摘要
躯体感觉是非听觉信号传入听觉相关核团的主要来源,这些传入信号包括本体感觉和来自躯体表面的触觉、温度觉以及痛觉。三叉神经感觉复合体和背柱核是躯体感觉系统上行传导通路中二级神经元胞体所在的部位,在接受头面部、躯干和四肢的躯体感受器的传入以及调节听觉和各种机体活动中具有重要作用。头面部的本体感觉信号和听觉信号在很多核团和脑区进行整合。目前已经确定躯体感觉信号传递至听觉系统的IC、听皮层、上橄榄复合体和蜗神经核等部位,并在这些部位进行听觉和躯体感觉的整合。
目前认为主观性耳鸣主要是由噪声或药物等损伤内耳毛细胞使其向听觉中枢的传入不平衡,引发IC等听觉中枢自发放电增加造成的。而大量的临床实践和实验研究证明,电刺激或穴位刺激躯体感受器能抑制耳鸣。所以,躯体感觉系统调节听觉系统活动,尤其是躯体感觉刺激抑制耳鸣的研究已成为热点。这些神经化学通路和生理机制的阐明对于治疗耳鸣以及耳鸣治疗方法的探索都有重大的理论意义和现实意义。
有资料显示,IC内GABA释放的减少亦会使其放电增加诱发耳鸣,而向IC内注射微量的GABA受体激动剂能显著地降低耳鸣的响度。Shore等发现电刺激三叉神经能抑制由声音诱发的IC神经元放电。因此有人推测躯体感觉传入信号通过某种神经通路增加了IC内GABA的释放,降低了IC神经元的放电,这可能是临床上刺激躯体感受器治疗耳鸣的机制之一。
在以往的研究中,重点主要放在了躯体感觉系统与听觉系统在蜗神经核和IC水平的整合关系,而对NLL与躯体感觉相互关系的研究则关注较少。NLL三个亚核内都含有GABA能神经元,且均向IC有投射,是IC内抑制传入的主要核团。电刺激DNLL能增加IC内GABA的释放,抑制由声音诱发的IC放电活动。现在认为这些抑制作用主要与声源定位有关。但是否存在Sp5、背柱核→NLL(GABA能)→IC的神经通路,经此通路将刺激躯体感受器的信号传递至NLL,进而激活NLL内向IC投射的GABA能神经元,并由此抑制IC的放电而抑制耳鸣,至今尚无详细的报道。该通路可能是躯体感觉系统影响IC神经元放电活动的重要组成部分。
有鉴于此,本文以SD大鼠为实验材料,应用神经束路追踪和免疫荧光等技术,对Sp5I和背柱核向NLL中GABA能神经元的直接投射进行了研究。实验分为三个部分:(1)Sp5I向NLL的直接定位投射研究;(2)Sp5I投射至NLL内的纤维终末与GABA能神经元之关系研究;(3)背柱核向NLL的直接定位投射研究。结果如下:
1.Sp5I向NLL的直接投射
分别将顺行追踪剂dextran-Texas Red电泳入Sp5I,逆行追踪剂FG电泳入DNLL、INLL和VNLL。观察dextran-Texas Red顺行标记纤维和终末在NLL内的分布。结果发现:①向NLL投射的神经元主要分布在较小区间内的Sp5I背侧和腹侧。②向NLL投射的纤维和终末主要分布在对侧DNLL、INLL和VNLL。③Sp5I主要向对侧下丘外侧皮质核、对侧上丘、双侧蜗神经核、对侧脑桥网状核、对侧脑桥内侧核和脑桥腹侧核等核团有投射。
2.Sp5I向NLL投射的纤维终末与GABA能神经元之关系研究
将顺行追踪剂dextran-Texas Red电泳入Sp5I,免疫荧光方法染色显示NLL内GABA能神经元。顺行标记纤维终末与GABA能神经元的重叠区域主要出现在对侧的DNLL、INLL、VNLL和下丘外侧皮质核。激光扫描共聚焦显微镜观察发现,来源于Sp5I的顺行标记纤维终末与DNLL、INLL和VNLL内的GABA能神经元有直接接触。
3.背柱核向NLL的直接投射
将顺行追踪剂dextran-Texas Red电泳入背柱核,发现顺行标记纤维和终末主要分布在对侧DNLL和VNLL,少量分布在对侧INLL。在对侧外侧丘系旁核、下丘外侧皮质核的边缘区、下橄榄核、丘间核、脑桥外侧核、脑桥内侧核和脑桥腹侧核也有顺行标记纤维和终末的分布。将逆行追踪剂FG分别电泳入DNLL、INLL和VNLL,发现逆行标记细胞主要分布在闩平面及其尾侧较小节段内的对侧薄束核和楔束核。将顺行追踪剂dextran-Texas Red电泳入背柱核,然后用免疫荧光化学反应染色显示NLL内GABA能神经元,结果未发现来源于背柱核的投射纤维终末与NLL内的GABA能神经元有接触。
这些结果提示:(1) Sp5I向NLL有直接投射,来自Sp5I的顺行标记纤维终末和NLL内的GABA能神经元有直接接触,即存在Sp5I→NLL(GABA能)→IC的神经通路;(2)背柱核向NLL有直接投射,但投射终末不与NLL内的GABA能神经元接触。这些通路的进一步确证及相应的生理功能还有待于进行超微结构和电生理学的研究。
经河北省科学技术情报研究院查新表明,本研究结果在国内外文献中尚未有相同的报道。这些成果为进一步研究刺激躯体感受器抑制耳鸣的神经机制、耳鸣形成机制以及躯体感觉信息与听觉信息在脑干听觉中枢的整合机制提供了部分形态学证据。
The somatosensory system is an important source of non-auditory inputs into various nuclei related to auditory.It coveys touch,temperature,pain from the body surface and proprioception from proprioceptive receptors of the body.The trigeminal sensory complex and the dorsal column nucleus are the sites of the secondary neurons receiving the somatosensory primary afferents from head,face,body and limbs,and regulating the acoustic activity through the efferent projections.Somatosensory and auditory signals are integrated by auditory neurons in different auditory nuclei.It has been established that somatosensory signals input to auditory neurons in the inferior colliculus(IC),auditory cortex(AC),superior olive complex(SOC) and cochlear nucleus(CN).
