大鼠三叉神经节神经元向三叉神经脊束核尾侧亚核和孤束核的分支投射
作者：张文斌 熊抗辉 王百忍 李惠民 李继硕
单位：第四军医大学解剖学教研室，梁銶琚脑研究中心，西安 710032
关键词：三叉神经节；三叉神经脊束核尾侧亚核；孤束核；荧光素；逆行追踪；分支投射；大鼠
解剖学报980305 摘 要 为研究三叉神经节神经元向三叉神经脊束核尾侧亚核(VC)和孤束核(NTS)的分支投射，用荧光素逆行追踪双标记方法，Fast blue(FB)和Nuclear yellow(NY)分别注射入三叉神经脊束核尾侧亚核和孤束核后，荧光显微镜(360nm激发波长)下可见三叉神经节内的多种逆行标记神经元。FB显示明亮的蓝色标记胞浆，而NY标记则为黄绿色的圆形胞核。虽大多数神经元为单标记，但部分也呈黄色胞核，蓝色胞浆的双标记细胞。双标记细胞多为直径30μm以下的中、小型，鲜见大型细胞。分支投射神经元可能扩散传递口、舌伤害性痛觉信息并在VC和NTS内与其他来源的内脏、躯体感觉传入信息相互影响。
, 百拇医药
三叉神经脊束核(spinal trigeminal nucleus,VSP)和孤束核(nucleus of the solitary tract,NTS)作为感觉中继站核，分别接受经三叉神经和舌咽、迷走等神经传入的头面部和内脏感觉信息。以往的研究证明，众多的三叉神经周围支中，只有舌、下牙槽及蝶腭等神经支的初级传入终末除投射入VSP外，部分终末支亦投射入NTS[1~3]。形态学的研究还证明，三叉神经感觉根一些传入纤维至中枢内的上升和下降支分支投射入感觉主核和脊束核[4]以及VSP的极间亚核和尾侧亚核[5]。但目前尚无向VSP和NTS的纤维投射起源于三叉神经节(trigeminal ganglion,VG)内相同神经元的研究报道。本实验以荧光素逆行追踪双标记的方法对VG内神经元向NTS和三叉神经脊束核分支投射进行了研究。
材料和方法
实验用SD雄性大鼠17只，体重200～280g,13例动物在腹腔内注射戊巴比妥钠(4mg/100g体重)麻醉下，手术暴露三叉神经脊束核的尾侧亚核(caudal subnucleus of spinal trigeminal nucleus,VC),用微量注射器(1μl)将2%快蓝(fast blue,FB,Sigma)水溶液缓慢注射入VC中段，成活2～3d后，再注射2%核黄(nuclear yellow,NY,Sigma)水溶液注射入同侧闩吻侧2～3mm平面的NTS，动物再成活15～20h。另4例动物变换荧光素的注射部位，即FB注入NTS而NY注入VC。深麻醉下经心脏先快速灌入50ml的生理盐水冲洗，继以含4%多聚甲醛的磷酸缓冲液(0.1mol/L,pH7.4)灌流固定。灌毕立即取脑和VG置入30%蔗糖磷缓液内过夜(4℃)。分别做脑和VG厚40μm和20μm的冰冻切片，即刻蒸馏水裱片，空气干燥。在配备A滤光片的荧光显微镜(Olympus BH2)下选择注射区准确且局限的材料，重点观察其VG内的逆行荧光标记神经元。
, 百拇医药
结 果
用360nm激发波长A滤光片，在荧光显微镜下可见两种荧光素表现不同的标记特征，FB显示明亮的蓝色胞浆，浅淡标记者依稀可辨缺损的中央核区。而NY标记则为黄绿色的圆形胞核(图A、B)。VC内注射FB后，整个VG内神经元常被大量标记。VG内标记神经元的数量和位置亦随注射中心区位移而略有变化。即注射中心区局限于VC背部者，其标记细胞主要位于VG的下颌神经区。相反，如标记中心区局限于VC腹部者，标记细胞主要位于眼和上颌神经区。标记细胞的形态、大小各不相同，一般大、中型细胞多呈圆形或椭圆形，小型者除圆形或椭圆形外，亦见不规则形或三角形。NY注射区范围局限于NTS内的材料主要在VG的下颌神经和上颌神经区域内见到黄绿色的标记胞核，这些黄绿色圆形胞核散布于蓝色胞浆的神经元之间，其数量后者多于前者。FB和NY逆行标记神经元均仅见于注射同侧的VG。虽大多数神经元为单标记，但也有部分呈黄色胞核，蓝色胞浆的双标记细胞(图A、B)。在NY胞核标记的细胞中约有21.3%也被FB标记而呈现双标记。因为FB标记的细胞数量远多于NY标记者，所以，仅较少比例的FB标记细胞显示双标记。值得注意的是，双标记细胞大多为直径30μm以下的中、小型，鲜见大型细胞(图A)。调换FB和NY的注射部位，即前者注射于NTS，后者注射于VC，在VG内的标记形式大体上与上述一致。
, 百拇医药
讨 论
