Identification of c-Fos immunoreactive brainstem neurons activated during fictive mastication in the rabbit

Experimental Brain Research

Volumn 165, Issue 4, 2005, Pages 478-489

  Athanassiadis, T ^a   Olsson, K A ^a   Kolta, A ^b   Westberg, K G ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Pattern generation; Rhythmical movements; Trigeminal system

Indexed keywords

BIOLOGICAL MARKER; PROTEIN C FOS;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; BRAIN REGION; BRAIN STEM; BRAIN TISSUE; CELL POPULATION; CONTROLLED STUDY; ELECTROSTIMULATION; MALE; MASTICATION; MOTONEURON; NEUROANATOMY; NONHUMAN; PARALYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; RECORDING; SURVIVAL; TRIGEMINAL NUCLEUS;

ANESTHESIA; ANIMALS; BRAIN STEM; DATA INTERPRETATION, STATISTICAL; EFFERENT PATHWAYS; ELECTRIC STIMULATION; IMMUNOHISTOCHEMISTRY; MALE; MASTICATION; MASTICATORY MUSCLES; MICROELECTRODES; MOTOR CORTEX; MOTOR NEURONS; NEURONS; PARALYSIS; PROTO-ONCOGENE PROTEINS C-FOS; RABBITS;

EID: 24044537640     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-005-2319-5     Document Type: Article

References (114)