As recently studies supported,tinnitus arises after the damage of the inner ear hair cells by noise exposure or application of drugs.These imbalance inputs are transferred from the cochlea to auditory nucleus,and then the hyperactivity of neurons were induced in the IC or other acoustic nuclei.Clinical evidence and animal experiments demonstrated that tinnitus can be suppressed by somatosensory electrical stimulation or acupuncture point stimulation. Therefore,it has become a focus on the relationship of the somatosensory system in modulating auditory activity,especially the mechanism of tinnitus suppressed by somatosensory stimulation.These illuminations of neurochemical pathways and physiological mechanisms have important academic and practical significance which to suppress tinnitus, and to further develop treatment for tinnitus.
Several lines of evidence suggest that the increase in firing rate of neurons by reducing of GABA-release in IC induced tinnitus.The loudness of tinnitus could be markedly suppressed by microinjection of GABA receptor agonist into IC.In 2006,Jain and Shore found that electrical stimulation of the trigeminal nerve produced suppression of sound-evoked responses in IC.Thus,there is an assumption whether its somatosensory inputs increased GABA-release within IC by certain neural pathway,and the discharge of neurons will be inhibited in the IC.It may be one of the mechanisms underlying of alleviation for tinnitus by somatosensory stimulation.
Up to now,numerous physiological and anatomical studies have been conducted on the integration between somatosensory and auditory in the level of CN and IC.However,it still remains unclear that what is the relationship between the somatosensory and auditory in the level of nucleus of the lateral lemniscus(NLL).Immunocytochemical studies have shown that three subnucleus of the lateral lemniscus contain GABAergic neurons,respectively.In addition,a GABAergic projection to the IC from the NLL has been confirmed,which is known to be a major source of inhibitory inputs to the IC.Previous studies have demonstrated that the effects of electrical stimulation within the DNLL can increase GABA-release in IC, and change the discharge characteristics of IC neuron.It is considered that the roles of inhibitory inputs were related to shaping binaural and monaural responses,and to pursuing sound source.It is unknown;however,whether there are neural pathways from Sp5,dorsal column nucleus to IC relayed by GABAergic neurons in NLL,by which conveyed the somatosensory signal to NLL and the GABAergic neurons projected to the IC were activated. The neural pathway may play an important role in effects of somatosensory signals on the discharge of IC neuron.
