Ultrastructural analysis of glutamate-, GABA-, and glycine-immunopositive boutons from supratrigeminal premotoneurons in the rat trigeminal motor nucleus

Journal of Neuroscience Research

Volumn 87, Issue 5, 2009, Pages 1115-1122

  Paik, Sang Kyoo ^a   Lee, Hyo Jeong ^a   Choi, Min Ki ^a   Cho, Yi Sul ^a   Park, Mae Ja ^a   Moritani, Masayuki ^b   Yoshida, Atsushi ^b   Kim, Yun Sook ^a   Bae, Yong Chul ^a  

^a Kyungpook National University   (South Korea)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Immunohistochemistry; Premotoneuron; Supratrigeminal region; Synaptic organization; Ultrastructure

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLERA TOXIN B SUBUNIT; GLUTAMIC ACID; GLYCINE; HORSERADISH PEROXIDASE;

AMINO ACID ANALYSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; IMMUNOGOLD STAINING; IMMUNOHISTOCHEMISTRY; MALE; MOTONEURON NUCLEUS; NERVE ENDING; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SYNAPTIC TRANSMISSION; TRIGEMINAL NUCLEUS;

ANIMALS; CHOLERA TOXIN; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; HORSERADISH PEROXIDASE; IMMUNOHISTOCHEMISTRY; MALE; MICROINJECTIONS; MICROSCOPY, ELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; TRIGEMINAL NUCLEI;

EID: 65949083551     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21929     Document Type: Article

References (49)

