BCFL and BNCFL can perhaps match a high proportion of the El (excitation-inhibition) neurons and may be involved in the formation of binaural property of El neurons. The unbalanced property between excitatory and inhibitory projections have very important role in the formation of unilateral auditory dominance and sound location. The bilateral collicular interaction modulates the amplitude signal processing of IC neuron on the basis of topographic projections between two ICs, and it may be also invovled in acoustic-experience-dependent plasticity in the IC. The bilateral collicular interaction which was mediated by GABAergic and glutamatergic receptors provide an adjustable and plastic modulation pattern for auditory signal processing of ICs.
引文
[1]韩琳琳,杨文伟,张皓,张季平,孙心德(2008)小鼠听皮质对下丘神经元方位敏感性的调控.生物物理学报.24:6-14.
[2]梅慧娴,郭玉萍,吴飞健,陈其才(20)05)不同时程弱前掩蔽声对小鼠下丘神经元声反应的选择性抑制.生物物理学报.21(6):418-424.
[3]王放,孙心德(2010)不同的声音强度对大鼠听皮层神经元特征频率可塑性的影响.中国应用生理学杂志.26(1):55-58.
[4]Adams JC (1979) Ascending projections to the inferior colliculus. J Comp Neurol. 183:519-538.
[5]Adams JC (1980) Crossed and descending projections to the inferior colliculus. Neurosci Lett.19(1):1-5.
[6]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(4):837-47.
[7]Aitkin LM, Kenyon CE, Philpott P (1981) The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J Camp Neurol.196(1):25-40.
[8]Aitkin LM, Phillips SC (1984) The interconnections of the inferior colliculi through their commissure. J Comp Neurol.228:210-216.
[9]Andersen RA, Roth GL, Aitkin LM, Merzenich MM (1980) The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J Comp Neurol.194(3):649-62.
[10]Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol.179:641-667.
[11]Bajo VM, Merchan MA, Lopez DE, Rouiller EM (1993) Neuronal morphology and efferent projections of the Dorsal nucleus of the lateral lemniscus in the rat. J Comp Neurol.334(2):241-62.
[12]Bajo VM, Moore DR (2005) Descending projections from the auditory cortex to the inferior colliculus in the gerbil, Meriones unguiculatus. J Comp Neurol. 486:101-116.
[13]Bakin JS, Weinberger NM (1990) Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 536:271-286.
[14]Bao S, Chan VT, Merzenich MM (2001) Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature.412:79-83.
[15]Bergan JF, Knudsen El (2009) Visual modulation of auditory responses in the owl inferior colliculus. J Neurophysiol.101:2924 - 2933.
[16]Blake DT, Heiser MA, Caywood M, Merzenich MM (2006) Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron.52:371-81
[17]Bormann J (1988) Electrophysiology of GABAA and GABAB receptor subtypes. Trend Neurosci.11:112-116.
[18]Browner RH, Webster DB (1975) Projections of the trapezoid body and the superior olivary complex of the Kangaroo rat (Dipodomys merriami). Brain Behav Evol. 11(5-6):322-54.
[19]Budinger E, Heil P, Scheich H (2000) Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). IV. Connections with anatomically characterized subcortical structures. Eur J Neurosci.12(7):2452-74.
[20]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.495:511-528.
[21]Casseday JH, Covey E (1996) A neuroetho logical theory of the operation of the inferior colliculus. Brain Behav Evol.47(6):311-36.
[22]Casseday JH, Ehrlich D, Covey E (2000) Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. J Neurophysiol.84(3):1475-87.
[23]Casseday JH, Fremouw T, Covey E (2002) In:The inferior colliculus:a hub for the central auditory system, edited by Oertel D, Fay RR, Popper AN. Integrative Functions in the Mammalian Auditory Pathway. Springer, New York, pp 238-318.
[24]Champoux F, Paiement P, Mercier C, Lepore F, Lassonde M, Gagne JP (2007) Auditory processing in a patient with a unilateral lesion of the inferior colliculus. Eur JNeurosci.25(1):291-7
[25]Chang EF, Bao S, Imaizumi K, Schreiner CE, Merzenich MM (2005) Development of spectral and temporal response selectivity in the auditory cortex. Proc Natl Acad 5ci USA.102:16460-16465.