运用神经元轴浆运输的逆行标记物、特别是联合配对使用荧光素常用来研究神经元的分支投射[6]。由于荧光素在中枢神经组织内容易扩散，所以，将其局限于中枢特定部位是准确分析结果的基础。在延髓特别是其尾段，同侧的NTS和VC相距较近，如FB或NY注射区涉及二核，势必造成VG内细胞双标记的假象。本实验用小剂量、缓慢注射，尽量缩小注射区范围，使之局限于靶核区内。同时，经背侧进针穿过脊束的FB注射区位于闩以下VC段，这样既避免累及主要投射入闩以上NTS 的舌神经和蝶腭神经在脊束内下行轴突支。而且位于闩以下VC段FB注射区同闩以上2～3mm平面NTS注射区呈吻尾关系，又可进一步避免两种荧光素注射区之间的相互影响。镜下观察首先摒弃注射中心区扩及邻近结构或脱离靶区的动物例，其次，选择NTS注射例的标记细胞只局限于VC内上颌和下颌神经区的材料(三叉神经领域内的眼神经无纤维投射入NTS)。这样就保证了实验结果的客观和可靠性。
三叉神经节内神经元中枢突有分支投射到三叉神经感觉核簇的吻、尾诸核[4,5]。本实验结果证明，三叉神经节内一些细胞还分支投射入VC和三叉神经感觉核以外的NTS，且投射至后者的VG节细胞约有21.3%是属于分支投射细胞。除周围神经初级传入外，在中枢神经内普遍存在神经元分支投射的现象[7～9]。与非分支投射神经元相比，分支投射神经元被认为在传递同样信息时，可对其靶结构产生更广泛、更有效的影响[7，9]。SP是传递伤害性信息的神经活性物质[10]。SP、CGRP等多肽类神经递质单独或者共存于三叉神经节细胞内，特别是节内中、小型细胞多含SP，且它们直接投射入VC和NTS[11～13]。因为以往其他学者以及我们的研究结果均证明，闩以上2～3mm平面的NTS内侧亚核区主要接受舌神经和蝶腭神经初级传入终末的浓密投射[1，3]。本实验结果提示，VG内的双标记细胞可能代表周围突组成舌神经和蝶腭神经且主要支配口、舌和鼻粘膜的感觉神经元，其中枢突既向VC又向NTS投射。舌神经和蝶腭等神经传递口、舌和鼻粘膜区域感觉信息，包括伤害性刺激传入信息，经VG内中、小型神经元分支的中枢突扩散投射并广泛影响中枢内感觉中继核团。NTS和VC分别接受内脏和三叉神经初级传入终末，同时NTS和VC两者还存在双向纤维联系[14，15]。经分支投射神经元扩散传递的口、舌伤害性信息也可能在VC和NTS内，与其他来源的内脏、躯体多种感觉传入信息相互影响，产生复杂的抑制或易化的调节、整合作用。其对伤害性传入信息的调控及功能意义还有待进一步深入研究。
, 百拇医药
收稿1997-07 修回1997-12
图版说明
图A、B分别注射Fast blue(FB)和Nuclear yellow(NY)入三叉神经脊束核尾侧亚核(VC)和孤束核后三叉神经节内的逆行标记细胞。有3种类型的标记细胞，即NY单标记胞核(三角)、FB单标记胞浆(空心箭头)和FB+NY双标记神经元(实心白色箭头)。双标记神经元多为中、小型。图A中央左侧可见一小型的双标记神经元。图B左下方可见一较大型的FB单标记神经元。标尺示80μm，两图的放大倍数相同。
Explanation of figuers
Photomicrographs of retrogradely labeled neurons in the trigeminal ganglion after Fast blue(FB)and Nuclear yellow (NY) injecting into the caudal subnucleus of spinal trigeminal nucleus(VC)and the nucleus of the solitary tract,respectively.There are three kinds of labeled neurons:single-labeled nucleus of neurons with NY(triangles),single-labeled cytoplasm of neurons with FB(hollow arrows)and double-labeled neurons(solid white arrows).Most double-labeled neurons are small and medium in size.There is a samll sized double-labeled neuron in the central left side of Fig.A. A large sized FB single-labeled neuron is found in the left lower side of Fig.B. Bar=80μm in Fig.A,the magnification of Fig.B is the same as Fig.A.