Based on those,the following experiments were processed by using anterograde and retrograde neural tracing technique,combined with immunofluorescence in Sprague-Dawley rat.The direct projection from Sp5I and dorsal column nucleus to GABAergic neurons in NLL was studied in the following experiments.Those included three parts:(1) whether there were the direct projections from the Sp5I to the NLL;(2) whether there were the terminal endings from the Sp5I making contacts with GABAergic neurons in NLL;(3) whether there were direct projections from the dorsal column nucleus to the NLL.The results were as followed:
1.The direct projection from the Sp5I to the NLL
With the respective injection of anterograde trace dextran-Texas Red into the Sp5I and retrograde tracer FG into DNLL,1NLL and VNLL,the distribution of dextran-Texas Red-labeled fibers and terminals were observed in the NLL,and the FG-labeled neurons were observed in the Sp5I.The following were the results:①The FG-labeled neurons were located in dorsal,ventral and ventrolateral of contralateral the Sp5I.②The fibers and terminals of the Sp5I-NLL projection were located in the DNLL,INLL and VNLL.③The anterogradely labeled fibers and terminals were observed in contralaterally external cortex of the inferior colliculus,superior colliculus,pontine reticular nucleus,lateral pontine nucleus,medial pontine nucleus and bilateral CN.
2.Relationship between fibers projected from the Sp5I and GABAergic neurons in the NLL
After anterograde tracer dextran-Texas Red was injected into the Sp5I,and then frozen sections of rat's brainstem were immunostained by fluorescence with glutamic acid decarboxylase(GAD) antibody to reveal the GABAergic neurons in the NLL.The overlap distribution of anterograde labeled fibers and terminals with GABAergic neurons were found in the contralaterally DNLL,INLL,VNLL and external cortex of the inferior colliculus.The direct contacts between the dextran-Texas Red-labeled Sp5I terminal endings and GABAergic neurons in the DNLL,INLL and VNLL were found under the laser scanning confocal microscope(LSCM).
3.The direct projection from the dorsal column nucleus to the NLL
Following dextran-Texas Red was injected into the dorsal column nucleus,the anterograde labeled fibers and terminals were seen in contralaterally DNLL,INLL and VNLL. Moderate terminals were observed in paralemniscal nucleus,lateral border region of the IC, inferior olive,intercollicular nucleus,lateral pontine nucleus and ventral pontine nucleus. After FG was injected into the DNLL,INLL and VNLL,the FG-retrograde labeled neurons were found in contralateral gracile nucleus and cuneate nucleus.After anterograde trace dextran-Texas Red was injected into the dorsal column nucleus,and the GABAergic neurons were visualized by immunofluorescence,the direct contacts between the anterograde terminals and GABAergic neurons were not observed by LSCM.
The above results show that:(1) There were direct projections from the Sp5I and the dorsal column nucleus to the NLL;and the terminal endings from the Sp5I made contacts with GABAergic neurons within the DNLL,INLL and VNLL,the possible neural pathway was Sp5→NLL(GABAergic)→IC.(2) The dorsal column nucleus was found to project directly to the NLL;and there was not any contact between terminal from the Sp5I and GABAergic neuron in the NLL.To confirm this possible pathway and physiological function, further researches are still needed by electrophysiology and immunoelectron microscopy.
The results of present study were not the same report in the world ground on the indagator of Hebei Science and Technology Information Institute recently.The results provided morphological foundation for investigating the integrated mechanism of somatosensory with auditory in auditory nuclei and modulation mechanism of suppressing tinnitus by somatosensory stimulation in future.
引文
[1]Levine RA,Abel M,Cheng H.CNS somatosensory-auditory interactions elicit or modulate tinnitus[J].Exp Brain Res,2003,Dec;153(4):643-8.
[2]Cacace AT.Expanding the biological basis of tinnitus:crossmodal origins and the role of neuroplasticity[J].Hear Res,2003,Jan;175(1-2):112-32.
[3]Zhou J,Shore S.Projections from the trigeminal nuclear complex to the cochlear nuclei:a retrograde and anterograde tracing study in the guinea pig[J].J Neurosci Res,2004,78(6):901-907.
[4]Zhou J,Shore S.Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig[J].J Comp Neurol,2006,495(1):100-112.
[5]Eggermont JJ.Tinnitus:neurobiological substrates[J].Drug Discov Today,2005,Oct 1;10(19):1283-90.
[6]Zhang J,Guan Z.Modulatory effects of somatosensory electrical stimulation on neural activity of the dorsal cochlear nucleus of hamsters[J].J Neurosci Res,2008,Apr;86(5):1178-87.
[7]Zhang J,Guan Z.Pathways involved in somatosensory electrical modulation of dorsal cochlear nucleus activity[J].Brain Res,2007,1184:121-31.
[8]Engelberg M,Bauer W.Transcutaneous electrical stimulation for tinnitus[J].Laryngoscope,1985,95(10):1167-73.
[9]Phillips JS,Baguley DM,Patel H,Moffat DA.Tinnitus evoked by cutaneous stimulation [J].Neurology,2004,Nov 9;63(9):1756.
