Axon terminals expressing vesicular glutamate transporter VGLUT1 or VGLUT2 within the trigeminal motor nucleus of the rat: Origins and distribution patterns

Journal of Comparative Neurology

Volumn 512, Issue 5, 2009, Pages 595-612

  Pang, You Wang ^a,b   Ge, Shun Nan ^a   Nakamura, Kouichi C ^c,d   Li, Jin Lian ^a   Xiong, Kang Hui ^a   Kaneko, Takeshi ^c,d   Mizuno, Noboru ^c  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b No 180 Hospital of Chinese PLA   (China)

^c KYOTO UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Electron microscopy; Glutamatergic neurons; Immunohistochemistry; In situ hybridization; Masticatory motoneurons; Premotor neurons

Indexed keywords

VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HISTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; JAW MOVEMENT; MESENCEPHALON; MOTONEURON; MUSCLE SPINDLE AFFERENT NERVE; NERVE ENDING; NERVE FIBER; NERVE FIBER TRANSECTION; NONHUMAN; PRIORITY JOURNAL; RAT; TRIGEMINAL NUCLEUS; ANIMAL; CYTOLOGY; GENETICS; HISTOLOGY; MALE; METABOLISM; NERVE TRACT; SPRAGUE DAWLEY RAT; SYNAPTOSOME; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; GLUTAMIC ACID; IN SITU HYBRIDIZATION; MALE; MOTOR NEURONS; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; TRIGEMINAL NUCLEI; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 59049093935     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21894     Document Type: Article

References (74)