1. Aldes LD, Boone TB (1985) Organization of projections from the principal sensory trigeminal nucleus to the hypoglossal nucleus in the rat: an experimental light and electron microscopic study with axonal tracer techniques. Exp Brain Res 59:16-29
2. 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
3. Appenteng K, Conyers L, Curtis J, Moore J (1990) Monosynaptic connections of single V interneurones to the contralateral V motor nucleus in anaesthetised rats. Brain Res 514:128-130
4. Ariyasinghe S, Inoue M, Yamamura K, Harasawa Y, Kurose M, Yamada Y (2004) Coordination of jaw and extrinsic tongue muscle activity during rhythmic jaw movements in anesthetized rabbits. Brain Res 1016:201-216
5. Barajon I, Gossard JP, Hultborn H (1992) Induction of Fos expression by activity in the spinal rhythm generator for scratching. Brain Res 588:168-172
6. Brocard F, Lund JP, Kolta A (2004) Firing properties of trigeminal principal sensory nucleus neurons change during the emergence of mastication in weaning rats. Soc Neurosci Abstr 34:879:7
7. Brudzynski SM, Wang D (1996) c-Fos immunohistochemical localization of neurons in the mesencephalic locomotor region in the rat brain. Neuroscience 75:793-803
8. Carr PA, Huang A, Noga BR, Jordan LM (1995) Cytochemical characteristics of cat spinal neurons activated during fictive locomotion. Brain Res Bull 37:213-218
9. Chandler SH, Tal M (1986) The effects of brain stem transections on the neuronal networks responsible for rhythmical jaw muscle activity in the guinea pig. J Neurosci 6:1831-1842
10. Chandler SH, Goldberg LJ (1988) Effects of pontomedullary reticular formation stimulation on the neuronal networks responsible for rhythmical jaw movements in the guinea pig. J Neurophysiol 59:819-832
11. Chandler SH, Turman JE, Salem L, Goldberg LJ (1990) The effects of nanoliter ejections of lidocaine into pontomedullary reticular formation on cortically induced rhythmical jaw movements in the guinea pig. Brain Res 256:54-64
12. Coggeshall RE, Lekan HA (1996) Methods for determining numbers of cells and synapses: a case for more uniform standards of review. J Comp Neurol 364:6-15
13. Dai X, Noga BR, Douglas JR, Jordan LM (2005) Localisation of spinal neurons activated during locomotion using the c-Fos immunohistochemical method. J Neurophysiol. DOI 10.1152/ jn.00578.2004
14. Dallel R, Raboisson P, Woda A, Sessle BJ (1990) Properties of nociceptive and non-nociceptive neurons in trigeminal subnucleus oralis of the rat. Brain Res 521(1-2):95-106
15. Dampney RA, Li YW, Hirooka Y, Potts P, Poison JW (1995) Use of c-Fos functional mapping to identify the central baroreceptor reflex pathway: advantages and limitations. Clin Exp Hypertens 17:197-208
16. De S, Shuler CF, Turman JE (2003) The ontogeny of Krox-20 expression in brainstem and cerebellar neurons. J Chem Neuroanat 25:213-226
17. Donga R, Lund JP, Veilleux D (1990) An electrophysiological study of trigeminal commissural interneurons in the anaesthetized rabbit. Brain Res 515:351-354
18. Donga R, Lund JP (1991) Discharge patterns of trigeminal commissural last-order interneurons during fictive mastication in the rabbit. J Neurophysiol 66:1564-1578
19. Dragunow M, Faull R (1989) The use of c-fos as a metabolic marker in neuronal pathway tracing. J Neurosci Methods 29:261-265
20. Eisenman J, Landgren S, Novin D (1963) Functional organization in the main sensory trigeminal nucleus and in the rostral subdivision of the nucleus of the spinal trigeminal tract in the cat. Acta Physiol Scand 59(Suppl 214):S1-S44
21. Enomoto A, Kogo M, Koizumi H, Ishihama K, Yamanishi T (2002) Localization of premotoneurons for an NMDA-induced repetitive rhythmical activity to TMNs. Neuroreport 13:2303-2307
22. Falls WM (1984) Termination in trigeminal nucleus oralis of ascending intratrigeminal axons originating from neurons in the medullary dorsal horn: an HRP study in the rat employing light and electron microscopy. Brain Res 290:136-140
23. Fay RA, Norgren R (1997a) Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus. I. Masticatory muscle motor systems. Brain Res Rev 25:255-275
24. Fay RA, Norgren R (1997b) Identification of rat brainstem multisynaptic connections to the oral motor nuclei in the rat using pseudorabies virus. II. Facial muscle motor systems. Brain Res Rev 25:276-290
25. Fay RA, Norgren R (1997c) Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudo-rabies virus. III. Lingual muscle motor systems. Brain Res Rev 25:291-311
26. Goldberg LJ, Chandler SH (1990) Central mechanisms of rhythmical trigeminal activity. In: Taylor A (ed) Neurophysiology of the jaws and teeth. MacMillan, London, pp 268-293