1. Bae YC, Nakagawa S, Yasuda K, Yabuta NH, Yoshida A, Pil PK, Moritani M, Chen K, Nagase Y, Takemura M, Shigenaga Y. 1996. Electron microscopic observation of synaptic connections of jaw-muscle spindle and periodontal afferent terminals in the trigeminal motor and supratrigeminal nuclei in the cat. J Comp Neurol 374:421-435.
2. Bae YC, Nakamura T, Ihn HJ, Choi MH, Yoshida A, Moritani M, Honma S, Shigenaga Y. 1999. Distribution pattern of inhibitory and excitatory synapses in the dendritic tree of single masseter alpha-motoneurons in the cat. J Comp Neurol 414:454-468.
3. Bae YC, Ihn HJ, Park MJ, Ottersen OP, Moritani M, Yoshida A, Shigenaga Y. 2000. Identification of signal substances in synapses made between primary afferents and their associated axon terminals in the rat trigeminal sensory nuclei. J Comp Neurol 418:299-309.
4. Bae YC, Choi BJ, Lee MG, Lee HJ, Park KP, Zhang LF, Honma S, Fukami H, Yoshida A, Ottersen OP, Shigenaga Y. 2002. Quantitative ultrastructural analysis of glycine- and gamma-aminobutyric acid-immunoreactive terminals on trigeminal alpha- and gamma-motoneuron somata in the rat. J Comp Neurol 442:308-319.
5. Bae YC, Kim JP, Choi BJ, Park KP, Choi MK, Moritani M, Yoshida A, Shigenaga Y. 2003. Synaptic organization of tooth pulp afferent terminals in the rat trigeminal sensory nuclei. J Comp Neurol 463:13-24.
6. Bae YC, Ahn HJ, Park KP, Kim HN, Paik SK, Bae JY, Lee HW, Kim KH, Yoshida A, Moritani M, Shigenaga Y. 2005a. The synaptic microcircuitry associated with primary afferent terminals in the interpolaris and caudalis of trigeminal sensory nuclear complex. Brain Res 1060:118-125.
7. Bae YC, Park KS, Bae JY, Paik SK, Ahn DK, Moritani M, Yoshida A, Shigenaga Y. 2005b. GABA and glycine in synaptic microcircuits associated with physiologically characterized primary afferents of cat trigeminal principal nucleus. Exp Brain Res 162:449-457.
8. Dessem D, Iyadurai OD, Taylor A. 1988. The role of periodontal receptors in the jaw-opening reflex in the cat. J Physiol 406:315-330.
9. Dessem D, Donga R, Luo P. 1997. Primary- and secondary-like jawmuscle spindle afferents have characteristic topographic distributions. J Neurophysiol 77:2925-2944.
10. Ji ZQ, Aas JE, Laake J, Walberg F, Ottersen OP. 1991. An electron microscopic, immunogold analysis of glutamate and glutamine in terminals of rat spinocerebellar fibers. J Comp Neurol 307:296-310.
11. Kamogawa H, Hanashima N, Naito K, Kagaya K. 1988. Candidate interneurons mediating peripherally evoked disynaptic inhibition of masseter motoneurons of both sides. Neurosci Lett 95:149-154.
12. Kamogawa H, Manabe K, Kondo M, Naito K. 1994. Supra- and juxtatrigeminal inhibitory premotor neurons with bifurcating axons projecting to masseter motoneurons on both sides. Brain Res 639:85-92.
13. 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.
14. Kolston J, Osen KK, Hackney CM, Ottersen OP, Storm-Mathisen J. 1992. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol (Berl) 186:443-465.
15. Kolta A. 1997. In vitro investigation of synaptic relations between interneurons surrounding the trigeminal motor nucleus and masseteric motoneurons. J Neurophysiol 78:1720-1725.
16. Kolta A, Westberg KG, 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.
17. Li JL, Wu SX, Tomioka R, Okamoto K, Nakamura K, Kaneko T, Mizuno N. 2005. Efferent and afferent connections of GABAergic neurons in the supratrigeminal and the intertrigeminal regions. An immunohistochemical tract-tracing study in the GAD67-GFP knock-in mouse. Neurosci Res 51:81-91.
18. Li YQ, 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.
19. Li YQ, Tao FS, Okamoto K, Nomura S, Kaneko T, Mizuno N. 2002. The supratrigeminal region of the rat sends GABA/glycine-cocontaining axon terminals to the motor trigeminal nucleus on the contralateral side. Neurosci Lett 330:13-16.
20. Luo P, Wong R, Dessem D. 1995. Ultrastructural basis for synaptic transmission between jaw-muscle spindle afferents and trigeminothalamic neurons in the rostral trigeminal sensory nuclei of the rat. J Comp Neurol 363:109-128.
21. Luo P, Dessem D. 1999. Ultrastructural anatomy of physiologically identified jaw-muscle spindle afferent terminations onto retrogradely labeled jaw-elevator motoneurons in the rat. J Comp Neurol 406:384-401.
22. Minkels RF, Jüch PJ, van Willigen JD. 1995. Interneurones of the supra-trigeminal area mediating reflex inhibition of trigeminal and facial motorneurones in the rat. Arch Oral Biol 40:275-284.
23. 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.
