Ultrastructure and synaptology of the paratrigeminal nucleus in the rat: Primary pharyngeal and laryngeal afferent projections

Synapse

Volumn 59, Issue 4, 2006, Pages 220-234

  Saxon, Dale W ^a   Hopkins, David A ^b,c  

^a Indiana University School of Medicine Evansville   (United States)

^b DALHOUSIE UNIVERSITY   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Aerodigestive tract; Lamina I II; Medullary dorsal horn; Orofacial; Transganglionic

Indexed keywords

ANIMAL ANATOMY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL SHAPE; DENDRITE; DIGESTIVE SYSTEM; LARYNX; MALE; MICROSCOPY; MUSCLE SPINDLE AFFERENT NERVE; NERVE ENDING; NERVE PROJECTION; NEUROANATOMY; NISSL SUBSTANCE; NONHUMAN; PARATRIGEMINAL NUCLEUS; PHARYNX; PRIORITY JOURNAL; RAT; RAT STRAIN; ROUGH ENDOPLASMIC RETICULUM; SPINAL CORD DORSAL HORN; SYNAPTIC TRANSMISSION; ULTRASTRUCTURE;

AFFERENT PATHWAYS; ANIMALS; IMMUNOHISTOCHEMISTRY; LARYNGEAL NERVES; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PHARYNX; RATS; RATS, WISTAR; SYNAPSES; TRIGEMINAL NUCLEUS, SPINAL;

EID: 32044442765     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20233     Document Type: Article

References (78)