[26]Chang EF, Merzenich MM (2003) Environmental noise retards auditory cortical development. Science.300:498-502.
[27]Chen G, Yan J (2007) Cholinergic modulation incorporated with a tone presentation induces frequency-specific threshold decreases in the auditory cortex of the mouse. Eur J Neurosci.25:1793-1803.
[28]Covey E, Casseday JH (1995) The lower brainstem auditory pathways. In:hearing by Bats, edited by Popper AN and Fay RR. New york, Springer-Berlag. pp 146-190.
[29]de Villers-Sidani E, Chang EF, Bao S, Merzenich MM (2007) Critical period window for spectral tuning defined in the primary auditory cortex (AI) in the rat. J Neurosci.27:180-189.
[30]de Villers-Sidani E, Simpson KL, Lu YF, Lin RC, Merzenich MM (2008) Manipulating critical period closure across different sectors of the primary auditory cortex. Nat Neurosci.11:957-965.
[31]Dehmel S, Cui YL, Shore SE (2008) Cross-modal interactions of auditory and somatic inputs in the brainstem and midbrain and their imbalance in tinnitus and deafness. Am J Audiol 17(2):S193-209.
[32]Dexter F, Brown DL (2004). Financial disclosure. Anesth Analg 98,1811.
[33]Faye-Lund H, Osen KK (1985) Anatomy of the inferior colliculus in rat. Anat Embryol (Berl).171(1):1-20.
[34]Feliciano M, Saldana E, Mugnaini E (1995) Direct projections from the rat primary auditory neocortex to nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei. And Neurosci.1:287-308.
[35]Feliciano M, Potashner SJ (1995) Evidence for a glumamayergic pathway from the guinea pig auditory cortex to the inferior colliculus. J Neurochem.65(3):1348-57.
[36]Fritz J, Shamma S, Elhilali M, Klein D (2003) Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat Neurosci.6: 1216-23.
[37]Fubara BM, Casseday JH, Covey E, Schwartz-Bloom RD (1996) Distribution of GABAA, GABAB and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus. J Comp Neurol.369:83-92.
[38]Gao E, Suga N (1998) Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system. Proc Natl Acad Sci USA.95:12663-12670.
[39]Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats:role of the corticofugal system. Proc Natl Acad Sci USA.97:8081-8086.
[40]Glendenning KK, Baker BN, Hutson KA, Masterton RB (1992) Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSO. J Comp Neurol.319:100-122.
[41]Glendenning KK, Brunso-Bechtold JK, Thompson GC, Masterton RB (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J Comp Neurol. 197(4):673-703.
[42]Glendenning KK, Hutson KA, Nudo RJ, Masterton RB (1985) Acoustic chiasm Ⅱ: Anatomical basis of binaurality in lateral superior olive of cat. J Comp Neurol. 232(2):261-85.
[43]Glendenning KK, Hutson KA(1998) Lack of topography in the ventral nucleus of the lateral lemniscus. Microsc Res Tech.41(4):298-312.
[44]Glendenning KK, Masterton RB (1983) Acoustic chiasm:efferent projections of the lateral superior olive. J Neurosci.3(8):1521-37.
[45]Gonzalez-Hernandez T, Mantolan-Sarmiento B, Gonzalez-Gonzalez B, Perez-Gonzalez H (1996) Sources of GABAergic input to the inferior colliculus of the rat. J Comp Neurol.372:309-26.
[46]Grutzendler J, Kasthuri N, Gan WB (2002) Long-term dendritic spine stability in the adult cortex. Nature.420:812-816.
[47]Helfert RH, Bonneau JM, Wenthold RJ, Altschuler RA (1989) GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res. 501(2):269-86.
[48]Henkel CK (1983) Evidence of sub-collicular auditory projections to the medial geniculate nucleus in the cat:an autoradiographic and horseradish peroxidase study. Brain Res.259(1):21-30.
[49]Henkel CK, Brunso-Bechtold JK (1993) Laterality of superior olive projections to the inferior colliculus in adult and developing ferret. J Comp Neurol.331 (4):458-68.
[50]Henkel CK, Shneiderman A (1988) Nucleus sagulum:projections of a lateral tegmental area to the inferior colliculus in the cat. J Comp Neurol.271(4):577-88.
[51]Herbert H, Aschoff A, Ostwald J (1991) Topography of projections from the auditory cortex to the inferior colliculus in the rat. J Comp Neurol.304:103-122.