, http://www.100md.com
参考文献
[1]Nomura S,Yukhik Y,Takada M,et al.Trigeminal primary afferent neurons projecting directly to the solitary nucleus in the cat:a transganglionic and retrograde horseradish proxidase study.Neurosci Lett,1984,50(2):257
[2]Whitehead MC,and Frank ME.Anatomy of the gustatory system in the hamster:central projections of the chorda tympani and the lingual nerve.J Comp Neural,1983,220(3):378
[3]张文斌，李惠民，李继硕.三叉神经初级传入纤维与孤束核的联系——HRP跨越神经节追踪研究.神经解剖学杂志，1990，6(1)：97
, 百拇医药
[4]Li Y O,Takada M,Ohishi H,et al.Trigeminal ganglion neurons which project by way of axon collaterals to both the caudal spinal trigeminal and the principal sensory trigeminal nuclei,Brain Res.1992,594(1):155
[5]Hayashi H.Distributions of vibressae afferent fibers collaterals in the trigeminal nuclei as revealed by intraaxonal injection of horseradish peroxiase.Brain Res,1980,83(3):442
[6]Richmond FJR,Gladdy R,Creasy JL,et al.Efficacy of seven retrograde tracers,compared in multiple-labelling studies of feline motoneurons.J Neuronsci Methods,1994,53(1):35
, 百拇医药
[7]Feger J,Crossman AR,Identification of different subpopulation of neostriatal neurones projecting to globus pallidus or substantia nigra in the monkey:a retrograde fluorescence double-labeling study.Neuroscience Lett,1984,49(1):7
[8]Kupers HGJM,Bentivoglio M,Catsman-Berrevoets CE,et al.Double retrograde neuronal labeling through divergent axon colla terals,using two fluorescent tracers with the same excitation wavelength which label different features of the cell.Exp Brain Res,1980,40(3):383
, 百拇医药
[9]Macchi G,Bentivoglio M,Molinari M,et al.The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling.Exp Brain Res,1984,54(2):225
[10]Kantner RM,Kirby ML,Goldstein BD.Increase in substance P in the dorsal horn during a chemogenic nociceptive stimulus.Brain Res,1985,338(1):196
[11]Fiacco MD,Cuello AC.Substance P and enkephalin-containing neurons in the rat trigeminal system.Neuroscience,1980,5(5):803
, http://www.100md.com
[12]Maley BE,Elde R.Immunohistochemical localization of putative neurotransmitter within the feline nucleus tractus solitarii.Neuroscience,1982,7(3):2469
[13]Zhang WB,Li JS,Li HM.SP-like immunoreactivity in the primary trigeminal neurons projecting to the nucleus tractus solitarii.Brain Res,1991,558(1):87
[14]Menetrey D,Basnaum AI.Spinal and trigeminal projections to the nucleus of the solitary tract:a possible substrate for somatovisceral and viscerovisceral reflex activation.J Comp Neurol,1987,255(3):439