[10]万文蓉.古籍文献针灸治疗耳鸣处方特点探析[J].江西中医学报,2003,15(12):38-41.
[11]邱德明,李少芬,李少敏.创研激光经络穴位疗法治疗耳鸣症[J].医学研究杂志,2006,35(8):41-43.
[12]邱德明,李少芬.激光经络穴位疗法康复治疗噪声性耳鸣症[J].医学研究通讯,2005,34(1):75-76.
[13]Cacace AT,Cousins JP,Parnes SM,et al.Cutaneous-evoked tinnitus.I.Phenomenology,psychophysics and functional imaging[J].Audiol Neurootol,1999,4(5):247-257.
[14]Zhang JS,Kaltenbach JA.Increases in spontaneous activity in the dorsal cochlear nucleus of the rat following exposure to high-intensity sound[J].Neurosci Lett,1998,250(3):197-200.
[15]Ma WL,Hidaka H,May BJ.Spontaneous activity in the inferior colliculus of CBA/J mice after manipulations that induce tinnitus[J].Hear Res,2006,212(1-2):9-21.
[16]Brozoski TJ,Ciobanu L,Bauer CA.Central neural activity in rats with tinnitus evaluated with manganese-enhanced magnetic resonance imaging (MEMRI)[J].Hear Res,2007,228(1-2):168-179.
[17]Smits M,Kovacs S,de Ridder D,et al.Lateralization of functional magnetic resonance imaging (fMRI) activation in the auditory pathway of patients with lateralized tinnitus[J].Neuroradiology,2007,49(8):669-679.
[18]Paul AK,Lobarinas E,Simmons R,et al.Metabolic imaging of rat brain during pharmacologically-induced tinnitus[J].Neuroimage,2009,Jan 15;44(2):312-318.
[19]Bahmad FM Jr,Venosa AR,Oliveira CA.Benzodiazepines and GABAergics in treating severe disabling tinnitus of predominantly cochlear origin[J].Int Tinnitus J,2006,12(2):140-144.
[20]Wang HT,Luo B,Huang YN,et al.Sodium salicylate suppresses serotonin-induced enhancement of GABAergic spontaneous inhibitory postsynaptic currents in rat inferior colliculus in vitro[J].Hear Res,2008,236(1-2):42-51.
[21]Brozoski TJ,Spires TJ,Bauer CA.Vigabatrin,a GABA transaminase inhibitor,reversibly eliminates tinnitus in an animal model[J].J Assoc Res Otolaryngol,2007,8(1):105-118.
[22]Moore JK,Moore RY.Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat[J].J.Comp.Neurol,1987,260(2):157-174.
[23]Winer JA,Larue DT,Pollak GD.GABA and glycine in the central auditory system of the mustache bat:structural substrates for inhibitory neuronal organization[J].J Comp Neurol,1995,355(3):317-353.
[24]Adams JC,Mugnaini E.Dorsal nucleus of the lateral lemniscus:a nucleus of GABAergic projection neurons[J].Brain Res Bull,1984,13(4):585-590.
[25]Thompson GC,Cortez AM,Lam DM.Localization of GAB A immunoreactivity in the auditory brainstem of guinea pigs[J].Brain Res,1985,339(1):119-122.
[26]Zhang D,Li L,Kelly B,et al.GABAergic projections from the lateral lemniscus to the inferior colliculus of therat[J].Hear Res,1998,117(1-2):1-12.
[27]Covey E.Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat[J].J Neurophysiol,1993,69(3):842-59.
[28]Kelly JB,Li L.Two sources of inhibition affecting binaural evoked responses in the rat's inferior colliculus:the dorsal nucleus of the lateral lemniscus and the superior olivary complex[J].Hear Res,1997,Feb;104(1-2):112-26.
[29]De la Mothe LA,Blumell S,Kajikawa Y,and Hackett TA.Cortical connections of the auditory cortex in marmoset monkeys:Core and medial belt regions[J].Journal of Comparative Neurology,2006,496(1):27-71.
[30]S.E.Shore.Auditory/Somatosensory Interactions.Encyclopedia of Neuroscience,2009,pp:691-699.
[31]Meredith MA,Keniston LR,Dehner LR,Clemo HR.Crossmodal projections from somatosensory area SIV to the auditory field of the anterior ectosylvian sulcus (FAES) in cat:further evidence for subthreshold forms of multisensory processing[J].Experimental Brain Research,2006,172(4):472^184.
[32]朱长庚.神经解剖学[M].北京:人民卫生出版社,2002:544.