[52]Hernandez O, Rees A, Malmierca MS (2006) A GABAergic component in the commissure of the inferior colliculus in rat. Neuroreport.17:1611-1614.
[53]Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron.45:279-291.
[54]Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K (2006) Experience-dependent and cell-type-specific spine growth in the neocortex. Nature. 441:979-983.
[55]Huffman RF, Henson OW (1990) The descending auditory pathways and acoustic motor systems:connections with the inferior colliculus. Brain Res Rev 15:295-323.
[56]Hutson KA, Glendenning KK, Masterton RB (1991) Acoustic chiasm. IV:Eight midbrain decussations of the auditory system in the cat. J Comp Neurol. 312(1):105-31.
[57]Inglis WL, Olmstead MC, Robbins TW (2000) Pedunculopontine tegmental nucleus lesions impair stimulus--reward learning in autoshaping and conditioned reinforcement paradigms. Behav Neurosci.114:285-294.
[58]Insanally MN, Kover H, Kim H, Bao S (2009) Feature-dependent sensitive periods in the development of complex sound representation. J Neurosci.29:5456-5462.
[59]Jafari MR, Zhang Y, Yan J (2007) Multiparametric change in the receptive field of cortical auditory neurons induced by thalamic activation in the mouse. Cere cortex. 17:71-80.
[60]Jain R, Shore S (2006) External inferior colliculus integrates trigeminal and acoustic information:unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig. Neurosci Lett.395(1):71-5.
[61]Jen PHS, Chen QC, Sun XD (1998) Corticofugal regulation of auditory sensitivity in the bat inferior colliculus. J Comp Physiol A.183:683-697.
[62]Jen PHS, Chen QC, Wu FJ (2002a) Interaction between excitation and inhibition affects frequency tuning curve, response size and latency of neurons in the auditory cortex of the big brown bat, Eptesicus fuscus. Hear Res.174:281-289.
[63]Jen PHS, Feng RB (1999) Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons. J Comp PhysiolA.184(2):185-94.
[64]Jen PHS, Schlegel P (1982) Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol A. 147:351-364.
[65]Jen PHS, Sun XD, Chen QC (2001) An electrophysiological study of neural pathways for corticofugally inhibited neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus. Exp Brain Res.137:292-302.
[66]Jen PHS, Wu FJ, Chen QC (2002b) The effect of two-tone stimulation on responses of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. Hearing Res.168:139-149.
[67]Jen PHS, Zhou XM (2003) Corticofugal modulation of amplitude domain processing in the midbrain of the big brown bat, Eptesicus fuscus. Hear Res.184: 91-106.
[68]Ji W, Gao E, Suga N (2001) Effects of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J Neurophysiol. 86:211-225.
[69]Ji W, Suga N (2007) Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning. JNeurosci.27(18):4910-8.
[70]Kayser C, Petkov CI, Logothetis NK (2008) Visual modulation of neurons in the auditory cortex. Cereb Cortex.18:1560-1574.
[71]Kelly JB, Kavanagh GL (1994) Sound localization after unilateral lesion of inferior colliculus in the ferret (Mustela putorius). J Neurophysiol.71:1078-1087.
[72]Kelly JB, Sally SL (1988) Organization of auditory cortex in the albino rat:binaural response properties, J Neurophysiol.59:1756-1769.
[73]Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science.279:1714-1718.
[74]Klug A, Park TJ, Pollak GD (1995) Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat. J Neurophysiol.74:1701-1713.
[75]Knudsen, El (1999) Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl. J Comp Physiol A.185:305-321.
[76]Knudsen El, Mogdans J (1992) Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl optic tectum. J Neurosci.12:3485-3493.
[77]Koch U, Grothe B (1998) GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol. 80:71-82.
[78]Koyama Y, Jodo E, Kayama Y (1994) Sensory responsiveness of "broad-spike" neurons in the laterodorsal tegmental nucleus, locus coeruleus and dorsal raphe of awake rats:implications for cholinergic and monoaminergic neuron-specific responses. Neuroscience.63:1021-1031.
[79]Kudo M (1981) Projections of the nuclei of the lateral lemniscus in the cat:an autoradiographic study. Brain Res.221(1):57-69.