24. Ohta M, Moriyama Y. 1986. Supratrigeminal neurons mediate the shortest, disynaptic pathway from the central amygdaloid nucleus to the contralateral trigeminal motoneurons in the rat. Comp Biochem Physiol A 83:633-641.
25. Ornung G, Ottersen OP, Cullheim S, Ulfhake B. 1998. Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp Brain Res 118:517-532.
26. Ottersen OP, Storm-Mathisen J. 1984. Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229:374-392.
27. Ottersen OP. 1989. Postembedding immunogold labelling of fixed glutamate: an electron microscopic analysis of the relationship between gold particle density and antigen concentration. J Chem Neuroanat 2:57-66.
28. Paik SK, Oh SJ, Son YJ, Ma SK, Ahn CH, Kim SK, Chang Z, Moritani M, Yoshida A, Bae YC. 2005. Neural mechanisms controlling jaw-jerk reflex in the cat. Neuroreport 16:1565-1568.
29. Paik SK, Bae JY, Park SE, Moritani M, Yoshida A, Yeo EJ, Choi KS, Ahn DK, Moon C, Shigenaga Y, Bae YC. 2007. Developmental changes in distribution of gamma-aminobutyric acid- and glycine-immunoreactive boutons on rat trigeminal motoneurons. I. Jaw-closing motoneurons. J Comp Neurol 503:779-789.
30. Paxinos G, Watson C. 2005. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
31. Ralston HJ 3rd, Light AR, Ralston DD, Perl ER. 1984. Morphology and synaptic relationships of physiologically identified low-threshold dorsal root axons stained with intra-axonal horseradish peroxidase in the cat and monkey. J Neurophysiol 51:777-792.
32. Rampon C, Peyron C, Petit JM, Fort P, Gervasoni D, Luppi PH. 1996. Origin of the glycinergic innervation of the rat trigeminal motor nucleus. Neuroreport 7:3081-3085.
33. Semba K, Masarachia P, Malamed S, Jacquin M, Harris S, Egger MD. 1984. Ultrastructure of pacinian corpuscle primary afferent terminals in the cat spinal cord. Brain Res 302:135-150.
34. Semba K, Masarachia P, Malamed S, Jacquin M, Harris S, Yang G, Egger MD. 1985. An electron microscopic study of terminals of rapidly adapting mechanoreceptive afferent fibers in the cat spinal cord. J Comp Neurol 232:229-240.
35. Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H. 1988. Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res 445:392-399.
36. 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.
37. Shigenaga Y, Moritani M, Oh SJ, Park KP, Paik SK, Bae JY, Kim HN, Ma SK, Park CW, Yoshida A, Ottersen OP, Bae YC. 2005. The distribution of inhibitory and excitatory synapses on single, reconstructed jaw-opening motoneurons in the cat. Neuroscience 133:507-518.
38. Shupliakov O, Brodin L, Cullheim S, Ottersen OP, Storm-Mathisen J. 1992. Immunogold quantification of glutamate in two types of excitatory synapse with different firing patterns. J Neurosci 12:3789-3803.
39. Stornetta RL, Sevigny 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.
40. Takahashi O, Satoda T, Uchida T. 1995. Distribution of GABA-immunoreactive premotor neurons projecting to the trigeminal motor nucleus in the rat. J Hirnforsch 36:203-208.
41. Todd AJ, Watt C, Spike RC, Sieghart W. 1996. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci 16:974-982.
42. 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.
43. Turman JE Jr, Chandler SH. 1994a. Immunohistochemical evidence for GABA and glycine-containing trigeminal premotoneurons in the guinea pig. Synapse 18:7-20.
44. Turman JE Jr, Chandler SH. 1994b. Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons. Brain Res 634:49-61.
45. Turman JE Jr, Ajdari J, Chandler SH. 1999. NMDA receptor NR1 and NR2A/B subunit expression in trigeminal neurons during early postnatal development. J Comp Neurol 409:237-249.
46. Turman JE Jr, Hiyama L, Castillo M, Chandler SH. 2001. Expression of group I and II metabotropic glutamate receptors in trigeminal neurons during postnatal development. Dev Neurosci 23:41-54.
47. Watanabe M, Tanaka E, Nishi M, Iwabe T, Hattori Y, Suemune S, Tanne K. 2002. Expression of c-Fos-like immunoreactive neurons in the supratrigeminal region in the rat following noxious stimulation of the orofacial tissues. Neurosci Lett 335:99-102.
48. Watson AH. 2004. Synaptic interactions between the terminals of slow-adapting type II mechanoreceptor afferents and neurones expressing gamma-aminobutyric acid- and glycine-like immunoreactivity in the rat spinal cord. J Comp Neurol 471:168-179.
49. Weinberg RJ, van Eyck SL. 1991. A tetramethylbenzidine/tungstate reaction for horseradish peroxidase histochemistry. J Histochem Cytochem 39:1143-1148.