1. Alvarez FJ, Villalba RM, Zerda R, Schneider SP. 2004. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472:257-280.
2. Amri M, Car A, Roman C. 1990. Axonal branching of medullary swallowing neurons projecting on the trigeminal and hypoglossal motor nuclei: demonstration by electrophysiological and fluorescent double labeling techniques. Exp Brain Res 81:384-390.
3. Appenteng K, Girdlestone D. 1987. Transneuronal transport of wheat germ agglutinin-conjugated horseradish peroxidase into trigeminal interneurones of the rat. J Comp Neurol 258:387-396.
4. Blom S. 1960. Afferent influences on tongue muscle activity. A morphological and physiological study in the cat. Acta Physiol Scand 49(Suppl 170):1-97.
5. Bowman JP. 1971. The muscle spindle and neural control of the tongue: implications for speech. Springfield, IL: Charles C. Thomas.
6. Brodal A. 1981. Neurological anatomy in relation to clinical medicine, 3rd ed. New York: Oxford University Press.
7. Byers MR, O'Connor TA, Martin RF, Dong WK. 1986. Mesencephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol 250:181-191.
8. Chandler SH. 1989. Evidence for excitatory amino acid transmission between mesencephalic nucleus of V afferents and jaw-closing motoneurons in the guinea pig. Brain Res 477:252-264.
9. Fort P, Luppi P-H, Sakai K, Salvert D, Jouvet M. 1990. Nuclei of origin of monoaminergic, peptidergic, and cholinergic afferents to the cat trigeminal motor nucleus: a double-labeling study with cholera-toxin as a retrograde tracer. J Comp Neurol 301:262-275.
10. Fremeau RT Jr, Tryer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
11. Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH. 2004. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98-103.
12. Fujiyama F, Furuta T, Kaneko T. 2001. Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379-387.
13. Fujiyama F, Unzai T, Nakamura K, Nomura S, Kaneko T. 2006. Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur J Neurosci 24:2813-2824.
14. Furuta T, Timofeeva E, Nakamura K, Okamoto-Furuta K, Togo M, Kaneko T, Deschênes M. 2008. Inhibitory gating of vibrissal inputs in the brainstem. J Neurosci 8:1789-1797.
15. Goldberg LJ, Nakamura Y. 1968. Lingually induced inhibition of masseteric motoneurons. Experientia 24:371-373.
16. Hioki H, Fujiyama F, Taki K, Tomioka R, Furuta T, Tamamaki N, Kaneko T. 2003. Differential distribution of vesicular glutamate transporters in the rat cerebellar cortex. Neuroscience 117:1-6.
17. Holstege G, Kuypers HGJM, Dekker JJ. 1977. The organization of the bulbar fibre connections to the trigeminal, facial and hypoglossal motor nuclei. II. An autographic tracing study in cat. Brain 100:265-286.
18. Hosokawa H. 1961. Proprioceptive innervations of striated muscle in the territory of cranial nerves. Texas Rep Biol Med 19:405-464.
19. Hughes DI, Polgar E, Shehab SAS, Todd AJ. 2004. Peripheral axotomy induces depletion of the vesicular glutamate transporter VGLUT1 in central terminals of myelinated afferent fibres in the rat spinal cord. Brain Res 1017:69-76.
20. Jerge CR. 1963. The function of the nucleus supratrigeminalis. J Neurophysiol 26:393-402.
21. Kaneko T, Fujiyama F. 2002. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 42:243-250.
22. Kaneko T, Mizuno N. 1988. Immunohistochemical study of glutaminase-containing neurons in the cerebral cortex and thalamus of the rat. J Comp Neurol 267:590-602.
23. Kaneko T, Mizuno N. 1994. Glutamate-synthesizing enzymes in GABAergic neurons of the neocortex: a double immunofluorescence study in the rat. Neuroscience 61:839-849.
24. Kaneko T, Fujiyama F, Hioki H. 2002. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39-62.
25. Kidokoro Y, Kubota K, Shuto S, Sumino R. 1968. Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J Neurophysiol 31:709-716.
26. Kolta A, Westberg K-G, Lund JP. 2000. Identification of brainstem interneurons projecting to the trigeminal motor nucleus and adjacent structures in the rabbit. J Chem Neuroanat 19:175-195.
27. Kubota K, Masegi T. 1972. Muscle spindle distribution in the masticatory muscle of the Japanese shrew-mole. J Dent Res 51:1080-1091.
28. Kubota K, Masegi T. 1977. Muscle spindle supply to the human jaw muscle. J Dent Res 51:1080-1091.