[80]Kulesza RJ, Vinuela A, Saldana E, Berrebi AS (2002) Unbiased stereological estimates of neuron number in subcortical auditory nuclei of the rat. Hear Res. 168(1-2):12-24.
[81]Kumoi K, Saito N, Tanaka C (1993) Immunohistochemical localization of gamma-aminobutyric acid-and aspartate-containing neurons in the guinea pig superior olivary complex. Hear Res.68(2):173-9.
[82]Kiinzle H (1993) Tectal and related target areas of spinal and dorsal column nuclear projections in hedgehog tenrecs. Somatosens Mot Res.10(3):339-53.
[83]Kuwabara N, Zook JM (2000) Geniculo-collicular descending projections in the gerbil. Brain Res.878(1-2):79-87.
[84]Leake PA, Hradek GT, Chair L, Snyder RL (2006) Neonatal deafness results in degraded topographic specificity of auditory nerve projections to the cochlear nucleus in cats. J Comp Neuro.1497:13-31.
[85]Leake PA, Snyder RL, Rebscher SJ, Moore CM, Vollmer M (2000) Plasticity in central representations in the inferior colliculus induced by chronic single-vs. two-channel electrical stimulation by a cochlear implant after neonatal deafness. Hear Res.147:221-241.
[86]Li H, Mizuno N (1997) Direct projections from nucleus X to the external cortex of the inferior colliculus in the rat. Brain Res.774(1-2):200-6.
[87]Litovsky RY, Fligor BJ, Tramo MJ (2002) Functional role of the human inferior colliculus in binaural hearing. Hear Res.165(1-2):177-88.
[88]Lu Y, Jen PHS (2001) GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons. Exp Brain Res.141:331-339.
[89]Lu Y, Jen PHS (2002) Interaction of excitation and inhibition in inferior collicular neurons of the big brown bat, Eptesicu fuscus. Hearing Res.169:140-150.
[90]Lu Y, Jen PHS (2003) Binaural interaction in the inferior colliculus of the big brown bat, Eplesicus fuscus. Hearing Res.177:100-110.
[91]Lu Y, Jen PHS, Wu M (1998) GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses. J Newophysiol. 79:2303-2315.
[92]Lu Y, Jen PHS, Zheng QY (1997) GABAergic disinhibition changes the recovery cycle of bat inferior colliculus neurons. J Comp Physiol A.181:331-341.
[93]Ma X, Suga N (2001a) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc Natl Acad Sci USA.98:14060-14065.
[94]Ma X, Suga N (2001b) Plasticity of bat's central auditory system evoked by focal electric stimulation of auditory and/or somatosensory cortices. J Neurophysiol. 85:1078-1087.
[95]Ma X, Suga N (2003) Augmentation of plasticity of the central auditory system by the basal forebrain and/or somatosensory cortex. J Neurophysiol.89:90-103.
[96]Ma X, Suga N (2007) Multiparametric corticofugal modulation of collicular duration-tuned neurons:modulation in the amplitude domain. J Neurophysiol. 97(5):3722-30.
[97]Ma X, Suga N (2008) Corticofugal modulation of the paradoxical latency shifts of inferior collicular neurons. J Neurophysiol.100:1127-34.
[98]Malmierca MS (2003) The structure and physiology of the rat auditory system:an overview. Int Rev Neurobiol.56:147-211.
[99]Malmierca MS, Izquierdo MA, Cristaudo S, Hernandez O, Perez-Gonzalez D, Covey E, Oliver DL (2008) A discontinuous tonotopic organization in the inferior colliculus of the rat. J Neurosci.28:4767-4776.
[100]Malmierca MS, Leergaard TB, Bajo VM, Bjaalie JG, Merchan MA (1998) Anatomic evidence of a three-dimensional mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in cat. J Neurosci.18(24):10603-18.
[101]Malmierca MS, Hernandez O, Antunes F M, Rees A (2009) Divergent and point-to-point connections in the commissural pathways between the inferior colliculi.J Comp Neurol.514:226-239.
[102]Malmierca MS, Hernandez O, Falconi A, Lopez-Poveda EA, Merchan M, Rees A (2003) The commissure of the inferior colliculus shapes frequency response areas in rat:an in vivo study using reversible blockade with microinjection of kynurenic acid. Exp Brain Res.153:522-529.