[33]Li H,Mizuno N.Single neurons in the spinal trigeminal and dorsal column nuclei project to both the cochlear nucleus and the inferior colliculus by way of axon collaterals:a fluorescent retrograde double-labeling study in the rat[J].Neurosci Res,1997,29(2):135-142.
[34]Romfh JH,Capra NF,Gatipon GB.Trigeminal nerve and temporomandibular joint of the cat:a horseradish peroxidase study[J].Exp Neurol,1979,65(1):99—106.
[35]Jacquin MF,Barcia M,Rhoades RW.Structure-function relationships in rat brainstem subnucleus interpolaris:IV Projection neurons[J].J Comp Neurol,1989,282(l):45-62.
[36]Nazruddin,Suemune S,Shirana Y,Yamauchi K,Shigenaga Y.The cells of origin of the hypoglossal afferent nerves and central projections in the cat[J].Brain Res,1989,490(2):219-235.
[37]Takemura M,Sugimoto T,Shigenaga Y.Difference in central projection of primary afferents innervating facial and intraoral structures in the rat[J].Exp Neurol,1991,111(3):324-331.
[38]Suemune S,Nishimori T,Hosoi M,Suzuki Y,Tsuru H,Kawata T,Yamauchi K,Maeda N. Trigeminal nerve endings of lingual mucosa and musculature of the rat[J].Brain Res,1992,586(1):162-165.
[39]Shore SE.Multisensory integration in the dorsal cochlear nucleus:unit responses to acoustic and trigeminal ganglion stimulation[J].Eur J Neurosci,2005,21(12):3334-3348.
[40]Jain R,Shore S.External inferior colliculus integrates trigeminal and acoustic information:unit responses to trigeminal nucleus and acoustic stimulation in the guinea pig[J].Neurosci Lett,2006,395(l):71-75.
[41]Tammer R,Ehrenreich L,Jurgens U.Telemetrically recorded neuronal activity in the inferior colliculus and bordering tegmentum during vocal communication in squirrel monkeys (Saimiri sciureus)[J].Behavioural Brain Research,2004,151:331-336.
[42]Shore SE,Vass Z,Wys NL,Altschuler RA.Trigeminal ganglion innervates the auditory brainstem[J].J Comp Neurol,2000,419(3):271-285.
[43]Pfaller K,Arvidsson J.Central distribution of trigeminal and upper cervical primary afferents in the rat studied by anterograde transport of horseradish peroxidase conjugated to wheat germ agglutinin[J].J Comp Neurol,1988,268(1):91-108.
[44]Zhan X,Pongstaporn T,Ryugo DK.Projections of the second cervical dorsal root ganglion to the cochlear nucleus in rats[J].J Comp Neurol,2006,496(3):335-348.
[45]Haenggeli CA,Pongstaporn T,Doucet JR,Ryugo DK.Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat[J].J Comp Neurol,2005,484(2):191-205.
[46]Itoh K,Kamiya H,Mitani A,Yasui Y,Takada M,Mizuno N.Direct projections from the dorsal column nuclei and the spinal trigeminal nuclei to the cochlear nuclei in the cat[J].Brain Res,1987,400:145-150.
[47]Weinberg RJ,Rustioni A.A cuneocochlear pathway in the rat[J].Neuroscience,1987,20(1):209-219.
[48]Wright DD,Ryugo DK.Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat[J].J Comp Neurol,1996,365(1):159-172.
[49]Wolff A,Kunzle H.Cortical and medullary somatosensory projections to the in the hedgehog tenrec[J].Neurosci Lett,1997,221(2-3):125-128.
[50]Ohlrogge M,Doucet JR,Ryugo DK.Projections of the pontine nuclei to the cochlear nucleus in rats[J].J Comp Neurol,2001,Jul 30;436(3):290-303
[51]Burian M,Gstoettner W,Zundritsch R.Saccular afferent fibers to the cochlear nucleus in the guinea pig[J].Archives of Otorhinolaryngology,1989,246(5):238-241.
[52]Gstoettner W,Burian M,Zundritsch R,Mayr R.The origin of the vestibulo-cochlear projection in the guinea pig[J].Neurosci Lett,1991,122(2):163-166.
[53]Kevetter GA,Perachio AA.Projections from the sacculus to the cochlear nuclei in the mongolian gerbil[J].Brain Behav Evol,1989,34(4):193-200.
[54]Hermann GE,Holmes GM,Rogers RC,Beattie MS,Bresnahan JC.Descending spinal projections from the rostral gigantocellular reticular nuclei complex[J].J Comp Neurol,2003,Jan6;455(2):210-21.