27. Gurahian SM, Chandler SH, Goldberg LJ (1989) Intracellular analysis of trigeminal motoneuron rhythmical activity during stimulation of pontomedullary reticular formation in anesthetized guinea pig. J Neurophysiol 62:1225-1236
28. Haartsen AB (1962) Cortical projections to mesencephalon, pons, medulla oblongata and spinal cord. An experimental study in the goat and the rabbit. PhD Thesis, Eduard Ijdo, NV, Leiden
29. Harris JA (1998) Using c-fos as a neural marker of pain. Brain Res Bull 45:1-8
30. Herdegen T, Leah JD (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Rev 28:370-490
31. Herrera DG, Robertson HA (1996) Activation of c-Fos in the brain. Prog Neurobiol 50:83-107
32. Hiraba K, Taira M, Sahara Y, Nakamura Y (1988) Single-unit activity in bulbar reticular formation during food ingestion in chronic cats. J Neurophysiol 60:1333-1349
33. Howe PRC, Moon E, Dampney RAL (1983) Distribution of serotonin nerve cells in the rabbit brainstem. Neurosci Letters 38:125-130
34. Hsiao CF, Del Negro CA, Trueblood PR, Chandler SH (1998) Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79:2847-2856
35. Hsiao CF, Chandler SH (2003) Discharge characteristics and membrane properties of interneurons in the rat supratrigeminal motor nucleus. Soc Neurosci Abstr 33:499:1
36. Huang A, Noga BR, Carr PA, Fedirchuk B, Jordan LM (2000) Spinal cholinergic neurons activated during locomotion: localization and electrophysiological characterization. J Neurophysiol 83:3537-3547
37. Hunt SP, Pini A, Evan G (1987) Induction of c-Fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634
38. Inoue T, Masuda Y, Nagashima T, Yoshikawa K, Morimoto T (1992) Properties of rhythmically active reticular neurons around the trigeminal motor nucleus during fictive mastication in the rat. Neurosci Res 14:275-294
39. Inoue T, Chandler SH, Goldberg LJ (1994) Neuropharmacological mechanisms underlying rhythmical discharge in trigeminal interneurons during fictive mastication. J Neurophysiol 71:2061-2073
40. Inoue M, Nozawa-Inoue K, Donga R, Yamada Y (2002) Convergence of selected inputs from sensory afferents to trigeminal premotor neurons with possible projections to masseter motoneurons in the rabbit. Brain Res 957:183-191
41. Jacquin MF, Semba K, Rhoades RW, Egger MD (1982) Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vasal nuclei. Brain Res 246:285-291
42. Jacquin MF, Chiaia NL, Haring JH, Rhoades RW (1990) Intersubnuclear connections within the rat trigeminal brainstem complex. Somatosens Mot Res 7:399-420
43. Jacquin MF, Rhoades RW (1990) Cell structure and response properties in the trigeminal subnucleus oralis. Somatosens Mot Res 7:265-288
44. Jacquin TD, Borday V, Schneider-Maunoury S, Topilko P, Ghilini G, Kato F, Charnay P, Champagnat J (1996) Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17:747-758
45. Julien C, Rossignol S (1982) Electroneurographic recordings with polymer cuff electrodes in paralyzed cats. J Neurosci Methods 5:267-272
46. 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
47. Katakura N, Chandler SH (1990) An iontophoretic analysis of the pharmacologic mechanisms responsible for trigeminal motoneuronal discharge during masticatory-like activity in the guinea pig. J Neurophysiol 63:356-369
48. Kiehn O, Kjaerulff O (1998) Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 860:110-129
49. Kogo M, Funk GD, Chandler SH (1996) Rhythmical oral-motor activity recorded in an in vitro brainstem preparation. Somatosens Motor Res 13:39-48
50. Kolta A (1997) In vitro investigation of synaptic relations between interneurons surrounding the trigeminal motor nucleus and masseteric motoneurons. J Neurophysiol 78:1720-1725
51. 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
52. Kovács KJ (1998) c-Fos as a transcriptional factor: a stressful (re)view from a functional map. Neurochem Int 33:287-297
53. Landgren S, Olsson KÅ (1976) Localization of evoked potentials in the digastric, masseteric, supra- and intertrigeminal subnuclei of the cat. Exp Brain Res 26:299-318
54. Landgren S, Olsson KÅ, Westberg KG (1986) Bulbar neurones with axonal projections to the trigeminal motor nucleus in the cat. Exp Brain Res 65:98-111
55. Li JL, Kaneko T, Nomura S, Mizuno N (1998) Projections from the caudal spinal trigeminal nucleus to commissural interneurons in the supratrigeminal region: an electron microscope study in the rat. Neurosci Lett 254:57-60
56. Li YQ, 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
57. Liu ZJ, Masuda Y, Inoue T, Fuchihata H, Sumida A, Takada K, Morimoto T (1993) Coordination of cortically induced rhythmic jaw and tongue movements in the rabbit. J Neurophysiol 69:569-584
58. Lund JP, Sasamoto K, Murakami T, Olsson KÅ (1984). Analysis of rhythmical jaw movements produced by electrical stimulation of motor-sensory cortex of rabbits. J Neurophysiol 52:1014-1029