[103]Malmierca MS, Hernandez O, Rees A (2005a) Intercollicular commissural projections modulate neuronal responses in the inferior colliculus. Eur J Neurosci. 21:2701-2710.
[104]Malmierca MS, Merchan MA, Henkel CK, Oliver DL (2002) Direct projections from cochlear nuclear complex to auditory thalamus in the rat. J Neurosci. 22(24):10891-7.
[105]Malmierca MS, Saint Marie RL, Merchan MA, Oliver DL (2005b) Laminar inputs from dorsal cochlear nucleus and ventral cochlear nucleus to the central nucleus of the inferior colliculus:two patterns of convergence. Neuroscience.136:883-894.
[106]Malmierca MS, Rees A, Le Beau FE, Bjaalie JG (1995) Laminar organization of frequency-defined local axons within and between the inferior colliculi of the guinea pig. J Comp Neurol.357:124-144.
[107]Marsh RA, Fuzessery ZM, Grose CD, Wenstrup JJ (2002) Projection to the inferior colliculus from the basal nucleus of the amygdala. J Neurosci.22(23):10449-60.
[108]Massopust LC, Hauge DH, Ferneding JC, Doubek WG, Taylor JJ (1985) Projection systems and terminal localization of dorsal column afferents:an autoradiographic and horseradish peroxidase study in the rat. J Comp Neurol.237(4):533-44.
[109]Merchan MA, Berbel P (1996) Anatomy of the ventral nucleus of the lateral lemniscus in rats:a nucleus with a concentric laminar organization. J Comp Neurol. 372(2):245-63.
[110]Merchan M, Aguilar LA, Lopez-Poveda EA, Malmierca MS (2005) The inferior colliculus of the rat:quantitative immunocytochemical study of GAB A and glycine. Neuroscience.136:907-25.
[111]Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat:an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience.10:1185-1201.
[112]Moore DR, King AJ (2004) plasticity of binaural systems. In:Plasticity of the Auditory System, edited by Parks TN, Rubel EW, Fay RR, Popper AN. Springer; 96-172.
[113]Moore DR, Kotak VC, Sanes DH (1998) Commissural and lemniscal synaptic input to the gerbil inferior colliculus. J Neurophysiol.80:2229-2236.
[114]Moore RY, Bloom FE (1978) Central catecholamine neuron systems:anatomy and physiology of the dopamine systems. Annu Rev Neurosci.1:129-169.
[115]Moore RY, Goldberg JM (1966) Projections of the inferior colliculus in the monkey. Exp Neurol.14(4):429-38.
[116]Moriizumi T, Leduc-Cross B, Wu JY, Hattori T (1992) Separate neuronal populations of the rat substantia nigra pars lateralis with distinct projection sites and transmitter phenotypes. Neuroscience.46(3):711-20.
[117]Moriizumi T, Hattori T (1991) Pallidotectal projection to the inferior colliculus of the rat. Exp Brain Res.87(1):223-6.
[118]Nakahara H, Zhang LI, Merzenich MM. (2004) Specialization of primary auditory cortex processing by sound exposure in the "critical period". Proc Natl Acad Sci USA.101:7170-7174.
[119]Nordeen KW, Killackey HP, Kitzes LM (1983) Ascending auditory projections to the inferior colliculus in the adult gerbil, Meriones unguiculatus. J Comp Neurol. 214(2):131-43.
[120]Norena AJ, Gourevitch B, Aizawa N, Eggermont JJ (2006) Spectrally enhanced acoustic environment disrupts frequency representation in cat auditory cortex. Nat Neurosci.9:932-939.
[121]Olazabal UE, Moore JK (1989) Nigrotectal projection to the inferior colliculus: horseradish peroxidase transport and tyrosine hydroxylase immunohistochemical studies in rats, cats, and bats. J Comp Neurol.282(1):98-118.
[122]Oliver DL (1984) Dorsal cochlear nucleus projections to the inferior colliculus in the cat:a light and electron microscopic study.J Comp Neurol.224(2):155-72.
[123]Oliver DL (1987) Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat:possible substrates for binaural interaction. J Comp Neurol.264(1):24-46.
[124]Oliver DL, Beckius GE, Shneiderman A (1995) Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat:a study using electron microscopic autoradiography. J Comp Neurol.360(1):17-32.