[55]Van Bockstaele EJ,Pieribone VA,Aston-Jones G.Diverse afferents converge on the nucleus paragigantocellularis in the rat ventrolateral medulla:retrograde and anterograde tracing studies[J].J Comp Neurol,1989,Dec 22;290(4):561-584.
[56]Zhan X,Ryugo DK.Projections of the lateral reticular nucleus to the cochlear nucleus in rats[J].J Comp Neurol,2007,Oct 10;504(5):583-598.
[57]Weedman D,Ryugo D.Projections from auditory cortex to the cochlear nucleus in rats:synapses on granule cell dendrites[J].J Comp Neurol,1996,371(2):311—324.
[58]Shore S,El Kashlan H,Lu J.Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons[J].Neuroscience,2003,119(4):1085-1101.
[59]Kanold PO,Young ED.Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus[J].J Neurosci,2001,21(19):7848-7858.
[60]Saade NE,Frangieh AS,Atweh SF,Jabbur SJ.Dorsal column input to cochlear neurons in decerebrate decerebellate cats[J].Brain Res,1989,486(2):399-402.
[61]Zhou J,Nannapaneni N,Shore S.Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus[J].J Comp Neurol,2007,500(4):777-787.
[62]Schofield BR,Cant NB.Ventral nucleus of the lateral lemniscus in guinea pigs:cytoarchitecture and inputs from the cochlear nucleus[J].J.Comp.Neurol,1997, 379(3):363-385.
[63]Zook JM,Casseday JH.Origin of ascending projections to the inferior collculus in the mustache bat,Pteronotus parnellii[J].J Comp Neurol,1982,207(1):14-28.
[64]Covey E,Casseday JH.The monaural nuclei of the lateral lemniscus in an echolocating bat:parallel pathways for analyzing temporal features of sound[J].J Neurosci,1991,ll(ll):3456-3470.
[65]Vater M,Covey E,Casseday JH.The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus) synaptic arrangements and structural correlates of feedforward inhibitory function[J].Cell Tissue Res,1997,289:223-233.
[66]Glendenning KK,Brunso-Bechtold JK,Thompson GC,Masterton RB.Ascending auditory afferents to the nuclei of the lateral lemniscus[J].J Comp Neurol,1981,232:673-703.
[67]Labelle RE.Kelly JB.A retrograde transport study of the ascending projections to the dorsal nucleus of the lateral lemniscus in the albino rat[J].Assoc Res Otolaryngol,1996,Abstr,19:121.
[68]Huffman RF,Covey E.Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat,Eptesicus fuscus[J].J Comp Neurol,1995,357:532-545.
[69]Yang L,Liu Q,Pollak GD.Afferent connections to the dorsal nucleus of the lateral lemniscus of the mustache bat:evidence for two functional subdivisions[J].J Comp Neurol,1996,373:575-592.
[70]Shneiderman A,Oliver DL,Henkel C.Connections of the dorsal nucleus of the lateral lemniscus:an inhibitory parallel pathway in the ascending auditory system[J].J Comp Neurol,1988,276:188-208.
[71]Labelle RE.The connectivity and ultrastructure of the dorsal nucleus of the lateral lemniscus of the albino rat[D].Ottawa,Canada:Carleton University,1997.
[72]Merchan MA,Saldafia E,Plaza I.Dorsal nucleus of the lateral lemniscus in the rat:concentric organization and tonotopic projection to the inferior colliculus[J].J Comp Neurol,1994,342(2):259-278.
[73]Saint Marie RL,Luo L,Ryan AF.Spatial representation of frequency in the rat dorsal nucleus of the latetal lemniscus as revealed by acoustically induced c-fos mRNA expression[J].Hear Res,1999,Feb;128(l-2):70-74.
[74]Elverland HH.Ascending and intrinsic projections of the superior olivary complex in the cat[J].Exp Brain Res,1978,32(1):117-134.
[75]Glendenning KK,Masterton RB.Acoustic chiasm:efferent projections of the lateral superior olive[J].J Neurosci,1983,3(8):1521-1537.
[76]Hutson KA,Glendenning KK.Masterton RB.Acoustic chiasm IV:eight midbrain decussations of the auditory system in the cat[J].J Comp Neurol,1991,312(1):105-131.
[77]Vater M,Casseday JH,Covey E.Convergence and divergence of ascending binaural and monaural pathways from the superior olives of the mustached bat[J].J Comp Neurol,1995,351(4):632-646.