59. Lund JP (1991) Mastication and its control by the brain stem. Crit Rev Oral Biol Med 2:33-64
60. Lund JP, Kolta A, Westberg KG, Scott G (1998) Brainstem mechanisms underlying feeding behaviours. Curr Opin Neurobiol 8:718-724
61. Ma J, Novikov LN, Wiberg M, Kellerth JO (2001) Delayed loss ofspinal motoneurons after peripheral nerve injury in adult rats: a quantitative morphological study. Exp Brain Res 139:216-223
62. Maggi CA, Meli A (1986) Suitability of urethane anesthesia for physiopharmacological investigations in various systems. Part 1: general considerations. Experientia 42:109-114
63. Marfurt CF (1981) The central projections of trigeminal primary afferent neurons in the cat as determined by the tranganglionic transport of horseradish peroxidase. J Comp Neurol 203:785-798
64. Marfurt CF, Rajchert DM (1991) Trigeminal primary afferent projections to "non-trigeminal" areas of the rat central nervous system. J Comp Neurol 303:489-511
65. Matsutani K, Tsuruoka M, Shinya A, Furuya R, Kawawa T, Inoue T (2003) Coeruleotrigeminal suppression of nociceptive sensorimotor function during inflammation in the craniofacial region of the rat. Brain Res Bull 61:73-80
66. McBride RL, Sutin J (1984) Noradrenergic hyperinnervation of the trigeminal sensory nuclei. Brain Res 324:211-221
67. Meessen H, Olszewski J (1949) Cytoarchitektonischer Atlas des Rautenhirns des Kaninchens. Karger, Basel
68. Min MY, Hsu PC, Yang HW (2003) The physiological and morphological characteristics of interneurons caudal to the trigeminal motor nucleus in rats. Eur J Neurosci 18:2981-2998
69. Mizuno N (1970) Projection fibers from the main sensory trigeminal nucleus and the supratrigeminal region. J Comp Neurol 139:457-471
70. 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
71. Morgan JI, Curran T (1991) Stimulus-transcription coupling in the central nervous system: involvement of the inducible protooncogenes Fos and jun. Ann Rev Neurosci 14:421-451
72. Moriyama Y (1987) Rhythmical jaw movements and lateral pontomedullary reticular neurons in rats. Comp Biochem Physiol A 86:7-14
73. Nakamura Y, Katakura N (1995) Generation of masticatory rhythm in the brainstem. Neurosci Res 23:1-19
74. Nakamura Y, Katakura N, Nakajima M (1999) Generation of rhythmical ingestive activities of the trigeminal, facial, and hypoglossal motoneurons in in vitro CNS preparations isolated from rats and mice. J Med Dent Sci 46:63-73
75. Nakamura Y, Katakura N, Nakajima M, Liu J (2004) Rhythm generation for food-ingestive movements. Prog Brain Res 143:97-103
76. Nozaki S, Enomoto S, Nakamura Y ( 1983) Identification and input-output properties of bulbar reticular neurons involved in the cerebral cortical control of trigeminal motoneurons in cats. Exp Brain Res 49:363-372
77. Nozaki S, Iriki A, Nakamura Y (1986a) Localization of central rhythm generator involved in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. J Neurophysiol 55:806-825
78. Nozaki S, Iriki A, Nakamura Y (1986b) Role of corticobulbar projection neurons in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. J Neurophysiol 55:826-845
79. Nozaki S, Iriki A, Nakamura Y (1993) Trigeminal premotor neurons in the bulbar parvocellular reticular formation participating in induction of rhythmical activity of trigeminal motoneurons by repetitive stimulation of the cerebral cortex in the guinea pig. J Neurophysiol 69:595-608
80. Olsson KÅ, Sasamoto K, Lund JP (1986a) Modulation of transmission in rostral trigeminal sensory nuclei during chewing. J Neurophysiol 55:56-75
81. Olsson KÅ, Landgren S, Westberg KG (1986b) Location of, and peripheral convergence on, the interneuron in the disynaptic path from the coronal gyrus of the cerebral cortex to the trigeminal motorneurons in the cat. Exp Brain Res 65:83-97
82. Olsson KÅ, Westberg KG (1991) Integration in trigeminal premotor interneurones in the cat. 2. Functional characteristics of neurones in the subnucleus-gamma of the oral nucleus of the spinal trigeminal tract with a projection to the digastric motoneurone subnucleus. Exp Brain Res 84:115-124
83. Onimaru H, Homma I (2003) A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J Neurosci 23:1478-1486
84. Ro JY, Harriott A, Crouse U, Capra NF (2003) Innocuous jaw movements increase c-Fos expression in trigeminal sensory nuclei produced by masseter muscle inflammation. Pain 104:539-548
85. Rocha MJA, Herbert H (1997) Effects of anesthetics on Fos protein expression in autonomie brain nuclei related to cardiovascular regulation. Neuropharmacology 36:1779-1781
86. Sagar SM, Sharp FR, Curran T (1988) Expression of c-Fos protein in the brain: metabolic mapping at the cellular level. Science 240:1328-1331