[125]Oliver DL, Winer JA, Beckius GE, Saint Marie RL (1994) Morphology of GABAergic neurons in the inferior colliculus of the cat.J Comp Neurol.340:27-42.
[126]Osen KK (1972) Projection of the cochlear nuclei on the inferior colliculus in the cat. J Comp Neurol.144(3):355-72.
[127]Paloff AM, Usunoff KG (1992) Projections to the inferior colliculus from the dorsal column nuclei. An experimental electron microscopic study in the cat.J Hirnforsch.33(6):597-610.
[128]Pantev C, Lutkenhoner B (2000) Magnetoencephalographic studies of functional organization and plasticity of the human auditory cortex. J Clin Neurophysio.l 17:130-142.
[129]Pantev C, Oostenveld R, Engelien A, Ross B, Roberts LE, Hoke M (1998) Increased auditory cortical representation in musicians. Nature.392:811-814.
[130]Polley DB, Steinberg EE, Merzenich MM (2006) Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci. 26:4970-4982.
[131]Poon PW, Chen X (1992) Postnatal exposure to tones alters the tuning characteristics of inferior collicular neurons in the rat. Brain Res.585:391-394.
[132]Popelar J, Nwabueze-Ogbo FC, Syka J (2003) Changes in neuronal activity of the inferior colliculus in rat after temporal inactivation of the auditory cortex. Physiol Res. 52:615-628.
[133]Razak KA, Richardson MD, Fuzessery ZM (2008) Experience is required for the maintenance and refinement of FM sweep selectivity in the developing auditory cortex. Proc Natl Acad Sci USA.105:4465-4470.
[134]Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci.13:87-103.
[135]Richardson RT, DeLong MR (1991) Electrophysiological studies of the functions of the nucleus basalis in primates. Adv Exp Med Biol.295:233-252.
[136]Roberts RC, Ribak CE (1987) An electron microscopic study of GABAergic neurons and terminals in the central nucleus of the inferior colliculus of the cat.J Neurocytol.16:333-345.
[137]Romanski LM, Clugnet MC, Bordi F, LeDoux JE (1993) Somatosensory and auditory convergence in the lateral nucleus of the amygdala. Behav Neurosci. 107(3):444-50.
[138]Saint Marie RL (1996) Glutamatergic connections of the auditory midbrain: selective uptake and axonal transport of D-[3H] aspartate. J Comp Neurol.373: 225-270.
[139]Saldana E, Aparicio MA, Fuentes-Santamaria V, Berrebi AS (2009) Connections of the superior paraolivary nucleus of the rat:projections to the inferior colliculus. Neuroscience.163(1):372-87.
[140]Saldana 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.371:15-40.
[141]Saldana E, Merchan MA (1992) Intrinsic and commissural connections of the rat inferior colliculus.J Comp Neurol.319:417-437.
[142]Sanes DH, Constantine-Paton M (1985) The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus.J Neurosci.5:1152-1166.
[143]Sanes DH, Siverls V (1991) Development and specificity of inhibitory terminal arborizations in the central nervous system. J Neurobiol.22:837-854.
[144]Seidl AH, Grothe B (2005) Development of sound localization mechanisms in the mongolian gerbil is shaped by early acoustic experience. J Neurophysiol. 94:1028-1036.
[145]Schreiner CE, Langner G (1997) Laminar fine structure of frequency organization in auditory midbrain. Nature.388:383-386.
[146]Schweizer H (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum). J Comp Neurol.201(1):25-49.
[147]Shammah-Lagnado SJ, Alheid GF, Heimer L (1996) Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol.376(3):489-507.
[148]Shen.JX, Chen QC, Jen PHS (1997) Binaural and frequency representation in the primary auditory cortex of the big brown bat, Eptesicus fuscus. J Comp Physiol A. 181:591-597.
[149]Shinonaga Y, Takada M, Mizuno N (1994) Direct projections from the non-laminated divisions of the medial geniculate nucleus to the temporal polar cortex and amygdala in the cat. J Comp Neurol.340(3):405-26.
[150]Shneiderman A, Chase MB, Rockwood JM, Benson CG, Potashner SJ (1993) Evidence for a GABAergic projection from the dorsal nucleus of the lateral lemniscus to the inferior colliculus. J Neurochem.60(1):72-82.