1. Abrahams VC, Richmond FJ, Keane J. 1984. Projections from C2 and C3 nerves supplying muscles and skin of the cat neck: a study using transganglionic transport of horseradish peroxidase. J Comp Neurol 230:142-154.
2. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. 1989. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248-268.
3. Armstrong CL, Hopkins DA. 1998. Neurochemical organization of paratrigeminal nucleus projections to the dorsal vagal complex in the rat. Brain Res 785:49-57.
4. Arvidsson J, Pfaller K. 1990. Central projections of C4-C8 dorsal root ganglia in the rat studied by anterograde transport of WGA-HRP. J Comp Neurol 292:349-362.
5. Arvidsson J, Thomander L. 1984. An HRP study of the central course of sensory intermediate and vagal fibers in peripheral facial nerve branches in the cat. J Comp Neurol 223:35-45.
6. Bae YC, Ahn HJ, Park KP, Kim HN, Paik SK, Bae JY, Lee HW, Kim KH, Yoshida A, Moritani M, Shigenaga Y. 2005. 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, 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.
8. Bae YC, Oh JM, Hwang SJ, Shigenaga Y, Valtschanoff JG. 2004a. Expression of vanilloid receptor TRPV1 in the rat trigeminal sensory nuclei. J Comp Neurol 478:62-71.
9. Bae YC, Paik SK, Park KP, Ma SK, Jin JG, Ahn DK, Kim SK, Moritani M, Yoshida A. 2004b. Quantitative analysis of tooth pulp afferent terminals in the rat brain stem. Neuroreport 15:2485-2489.
10. Bieger D, Hopkins DA. 1987. Viscerotopic representation of the upper alimentary tract in the medulla oblongata in the rat: the nucleus ambiguus. J Comp Neurol 262:546-562.
11. Bon K, Lanteri-Minet M, de Pommery J, Michiels JF, Menétrey D. 1997. Cyclophosphamide cystitis as a model of visceral pain in rats: minor effects at mesodiencephalic levels as revealed by the expression of c-fos, with a note on Krox-24. Exp Brain Res 113:249-264.
12. Boucher Y, Simons CT, Cuellar JM, Jung SW, Carstens MI, Carstens E. 2003. Activation of brain stem neurons by irritant chemical stimulation of the throat assessed by c-fos immunohistochemistry. Exp Brain Res 148:211-218.
13. Bourgeais L, Gauriau C, Monconduit L, Villanueva L, Bernard JF. 2003. Dendritic domains of nociceptive-responsive parabrachial neurons match terminal fields of lamina I neurons in the rat. J Comp Neurol 464:238-256.
14. Bradley RM, Mistretta CM, Bates CA, Killackey HP. 1985. Transganglionic transport of HRP from the circumvallate papilla of the rat. Brain Res 361:154-161.
15. Burton H, Craig AD, Jr. 1979. Distribution of trigeminothalamic projection cells in cat and monkey. Brain Res 161:515-521.
16. Burton H, Craig AD, Jr., Poulos DA, Molt JT. 1979. Efferent projections from temperature sensitive recording loci within the marginal zone of the nucleus caudalis of the spinal trigeminal complex in the cat. J Comp Neurol 183:753-777.
17. Cajal SR. 1909. Histologic du Système Nerveux de l'Homme et des Vertébrés. Madrid: Instituto de Ramón y Cajal, (reprint 1972).
18. Cechetto DF, Standaert DG, Saper CB. 1985. Spinal and trigeminal dorsal horn projections to the parabrachial nucleus in the rat. J Comp Neurol 240:153-160.
19. Chan-Palay V. 1978a. The para trigeminal nucleus. I. Neurons and synaptic organization. J Neurocytol 7:405-418.
20. Chan-Palay V. 1978b. The paratrigeminal nucleus. II. Identification and inter-relations of catecholamine axons, indoleamine axons, and substance P immunoreactive cells in the neuropil. J Neurocytol 7:419-442.
21. Contreras RJ, Beckstead RM, Norgren R. 1982. The central projections of the trigeminal, facial, glossopharyngeal and vagus nerves: an autoradiographic study in the rat. J Auton Nerv Syst 6:303-322.
22. Craig AD, Jr., Burton H. 1981. Spinal and medullary lamina I projection to nucleus submedius in medial thalamus: a possible pain center. J Neurophysiol 45:443-466.
23. Dutschmann M, Herbert H. 1997. Fos expression in the rat parabrachial and Kolliker-Fuse nuclei after electrical stimulation of the trigeminal ethmoidal nerve and water stimulation of the nasal mucosa. Exp Brain Res 117:97-110.
24. Famiglietti EV, Jr. 1970. Dendro-dendritic synapses in the lateral geniculate nucleus of the cat. Brain Res 20:181-191.
25. Famiglietti EV, Jr., Peters A. 1972. The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 144:285-334.
26. Gobel S. 1976. Dendroaxonic synapses in the substantia gelatinosa glomeruli of the spinal trigeminal nucleus of the cat. J Comp Neurol 167:165-176.
27. Gobel S. 1978. Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis). J Comp Neurol 180:395-413.
28. Gobel S, Hockfield S. 1977. An anatomical analysis of the synaptic circuitry of layers I, II and III of trigeminal nucleus pars caudalis in the cat. In: Anderson DJ, Matthews B, editors. Pain in the Trigeminal Region. Amsterdam: Elsevier/North Holland, p 203-211.
29. Granum SL. 1986. The spinothalamic system of the rat. I. Locations of cells of origin. J Comp Neurol 247:159-180.
30. Gray EG. 1969. Electron microscopy of excitatory and inhibitory synapses: a brief review. Prog Brain Res 31:141-155.
31. Hamilton RB, Norgren R. 1984. Central projections of gustatory nerves in the rat. J Comp Neurol 222:560-577.
32. Hanamori T, Smith DV. 1989. Gustatory innervation in the rabbit: central distribution of sensory and motor components of the chorda tympani, glossopharyngeal, and superior laryngeal nerves. J Comp Neurol 282:1-14.
33. Harding BN. 1971. Dendro-dendritic synapses, including reciprocal synapses, in the ventrolateral nucleus of the monkey thalamus. Brain Res 34:181-185.