, http://www.100md.com
[15]Beitz AJ,Clements JR,Ecklund LJ,et al.The nuclei of origin of brainstem enkephalin and cholecystokinin projections to the spinal trigeminal nucleus of the rat.Neuroscience,1987,20(2):409
COLLATERAL PROJECTIONS TO BOTH CAUDAL SUBNUCLEUS
OF SPINAL TRIGEMINAL NUCLEUS AND NUCLEUS OF THE
SOLITARY TRACT FROM THE NEURONS IN TRIGEMINAL
GANGLION OF THE RAT
, 百拇医药
Zhang Wenbin△,Xiong Kanghui,Wang Bairen,Li Huimin,Li Jishuo
(Department of Anatomy and K.K.Leung Brain Research Centre,Fourth Military Medical Unversity,Xi'an)
The technique of double-labeled fluorescent tracing was used to determine whether the projections to the nucleus of the solitary tract(NTS) and caudal subnucleus of spinal trigeminal nucleus(VC)from the neurons in the trigeminal ganglion(VG)via axon collaterals.After Fast blue(FB)and Nuclear yellow(NY)were injected into VC and NTS,respectively,varied labeled neurons in VG were found under the fluorescence microscope(360nm excitation wavelength).FB displayed a blue fluorescent cytoplasm and NY appeared gold-yellow fluorescent nuclei.Although majority of the neurons were single-labeled with either FB or NY,some double-labeled neurons showing both yellow-green nuclei and blue cytoplasm were observed.Most double-labeled neurons were small and medium in size whose diameters were below 30μm.The interaction between the nociceptive information of oro-lingual mucosa,transmitted diffusively via the divergent axon collaterals of the neurons in VG,and the visceral and somatic sensations from other sources might take place in VC and NTS.
KEY WORDS trigeminal ganglion;caudal subnucleus of spinal trigeminal nucleus;nucleus of solitary tract;fluorescence;retrogrades transport;divergent projection;rat
△ Department of Anatomy and K.K.Leung Brain Research Centre,The Fourth Military Midical University,Xi'an 71003,China, 百拇医药
单位：第四军医大学解剖学教研室，梁銶琚脑研究中心，西安 710032
关键词：三叉神经节；三叉神经脊束核尾侧亚核；孤束核；荧光素；逆行追踪；分支投射；大鼠
解剖学报980305 摘 要 为研究三叉神经节神经元向三叉神经脊束核尾侧亚核(VC)和孤束核(NTS)的分支投射，用荧光素逆行追踪双标记方法，Fast blue(FB)和Nuclear yellow(NY)分别注射入三叉神经脊束核尾侧亚核和孤束核后，荧光显微镜(360nm激发波长)下可见三叉神经节内的多种逆行标记神经元。FB显示明亮的蓝色标记胞浆，而NY标记则为黄绿色的圆形胞核。虽大多数神经元为单标记，但部分也呈黄色胞核，蓝色胞浆的双标记细胞。双标记细胞多为直径30μm以下的中、小型，鲜见大型细胞。分支投射神经元可能扩散传递口、舌伤害性痛觉信息并在VC和NTS内与其他来源的内脏、躯体感觉传入信息相互影响。
, 百拇医药
三叉神经脊束核(spinal trigeminal nucleus,VSP)和孤束核(nucleus of the solitary tract,NTS)作为感觉中继站核，分别接受经三叉神经和舌咽、迷走等神经传入的头面部和内脏感觉信息。以往的研究证明，众多的三叉神经周围支中，只有舌、下牙槽及蝶腭等神经支的初级传入终末除投射入VSP外，部分终末支亦投射入NTS[1~3]。形态学的研究还证明，三叉神经感觉根一些传入纤维至中枢内的上升和下降支分支投射入感觉主核和脊束核[4]以及VSP的极间亚核和尾侧亚核[5]。但目前尚无向VSP和NTS的纤维投射起源于三叉神经节(trigeminal ganglion,VG)内相同神经元的研究报道。本实验以荧光素逆行追踪双标记的方法对VG内神经元向NTS和三叉神经脊束核分支投射进行了研究。