[151]Shneiderman A, Oliver DL, Henkel CK (1988) Connections of the dorsal nucleus of the lateral lemniscus:an inhibitory parallel pathway in the ascending auditory system? J Comp Neurol.276(2):188-208.
[152]Shneiderman A, Oliver DL (1989) EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus:a possible source of inhibitory inputs to the inferior colliculus. J Comp Neurol.286:28-47.
[153]Smith PH (1992) Anatomy and physiology of multipolar cells in the rat inferior collicular cortex using the in vitro brain slice technique. J Neurosci.12:3700-3715.
[154]Stark H, Scheich H (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning:a long-term microdialysis study of metabolites. J Neurochem.68:691-697.
[155]Strominger N L (1973) The origins, course and distribution of the dorsal and intermediate acoustic striae in the rhesus monkey. J Comp Neurol.147(2):209-33.
[156]Strominger N L, Nelson LR, Dougherty WJ (1977) Second order auditory pathways in the chimpanzee. J Comp Neurol.172(2):349-65.
[157]Suga N (1997) Parallel-hierarchical processing of complex sounds for specialized auditory function. In:Encyclopedia of Acoustics, edited by Crocker MJ. New York: Wiley, pp 1409-1418.
[158]Suga N (2008) Role of corticofugal feedback in hearing.J Comp Physiol A. 194:169-183.
[159]Suga N, Ji W, Ma X, Tang J, Xiao Z, Yan J (2010) Corticofugal modulation and beyond for auditory signal processing and plasticity. In:Auditory and Vestibular Efferents, edited by Ryugo DK, Fay RR, Popper AN. Springer. Chapter 11, pp 313-352.
[160]Suga N, Xiao Z, Ma X, Ji W (2002) Plasticity and corticofugal modulation for hearing in adult animals. Neuron.36:9-18.
[161]Sumner CJ, Tucci DL, Shore SE (2005) Responses of ventral cochlear nucleus neurons to contralateral sound after conductive hearing loss. J Neurophysiol. 94:4234-4243.
[162]Sun XD, Chen QC, Jen PHS (1996) Corticofugal control of central auditory sensitivity in the big brown bat, Eptesicus fuscus. Neurosci Lett.212(2):131-4.
[163]Sun XD, Jen PHS, Sun DX, Zhang SF (1989) Corticofugal influences on the responses of bat inferiorcollicular neurons to sound stimulation. Brain Res.495:1-8.
[164]Takahashi K, Hishida R, Kubota Y, Kudoh M, Takahashi S, Shibuki K (2006) Transcranial fluorescence imaging of auditory cortical plasticity regulated by acoustic environments in mice. Eur J Neurosci.23:1365-1376.
[165]Tang J, Wu FJ, Wang D, Jen PHS, Chen QC (2007) The amplitude sensitivity of mouse inferior collicular neurons in the presence of weak noise. Chin J Physiol. 50(4):187-198.
[166]Thiel CM (2007). Pharmacological modulation of learning-induced plasticity in human auditory cortex. Restor Neurol Neurosci.25(3-4):435-443.
[167]Thiel CM, Friston KJ, Dolan RJ (2002) Cholinergic modulation of experience-dependent plasticity in human auditory cortex. Neuron.35:567-574.
[168]Tokunaga A, Sugita S, Otani K (1984) Auditory and non-auditory subcortical afferents to the inferior colliculus in the rat. JHirnforsch.25(4):461-72.
[169]Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature.420:788-794.
[170]van Noort J (1969) The anatomical basis for frequency analysis in the cochlear nuclear complex. Psychiatr Neurol Neurochir.72(1):109-14.
[171]Vater M, Habbicht H, Kossl M, Grothe B (1992) The functional role of GAB A and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol A.171(4):541-53.
[172]Virgili M, Contestabile A, Barnabei O (1991) Postnatal maturation of cholinergic markers in forebrain regions of C57BL/6 mice. Brain Res Dev. 63:281-285.
[173]Whitley JM, Henkel CK (1984) Topographical organization of the inferior collicular projection and other connections of the ventral nucleus of the lateral lemniscus in the cat. J Comp Nenrol.229(2):257-70.
[174]Wiberg M, Westman J, Blomqvist A (1987) Somatosensory projection to the mesencephalon:an anatomical study in the monkey. J Comp Neurol. 264(1):92-117.