29. Landgren S, Olsson KÅ, Westberg KG. 1986. Bulbar neurons with axonal projections to the trigeminal motor nucleus in the cat. Exp Brain Res 65:98-111.
30. Landry M, Bouali-Benazzouz R, Mestikawy SE, Ravassard P, Nagy F. 2004. Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J Comp Neurol 468: 380-394.
31. Lazarov NE. 2000. The mesencephalic trigeminal nucleus in the cat. Advances in anatomy, embryology and cell biology 153. Berlin: Springer.
32. Li J-L, Fujiyama F, Kaneko T, Mizuno N. 2003a. Expression of vesicular glutamate transporters, VGLUT1 and VGLUT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J Comp Neurol 457:236-249.
33. Li J-L, Xiong K-H, Dong Y-L, Fujiyama F, Kaneko T, Mizuno N. 2003b. Vesicular glutamate transporters, VGLUT1 and VGLUT2, in the trigeminal ganglion neurons of the rat, with special reference to coexpression. J Comp Neurol 463:212-220.
34. Li Y-Q, Takada M, Mizuno N. 1993. The sites of origin of serotoninergic afferent fibers in the trigeminal motor, facial, and hypoglossal nuclei in the rat. Neurosci Res 17:307-313.
35. Li Y-Q, Takada M, Kaneko T, Mizuno N. 1995. Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem of the rat. J Comp Neurol 356:563-579.
36. Li Y-Q, Takada M, Kaneko T, Mizuno N. 1996. GABAergic and glycinergic neurons projecting to the trigeminal motor nucleus: a double labeling study in the rat. J Comp Neurol 373:498-510.
37. Liang F, Hatanaka Y, Saito H, Yamamori T, Hashikawa T. 2000. Differential expression of γ-aminobutyric acid type B receptor-1a and -1b mRNA variants in GABA and non-GABAergic neurons of the rat brain. J Comp Neurol 416:475-495.
38. Lyons WE, Grzanna R. 1988. Noradrenergic neurons with divergent projections to the motor trigeminal nucleus and the spinal cord: a double retrograde neuronal labeling study. Neuroscience 26:681-693.
39. Matsuda K, Uemura M, Kume M, Matsushima R, Mizuno N. 1978. Topographical representation of masticatory muscles in the motor trigeminal nucleus in the rabbit: a HRP study. Neurosci Lett 8:1-4.
40. Meessen H, Olszewski J. 1949. Cytoarchitektonischer Atlas des Rautenhirns des Kaninchens. Basel: Karger
41. Mizuno N. 1970. Projection fibers from the main sensory trigeminal nucleus and the supratrigeminal region. J Comp Neurol 139:457-472.
42. Mizuno N, Konishi A, Sato M. 1975. Localization of masticatory motoneurons in the cat and rat by means of retrograde axonal transport of horseradish peroxidase. J Comp Neurol 164:105-116.
43. Mizuno N, Nomura S, Itoh K, Nakamura Y, Konishi A. 1978. Commissural interneurons for masticatory motoneurons: a light and electron microscope study using the horseradish peroxidase tracer technique. Exp Neurol 59:254-262.
44. Mizuno N, Matsuda K, Iwahori N, Uemura-Sumi M, Kume M, Matsushima R. 1981. Representation of the masticatory muscles in the motor trigeminal nucleus of the macaque monkeys. Neurosci Lett 21:19-22.
45. Mizuno N, Yasui Y, Nomura S, Itoh K, Konishi A, Takada M, Kudo M. 1983. A light and electron microscopic study of premotor neurons for the trigeminal motor nucleus. J Comp Neurol 215:290-298.
46. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
47. Nakamura Y, Mori S, Nagashima H. 1973. Origin and central pathways of crossed inhibitory effects of afferents from the masseteric muscle on the masseteric motoneurons of the cat. Brain Res 57:29-42.
48. Nakamura K, Watakabe A, Hioki H, Fujiyama F, Tanaka Y, Yamamori T, Kaneko T. 2007. Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient. Eur J Neurosci 26:3054-3067.
49. Odagiri N, Kubota K, Shibanai S. 1993. Density of muscle spindles in the jaw muscles of the Japanese flying squirrel and the guinea pig. Ann Anat 175:263-270.
50. Oliveira ALR, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hökfeld T, Cullheim S, Meister B. 2003. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50:117-129.
51. Olsson KÅ, Landgren S, Westberg KG. 1986. Location of, and peripheral convergence on, the interneurons in the disynaptic path from the coronal gyrus of the cerebral cortex to the trigeminal motoneurones in the cat. Exp Brain Res 65:83-97.
52. Olsson KÅ, Westberg K-G. 1991. Integration in trigeminal premotor interneurones in the cat. 2. Functional characteristics of neurons in the subnucleus-γ of the oral nucleus of the spinal trigeminal tract with a projection to the digastrics motoneurone subnucleus. Exp Brain Res 84:115-124.