材料和方法
实验用SD雄性大鼠17只，体重200～280g,13例动物在腹腔内注射戊巴比妥钠(4mg/100g体重)麻醉下，手术暴露三叉神经脊束核的尾侧亚核(caudal subnucleus of spinal trigeminal nucleus,VC),用微量注射器(1μl)将2%快蓝(fast blue,FB,Sigma)水溶液缓慢注射入VC中段，成活2～3d后，再注射2%核黄(nuclear yellow,NY,Sigma)水溶液注射入同侧闩吻侧2～3mm平面的NTS，动物再成活15～20h。另4例动物变换荧光素的注射部位，即FB注入NTS而NY注入VC。深麻醉下经心脏先快速灌入50ml的生理盐水冲洗，继以含4%多聚甲醛的磷酸缓冲液(0.1mol/L,pH7.4)灌流固定。灌毕立即取脑和VG置入30%蔗糖磷缓液内过夜(4℃)。分别做脑和VG厚40μm和20μm的冰冻切片，即刻蒸馏水裱片，空气干燥。在配备A滤光片的荧光显微镜(Olympus BH2)下选择注射区准确且局限的材料，重点观察其VG内的逆行荧光标记神经元。
, 百拇医药
结 果
用360nm激发波长A滤光片，在荧光显微镜下可见两种荧光素表现不同的标记特征，FB显示明亮的蓝色胞浆，浅淡标记者依稀可辨缺损的中央核区。而NY标记则为黄绿色的圆形胞核(图A、B)。VC内注射FB后，整个VG内神经元常被大量标记。VG内标记神经元的数量和位置亦随注射中心区位移而略有变化。即注射中心区局限于VC背部者，其标记细胞主要位于VG的下颌神经区。相反，如标记中心区局限于VC腹部者，标记细胞主要位于眼和上颌神经区。标记细胞的形态、大小各不相同，一般大、中型细胞多呈圆形或椭圆形，小型者除圆形或椭圆形外，亦见不规则形或三角形。NY注射区范围局限于NTS内的材料主要在VG的下颌神经和上颌神经区域内见到黄绿色的标记胞核，这些黄绿色圆形胞核散布于蓝色胞浆的神经元之间，其数量后者多于前者。FB和NY逆行标记神经元均仅见于注射同侧的VG。虽大多数神经元为单标记，但也有部分呈黄色胞核，蓝色胞浆的双标记细胞(图A、B)。在NY胞核标记的细胞中约有21.3%也被FB标记而呈现双标记。因为FB标记的细胞数量远多于NY标记者，所以，仅较少比例的FB标记细胞显示双标记。值得注意的是，双标记细胞大多为直径30μm以下的中、小型，鲜见大型细胞(图A)。调换FB和NY的注射部位，即前者注射于NTS，后者注射于VC，在VG内的标记形式大体上与上述一致。
, 百拇医药
讨 论
运用神经元轴浆运输的逆行标记物、特别是联合配对使用荧光素常用来研究神经元的分支投射[6]。由于荧光素在中枢神经组织内容易扩散，所以，将其局限于中枢特定部位是准确分析结果的基础。在延髓特别是其尾段，同侧的NTS和VC相距较近，如FB或NY注射区涉及二核，势必造成VG内细胞双标记的假象。本实验用小剂量、缓慢注射，尽量缩小注射区范围，使之局限于靶核区内。同时，经背侧进针穿过脊束的FB注射区位于闩以下VC段，这样既避免累及主要投射入闩以上NTS 的舌神经和蝶腭神经在脊束内下行轴突支。而且位于闩以下VC段FB注射区同闩以上2～3mm平面NTS注射区呈吻尾关系，又可进一步避免两种荧光素注射区之间的相互影响。镜下观察首先摒弃注射中心区扩及邻近结构或脱离靶区的动物例，其次，选择NTS注射例的标记细胞只局限于VC内上颌和下颌神经区的材料(三叉神经领域内的眼神经无纤维投射入NTS)。这样就保证了实验结果的客观和可靠性。
三叉神经节内神经元中枢突有分支投射到三叉神经感觉核簇的吻、尾诸核[4,5]。本实验结果证明，三叉神经节内一些细胞还分支投射入VC和三叉神经感觉核以外的NTS，且投射至后者的VG节细胞约有21.3%是属于分支投射细胞。除周围神经初级传入外，在中枢神经内普遍存在神经元分支投射的现象[7～9]。与非分支投射神经元相比，分支投射神经元被认为在传递同样信息时，可对其靶结构产生更广泛、更有效的影响[7，9]。SP是传递伤害性信息的神经活性物质[10]。SP、CGRP等多肽类神经递质单独或者共存于三叉神经节细胞内，特别是节内中、小型细胞多含SP，且它们直接投射入VC和NTS[11～13]。因为以往其他学者以及我们的研究结果均证明，闩以上2～3mm平面的NTS内侧亚核区主要接受舌神经和蝶腭神经初级传入终末的浓密投射[1，3]。本实验结果提示，VG内的双标记细胞可能代表周围突组成舌神经和蝶腭神经且主要支配口、舌和鼻粘膜的感觉神经元，其中枢突既向VC又向NTS投射。舌神经和蝶腭等神经传递口、舌和鼻粘膜区域感觉信息，包括伤害性刺激传入信息，经VG内中、小型神经元分支的中枢突扩散投射并广泛影响中枢内感觉中继核团。NTS和VC分别接受内脏和三叉神经初级传入终末，同时NTS和VC两者还存在双向纤维联系[14，15]。经分支投射神经元扩散传递的口、舌伤害性信息也可能在VC和NTS内，与其他来源的内脏、躯体多种感觉传入信息相互影响，产生复杂的抑制或易化的调节、整合作用。其对伤害性传入信息的调控及功能意义还有待进一步深入研究。
, 百拇医药
收稿1997-07 修回1997-12
图版说明
图A、B分别注射Fast blue(FB)和Nuclear yellow(NY)入三叉神经脊束核尾侧亚核(VC)和孤束核后三叉神经节内的逆行标记细胞。有3种类型的标记细胞，即NY单标记胞核(三角)、FB单标记胞浆(空心箭头)和FB+NY双标记神经元(实心白色箭头)。双标记神经元多为中、小型。图A中央左侧可见一小型的双标记神经元。图B左下方可见一较大型的FB单标记神经元。标尺示80μm，两图的放大倍数相同。