[78]Kelly JB,van Adel BA,lto M.Anatomical projections of the nuclei of the lateral lemniscus in the albino rat(Rattus norvegicus)[J].J Comp Neurol,2009,Feb 1;512(4):573-593.
[79]Henkel CK,Spangler KM.Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods[J].J Comp Neurol,1983,221(4):416-428.
[80]Bajo VM,Merchan MA,Lopez DE,Rouiller EM.Neuronal morphology and efferent projections of the dorsal nucleus of the lateral lemniscus in the rat[J].J Comp Neurol,1993,334(2):241-262.
[81]Glendenning KK,Baker BN.Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat[J].J Comp Neurol,1988,Sep;275(2):288-308.
[82]Godfrey DA,Parli JA,Dunn JD,Ross CD.Neurotransmitter microchemistry of the cochlear nucleus and superior olivary complex[M].Auditory Pathway,1988,107-121.
[83]Oliver DL,Bishop DC.Different proportions of GABA and glycine content distinguish the nuclei of the lateral lemniscus in the rat.A double-label immunouorescence study[J].Assoc Res Otolaryngol,1998,Abstr,21:93.
[84]Riquelme R,Merchan MA,Ottersen OP.GABA and glycine in the ventral nucleus of the lateral lemniscus:an immunocytochemical and in situ hybridization study in rat[J].Assoc Res Otolaryngol,1998,Abstr,21:93.
[85]Kelly JB,Buckthought AD,Kidd SA.Monaural and binaural properties of single neurons in the rat's dorsal nucleus of the lateral lemniscus[J].Hear Res,1998,122(l-2):25-40.
[86]Ito M,Kudo M,Kelly JB.Plasticity in the auditory brainstem after unilateral ablation of the inferior colliculus in the neonatal albino rat[J].World Congress Neurosci,1995,Abstr,4:197.
[87]OHver DL,Shneiderman A.An EM study of the dorsal nucleus of the lateral lemniscus:inhibitory,commissural synaptic connections between ascending auditory pathway[J].J Neurosci,1989,9(3):967-982.
[88]Brugge JF,Anderson DJ,Aitkin LM.Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal stimulation[J].J Neurophysiol,1970,33(3):441-458.
[89]Bajo VM,Villa AE,de Ribaupierre F,Rouiller EM.Discharge properties of single neurons in the dorsal nucleus of the lateral lemniscus of the rat[J].Brain Res Bull,1998,Dec;47(6):595-610.
[90]Burger RM,Pollak GD.Reversible inactivation of the dorsal nucleus of the lateral lemniscus reveals its role in the processing of multiple sound sources in the inferior colliculus of bats[J].J Neurosci,2001,Jul 1;21(13):4830-4843.
[91]Yang L,Pollak GD.Features of ipsilaterally evoked inhibition in the dorsal nucleus of the lateral lemniscus[J].Hear Res,1998,Aug;122(1-2):125-141.
[92]Zook JM,Casseday JH.Projections from the cochlear nuclei in the mustache bat,Pteronotus parnellii[J].J.Comp.Neurol,1985,237(3):307-324.
[93]Adams JC.Projections from octopus cells of the posteroventral cochlear nucleus to the ventral nucleus of the lateral lemniscus in cat and human[J].Aud Neurosci,1997,3:335-350.
[94]Schofield BR,Cant NB.Ventral nucleus of the lateral lemniscus in guinea pigs:cytoarchitecture and inputs from the cochlear nucleus[J].J Comp Neurol,1997,379(3):363-385.
[95]Warr WB,Beck JE.Multiple projections from the ventral nucleus of the trapezoid body in therat[J].Hear Res,1996,93(1-2):83-101.
[96]Helfert RH,Aschoff A.Superior olivary complex and nuclei of the lateral lemniscus[M].In:The Central Auditory System,New York,Oxford,1997,pp:193-258.
[97]Brunso-Bechtold JK,Thompson GC,Masterton RB.HRP study of the organization of auditory afferents ascending to the central nucleus of the inferior colliculus[J].J Comp Neurol,1981,197(4):705-722.
[98]Saint Marie RL,Baker RA.Neurotransmitter-specific uptake and retrograde transport of[~3H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus[J].Brain Res,1990,524(2):244-253.
[99]Coleman JR,Clerici WJ.Sources of projections to subdivisions of the inferior colliculus in the rat[J].J Comp Neurol,1987,262(2):215-226.
[100]Benson CG,Cant NB.The ventral nucleus of the lateral lemniscus of the gerbil (Meriones unguiculatus):organization of connections with the cochlear nucleus and the inferior colliculus[J].J Comp Neurol,2008,Oct 20;510(6):673-690.