[175]Willott JF, Westman J, Blomqvist A (1987) Somatosensory projection to the mesencephalon:an anatomical study in the monkey. J Comp Neurol.264(1):92-117.
[176]Winer JA (2006) Decoding the auditory corticofugal systems. Hear Res.212:1-8.
[177]Winer JA, Larue DT, Diehl JJ, Hefti BJ (1998) Auditory cortical projections to the cat inferior colliculus. J Comp Neurol.400:147-174.
[178]Winer JA, Larue DT, Pollak GD (1995) GAB A and glycine in the central auditory system of the mustache bat:structural substrates for inhibitory neuronal organization. J Comp Neurol.355(3):317-53.
[179]Winer JA, Schreiner CE (2005) The inferior colliculus. New york:springer-Verlag.
[180]Wu FJ, Jen PHS (2008) GABA-mediated modulation of the discharge pattern and rate-level function of two simultaneously recorded neurons in the inferior colliculus of the big brown bat, Eplesicus fuscus. Chin J Physiol.51(1):1-14.
[181]Wu FJ, Jen PHS (2009) Involvement of GABA-mediated inhibition in shaping the frequency selectivity of neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. Chin J Physiol.52(1):1-9.
[182]Wu YM, Yan J (2007) Modulation of the receptive fields of midbrain neurons elicited by thalamic electrical stimulation through corticofugal feedback. J Neurosci. 27:10651-10658.
[183]Xiong Y, Zhang Y, Yan J (2009). The neurobiology of sound-specific auditory plasticity:a core neural circuit. Neurosci Biobehav Rev.33:1178-1184.
[184]Yan J, Ehret G (2002) Corticofugal modulation of midbrain sound processing in the house mouse. Eur J Neurosci.16:119-128.
[185]Yan J, Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science.273:1100-1103.
[186]Yan J, Zhang Y, Ehret G (2005) Corticofugal shaping of frequency tuning curves in the central nucleus of the inferior colliculus of mice. J Neurophysiol.93:71-83.
[187]Yan W, Suga N (1998) Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nature Neurosci.1:54-58.
[188]Yasui Y, Nakano K, Kayahara T, Mizuno N (1991) Non-dopaminergic projections from the substantia nigra pars lateralis to the inferior colliculus in the rat. Brain Res. 559(1):139-44.
[189]Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci.4:1123-1130.
[190]Zhang YF, Suga N (1997) Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J Neurophysiol.78:3489-3492.
[191]Zhang YF, Suga N (2000) Modulation of responses and frequency tuning of thalamic and collicular neurons by cortical activation in mustached bats. J Neurophysiol.84:325-333.
[192]Zhang Y, Suga N (2005) Corticofugal feedback for collicular plasticity evoked by electric stimulation of the inferior colliculus. J Neurophysiol.94(4):2676-82.
[193]Zhang Y, Yan J (2008) Corticothalamic feedback for sound-specific plasticity of auditory thalamic neurons elicited by tones paired with basal forebrain stimulation. Cereb Cortex.18:1521-1528.
[194]Zhou J, Shore S (2004) Projections from the trigeminal nuclear complex to the cochlear nuclei:A retrograde and anterograde tracing study in the guinea pig. J Neurosci Res.78(6):901-907.
[195]Zhou XM, Jen PHS (2000a) Corticofugal inhibition compresses all types of rate-intensity functions of inferior collicular neurons in the big brown bat. Brain Res. 881:62-68.
[196]Zhou X, and Jen PH (2000b) Brief and short-term corticofugal modulation of subcortical auditory responses in the big brown bat, Eptesicus fuscus. J Neurophysiol.84:3083-3087.
[197]Zhou XM, Jen PHS (2007) Multi-parametric corticofugal modulation of sub-cortical auditory selectivity in the midbrain of bats. J Neurophysiol. 98:2509-2516.
[198]Zhou X, Merzenich MM (2008) Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex. Proc Natl Acad Sci USA. 105:4423-4428.
[199]Zhou X, Nagarajan N, Mossop BJ, Merzenich MM (2008) Influences of un-modulated acoustic inputs on functional maturation and critical-period plasticity of the primary auditory cortex. Neuroscience.154:390-396.
[200]Zook JM, Casseday JH (1982) Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii. J Comp Neurol.207(1):14-28.