53. Pang Y-W, Li J-L, Nakamura K, Wu S-X, Kaneko T, Mizuno N. 2006. Expression of vesicular glutamate transporter 1 immunoreactivity in peripheral and central endings of trigeminal mesencephalic nucleus neurons in the rat. J Comp Neurol 498:129-141.
54. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates, 4th ed. London: Academic Press.
55. Rampon C, Peyron C, Petit J-M, Fort P, Gervasoni D, Luppi P-H. 1996. Origin of the glycinergic innervations of the rat trigeminal motor nucleus. Neuroreport 7:3081-3085.
56. Rokx JT, van Willigen JD, Jansen HW. 1984. Muscle fiber types and muscle spindle in the jaw musculature of the rat. Arch Oral Biol 29:25-31.
57. Rowlerson A, Muscarello F, Baker D, Saed H. 1988. Muscle spindle distribution in relation to the fibre-type composition of masseter in mammals. J Anat 161:37-60.
58. Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana Y, Hosoi M, Yoshida A, Kagawa K. 1989. Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat - intra-axonal staining with HRP. Brain Res 505:91-110.
59. Shigenaga Y, Mitsuhiro Y, Shirana Y, Tsuru H. 1990. Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 514:214-37.
60. Shigenaga Y, Hirose Y, Yoshida A, Fukami H, Honma S, Bae YC 2000. Quantitative ultrastructure of physiologically identified premotoneuron terminals in the trigeminal motor nucleus in the cat. J Comp Neurol 426:13-30.
61. Stornetta RL, Sevign CP, Guyenet PG. 2002. Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 444:191-206.
62. Tochitani S, Liang F, Watakabe A, Hashikawa T, Yamamori T. 2001. The occ1 gene is preferentially expressed in the primary visual cortex in an activity-dependent manner: a pattern of gene expression related to the cytoarchitectonic area in adult macaque neocortex. Eur J Neurosci 13:297-307.
63. Todd AJ, Hughes DI, Polgar E, Nagy GG, Mackie M, Ottersen OP, Maxwell DJ. 2003. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17:13-27.
64. Travers JB, Norgren R. 1983. Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280-298.
65. Travers JB, Yoo JE, Chandran R, Herman K, Travers SP. 2005. Neurotransmitter phenotypes of intermediate zone reticular formation projections to the motor trigeminal and hypoglossal nuclei in the rat. J Comp Neurol 488:28-47.
66. Turman JE Jr, Chandler SH. 1994a. Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons. Brain Res 634:49-61.
67. Turman JE Jr, Chandler SH. 1994b. Immunohistochemical evidence for GABA and glycine-containing trigeminal premotorneurons in the guinea pig. Synapse 18:7-20.
68. Uemura-Sumi M, Takahashi O, Matsushima R, Takata M, Yasui Y, Mizuno N. 1982. Localization of masticatory motoneurons in the trigeminal motor nucleus of the guinea pig. Neurosci Lett 29:219-224.
69. Watakabe A, Ohsawa S, Hashikawa T, Yamamori T. 2006. Binding and complementary expression patterns of semaphorin 3E and plexin D1 in the mature neocortices of mice and monkeys. J Comp Neurol 499: 258-273.
70. Westberg K-G, Sandstrom G, Olsson KÅ. 1995. Integration in trigeminal premotor interneurones in the cat. 3. Input characteristics and synaptic actions of neurons in subnucleus-γ of the oral nucleus of the spinal trigeminal tract with a projection to the masseteric motoneurone subnucleus. Exp Brain Res 104:449-461.
71. Westberg K-G, Clavelou P, Sandstrom G, Lund JP. 1998. Evidence that trigeminal brainstem interneurons form subpopulations to produce different forms of mastication in the rabbit. J Neurosci 18:6466-6479.
72. Yasui Y, Tsumori T, Ono K, Kishi T. 1997. Nigral axon terminals are in contact with parvicellular reticular neurons which project to the motor trigeminal nucleus in the rat. Brain Res 775:219-224.
73. Yoshida A, Yasuda K, Dostrovsky O, Bae YC, Takemura M, Shigenaga Y, Sessle BJ. 1994. Two major types of premotoneurons in the feline trigeminal nucleus oralis as demonstrated by intracellular staining with horseradish peroxidase. J Comp Neurol 347:495-514.
74. Yoshida A, Hiraga T, Moritani M, Chen K, Takatsuki Y, Hirose Y, Bae YC, Shigenaga Y. 1998. Morphologic characteristics of physiologically defined neurons in the cat trigeminal nucleus principalis. J Comp Neurol 401:308-328.