Explanation of figuers
Photomicrographs of retrogradely labeled neurons in the trigeminal ganglion after Fast blue(FB)and Nuclear yellow (NY) injecting into the caudal subnucleus of spinal trigeminal nucleus(VC)and the nucleus of the solitary tract,respectively.There are three kinds of labeled neurons:single-labeled nucleus of neurons with NY(triangles),single-labeled cytoplasm of neurons with FB(hollow arrows)and double-labeled neurons(solid white arrows).Most double-labeled neurons are small and medium in size.There is a samll sized double-labeled neuron in the central left side of Fig.A. A large sized FB single-labeled neuron is found in the left lower side of Fig.B. Bar=80μm in Fig.A,the magnification of Fig.B is the same as Fig.A.
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参考文献
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COLLATERAL PROJECTIONS TO BOTH CAUDAL SUBNUCLEUS
OF SPINAL TRIGEMINAL NUCLEUS AND NUCLEUS OF THE
SOLITARY TRACT FROM THE NEURONS IN TRIGEMINAL
GANGLION OF THE RAT
, 百拇医药
Zhang Wenbin△,Xiong Kanghui,Wang Bairen,Li Huimin,Li Jishuo
(Department of Anatomy and K.K.Leung Brain Research Centre,Fourth Military Medical Unversity,Xi'an)
The technique of double-labeled fluorescent tracing was used to determine whether the projections to the nucleus of the solitary tract(NTS) and caudal subnucleus of spinal trigeminal nucleus(VC)from the neurons in the trigeminal ganglion(VG)via axon collaterals.After Fast blue(FB)and Nuclear yellow(NY)were injected into VC and NTS,respectively,varied labeled neurons in VG were found under the fluorescence microscope(360nm excitation wavelength).FB displayed a blue fluorescent cytoplasm and NY appeared gold-yellow fluorescent nuclei.Although majority of the neurons were single-labeled with either FB or NY,some double-labeled neurons showing both yellow-green nuclei and blue cytoplasm were observed.Most double-labeled neurons were small and medium in size whose diameters were below 30μm.The interaction between the nociceptive information of oro-lingual mucosa,transmitted diffusively via the divergent axon collaterals of the neurons in VG,and the visceral and somatic sensations from other sources might take place in VC and NTS.
KEY WORDS trigeminal ganglion;caudal subnucleus of spinal trigeminal nucleus;nucleus of solitary tract;fluorescence;retrogrades transport;divergent projection;rat
△ Department of Anatomy and K.K.Leung Brain Research Centre,The Fourth Military Midical University,Xi'an 71003,China, 百拇医药