[101]Merchan MA,Berbel P.Anatomy of the ventral nucleus of the lateral lemniscus in rats:a nucleus with a concentric laminar organization J].J Comp Neurol,1996,372(2):245-263.
[102]Portfors CV,Wenstrup JJ.Delay-tuned neurons in the inferior colliculus of the mustached bat:implications for analyses of target distance[J].J Neurophysiol,1999,82(3):1326-1338.
[103]Portfors CV,Felix RA 2nd.Specteal integration in the inferior colliculus of the CBA/CaJ Mouse[J].Neuroscience,2005,136(4):1159-1170.
[104]Portfors CV,Wenstrup JJ.Responses to combinations of tones in the nuclei of the lateral lemniscus[J].J Assoc Res Otolaryngol,2001,Jun;2(2):104-117.
[105]Portfors CV,Wenstrup JJ.Excitatory and facilitatory frequency response areas in the inferior colliculus of the superior paraolivary nucleus in guinea pigs[J].J Comp Neurol,2002,360:135-149.
[106]Nataraj K,Wenstrup JJ.Roles of inhibition in creating complex auditory responses in the inferior colliculus:facilitated combination-sensitive neurons[J].J Neurophysiol,2005,Jun;93(6):3294-3312.
[107]Casseday JH,Fremouw T,Covey E.The Inferior Colliculus:A Hub for the Central Auditory System[M].In:Integrative Functions in the Mammalian Auditory Pathway,Springer, 2002,pp:238-318.
[108]Faingold CL,Anderson CA,Randall ME.Stimulation or blockade of the dorsal nucleus of the lateral lemniscus alters binaural and tonic inhibition in contralateral inferior colliculus neurons[J].Hear Res,1993,Sep;69(1-2):98-106.
[109]Herraiz C,Toledano A,Diges I.Trans-electrical nerve stimulation(TENS) for somatic tinnitus[J].Prog Brain Res,2007,166:389-394.
[110]Lenhardt ML,Goldstein BA,Shulman A,et al.Use of high-frequency and muscle vibration in the treatment of tinnitus[J].Int Tinnitus J,2003,9(1):32-36.
[111]Okada DM,Onishi ET,Chami FI,et al.Acupuncture for tinnitus immediate relief[J].Braz J Otorhinolaryngol,2006,72(2):182-186.
[112]Rubinstein B,Axelsson A,Carlsson GE.Prevalence of signs and symptoms of craniomandibular disorders in tinnitus patients[J].J Craniomandib Disord,1990,4(3):186-192.
[113]Pinchoff RJ,Burkard RF,Salvi RJ,Coad ML,Lockwood AH.Modulation of tirmitus by voluntary jaw movements[J].Am J Otol,1998,19(6):785-789.
[114]Di(?)o MR,Mugnaini E.Distribution and phenotypes of unipolar brush cells in relation to the granule cell system of the rat cochlear nucleus[J].Neuroscience,2008,154(1):29-50.
[115]Aitkin LM,Kenyon CE,Philpott P.The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus[J].J Comp Neurol,1981,196:25-40.
[116]张培林,胡梦娟,杜富等.猫内脏大神经一级传入纤维在脊髓灰质和薄束核中的分布[J].解剖学报,1987,18(2):132-140.
[117]Mari(?)o J,Martinez L,Canedo A..Sensorimotor Integration at the Dorsal Column Nuclei[J].News Physiol Sci,1999,14:231-237.
[118]Shore S,Zhou J,Koehler S.Neural mechanisms underlying somatic tinnitus[J].Prog Brain Res,2007,166:107-123.
[119]刘峰.针刺治疗老年性耳鸣[J].中国针灸,2001,21(10):613.
[120]姿艾琳,左和鸣,安林等.用脑葡萄糖图技术研究纳洛酮对电针足三里穴传入信息的传递及其抑制胃牵拉反应的影响[J].针刺研究,1997,3:229-234.
[121]Siemen M,K(u|¨)nzle H.Afferent and efferent connections of the dorsal column nuclear complex and adjacent regions in the turtle[J].J Hirnforsch,1994,35(1):79-102.
[122]Maslany S,Crockett DP,Egger MD.Somatotopic organization of the dorsal column nuclei in the rat:transganglionic labelling with B-HRP and WGA-HRP[J].Brain Res,1991,564(l):56-65.
[123]Hannig S,Jixrgens U.Projections of the ventrolateral pontine vocalization area in the squirrel monkey[J].Exp Brain Res,2006,169(1):92-105.