87. Sandler VM, Puil E, Schwarz DW (1998) Intrinsic response properties of bursting neurons in the nucleus principalis trigemini of the gerbil. Neuroscience 83:891-904
88. Schwartz G, Enomoto S, Valiquette C, Lund JP (1989) Mastication in the rabbit: a description of movement and muscle activity. J Neurophysiol 62:273-287
89. Scott G, Westberg KG, Vrentzos N, Kolta A, Lund JP (2003) Effect of lidocaine and NMDA injections into the medial pontobulbar reticular formation on mastication evoked by cortical stimulation in anaesthetized rabbits. Eur J Neurosci 17:2156-2162
90. Shigenaga Y, Okamoto T, Nishimori T, Suemune S, Nasution ID, Chen IC, Tsuru K, Yoshida A, Tabuchi K, Hosoi M, Tsuru H (1986) Oral and facial representation in the trigeminal principal and rostral spinal nuclei of the cat. J Comp Neurol 244(1):1-18
91. Shigenaga Y, Yoshida A, Mitsuhiro Y, Tsuru K, Doe K (1988) Morphological and functional properties of trigeminal nucleus oralis neurons projecting to the trigeminal motor nucleus of the cat. Brain Res 461:143-149
92. Smith JC, Morrison DE, Ellenberger HH, Otto MR, Feldman JL (1989) Brain stem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 281:69-96
93. Steinbusch HW (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618
94. Sugimoto T, He YF, Xiao C, Ichikawa H (1998) c-Fos induction in the subnucleus oralis following trigeminal nerve stimulation. Brain Res 783:158-162
95. Sunada T, Kurasawa I, Hirose Y, Nakamura Y (1990) Intracellular response properties of neurons in the spinal trigeminal nucleus to peripheral and cortical stimulation in the cat. Brain Res 514:189-197
96. Takada M, Itoh K, Yasui Y, Mitani A, Nomura S, Mizuno N (1984) Distribution of premotor neurons for the hypoglossal nucleus in the cat. Neurosci Lett 52:141-146
97. Takemura M, Shimada T, Sugiyo S, Nokubi T, Shigenaga Y (2000) Mapping of c-Fos in the trigeminal sensory nucleus following high and low-intensity afferent stimulation in the rat. Exp Brain Res 130:113-123
98. Tanaka S, Kogo M, Chandler SH, Matsuya T (1999) Localization of oral-motor rhythmogenic circuits in the isolated rat brainstem preparation. Brain Res 821:190-199
99. Tsuboi A, Kolta A, Chen CC, Lund JP (2003) Neurons of the trigeminal main sensory nucleus participate in the generation of rhythmic motor patterns. Eur J Neurosci 17:229-238
100. Turman JE, Chandler SH (1994a) Immunohistochemical evidence for GABA and glycine-containing trigeminal premotoneurons in the guinea pig. Synapse 18:7-20
101. Turman JE, Chandler SH (1994b) Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons. Brain Res 634:49-61
102. Turman JE, Chopiuk NB, Shuler CF (2001) The Krox-20 null mutation differentially affects the development of masticatory muscles. Dev Neurosci 23:113-121
103. Veasey SC, Fornal CA, Metzler CW, Jacobs BL (1995) Response of serotonergic caudal raphe neurons in relation to specific motor activities in freely moving cats. J Neurosci 15:5346-5359
104. Voisin DL, Domejean-Orliaguet S, Chalus M, Dallel R, Woda A (2002) Ascending connections from the caudal part to the oral part of the spinal trigeminal nucleus in the rat. Neuroscience 109:183-193
105. Vornov JJ, Sutin J (1983) Brainstem projections to the normal and noradrenergically hyperinnervated trigeminal motor nucleus. J Comp Neurol 214:198-208
106. 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
107. Westberg KG, Sandström G, Olsson KÅ (1995) Integration in trigeminal premotor interneurons 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 motorneurone subnucleus. Exp Brain Res 104:449-461
108. Westberg KG, Clavelou P, Sandström 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
109. Westberg KG, Scott G, Olsson KA, Lund JP (2001) Discharge patterns of neurons in the medial pontobulbar reticular formation during fictive mastication in the rabbit. Eur J Neurosci 14:1709-1718
110. Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1989) Sensory and motor responses of trigeminal and reticular neurons during ingestive behavior in rats. Exp Brain Res 76:386-400
111. Yoshida A, Fukami H, Nagase Y, Appenteng K, Honma S, Zhang LF, Bae YC, Shigenaga Y (2001) Quantitative analysis of synaptic contacts made between functionally identified oralis neurons and trigeminal motoneurons in cats. J Neurosci 21:6298-6307
112. Zerari-Mailly F, Pinganaud G, Dauvergne C, Buisseret P, Buisseret-Delmas C (2001) Trigemino-reticulo-facial and trigemino-reticulo-hypoglossal pathways in the rat. J Comp Neurol 429:80-93
113. Zhang J, Luo P (2003) Ultrastructural features of synapse from dorsal parvocellular reticular formation neurons to hypoglossal motoneurons of the rat. Brain Res 963:262-273
114. Zimmerman EA, Chambers WW, Liu CN (1964) An experimental study of the anatomical organization of the corticobulbar system in the albino rat. J Comp Neurol 123:301-323