34. Hayakawa T, Takanaga A, Tanaka K, Maeda S, Seki M. 2003. Ultrastructure of the central subnucleus of the nucleus tractus solitarii and the esophageal afferent terminals in the rat. Anat Embryol (Berl) 206:273-281.
35. Housley GD, Martin-Body RL, Dawson NJ, Sinclair JD. 1987. Brain stem projections of the glossopharyngeal nerve and its carotid sinus branch in the rat. Neuroscience 22:237-250.
36. Imbe H, Ren K. 1999. Orofacial deep and cutaneous tissue inflammation differentially upregulates preprodynorphin mRNA in the trigeminal and paratrigeminal nuclei of the rat. Brain Res Mol Brain Res 67:87-97.
37. Jones EG, Powell TP. 1969. Electron microscopy of synaptic glomeruli in the thalamic relay nuclei of the cat. Proc R Soc Lond B Biol Sci 172:153-171.
38. Kalia M, Sullivan JM. 1982. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248-265.
39. Kerr FWL. 1966. The ultrastructure of the spinal tract of the trigeminal nerve and the substantia gelatinosa. Exp Neurol 16:359-376.
40. Kerr FWL. 1970a. The fine structure of the subnucleus caudalis of the trigeminal nerve. Brain Res 23:129-145.
41. Kerr FWL. 1970b. The organization of primary afferents in the subnucleus caudalis of the trigeminal: a light and electron microscopic study of degeneration. Brain Res 23:147-165.
42. Kilduff TS, Heller HC, Sharp FR. 1984. Paratrigeminal nucleus: a previously unrecognized thermal relay? In: Hales JRS, editor. Thermal Physiology. New York: Raven, p 101-104.
43. Kilduff TS, Miller JD, Radeke CM, Sharp FR, Heller HC. 1990. 14C-2-deoxyglucose uptake in the ground squirrel brain during entrance to and arousal from hibernation. J Neurosci 10:2463-2475.
44. Lapa RC, Watanabe I. 2005. Synaptic contacts established by inferior alveolar nerve fibres in the paratrigeminal nucleus: an electron microscopic study in the rat. Arch Oral Biol 50:73-79.
45. Lieberman AR, Webster KE. 1974. Aspects of the synaptic organization of intrinsic neurons in the dorsal lateral geniculate nucleus. An ultrastructural study of the normal and of the experimentally deafferented nucleus in the rat. J Neurocytol 3:677-710.
46. Leslie RA, Gwyn DG, Hopkins DA. 1982. The ultrastructure of the subnucleus gelatinosus of the nucleus of the tractus solitarius in the cat. J Comp Neurol 206:109-118.
47. Lindsey CJ, Buck HS, Fior-Chadi DR, Lapa RC. 1997. Presser effect mediated by bradykinin in the paratrigeminal nucleus of the rat. J Physiol (Lond) 502:119-129.
48. Ma WL, Zhang WB, Feng G, Cai YL. 2005. Calbindin D28k-containing neurons in the paratrigeminal nucleus receive convergent nociceptive information and project to nucleus of the solitary tract in rat. Brain Res 1038:132-140.
49. 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.
50. Marfurt CF, Zaleski EM, Adams CE, Weither CL. 1986. Sympathetic nerve fibers in rat orofacial and cerebral tissues as revealed by the HRP-WGA tracing technique: a light and electron microscopic study. Brain Res 366:373-378.
51. Menétrey D, Basbaum AI. 1987. Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J Comp Neurol 255:439-450.
52. Menétrey D, Leah J, de Pommery J. 1987. Efferent projections of the paratrigeminal nucleus in the rat. Neurosci Lett 73:48-52.
53. Merest DK. 1971. Dendrodendritic synapses of cells that have axons: the fine structure of the Golgi type II cell in the medial geniculate body of the cat. Z Anat Entwicklungs-Gesch 133:216-246.
54. Mrini A, Jean A. 1995. Synaptic organization of the interstitial subdivision of the nucleus tractus solitarii and of its laryngeal afferents in the rat. J Comp Neurol 355:221-236.
55. Neuhuber WL, Zenker W. 1989. Central distribution of cervical primary afferents in the rat, with emphasis on proprioceptive projections to vestibular, perihypoglossal, and upper thoracic spinal nuclei. J Comp Neurol 280:231-253.
56. Nishimori T, Sera M, Suemune S, Yoshida A, Tsuru K, Tsuiki Y, Akisaka T, Okamoto T, Dateoka Y, Shigenaga Y. 1986. The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei. Brain Res 372:375-381.
57. Nomura S, Mizuno N. 1982. Central distribution of afferent and efferent components of the glossopharyngeal nerve: an HRP study in the cat. Brain Res 236:1-13.
58. Panneton WM. 1991. Primary afferent projections from the upper respiratory tract in the muskrat. J Comp Neurol 308:51-65.
59. Panneton WM, Burton H. 1981. Corneal and periocular representation within the trigeminal sensory complex in the cat studied with transganglionic transport of horseradish peroxidase. J Comp Neurol 199:327-344.
60. Panneton WM, Burton H. 1985. Projections from the paratrigeminal nucleus and the medullary and spinal dorsal horns to the peribrachial area in the cat. Neuroscience 15:779-797.
61. Panneton WM, Hopkins DA. 1999. The paratrigeminal nucleus: the interface between somatic and visceral sensory systems. Proc Soc Neurosci 25:401.
62. Panneton WM, Loewy AD. 1980. Projections of the carotid sinus nerve to the nucleus of the solitary tract in the cat. Brain Res 191:239-244.
63. Peters A, Palay SL, Webster H de F. 1991. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells. New York: Oxford University Press.
64. Pfaller K, Arvidsson J. 1988. 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 Comp Neurol 268:91-108.
65. Phelan KD, Falls WM. 1989. The interstitial system of the spinal trigeminal tract in the rat: anatomical evidence for morphological and functional heterogeneity. Somatosens Mot Res 6:367-399.
66. Ralston HJ, 3rd. 1971. Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature 230:585-587.
67. Ribeiro-da-Silva A, Pignatelli D, Coimbra A. 1985. Synaptic architecture of glomeruli in superficial dorsal horn of rat spinal cord, as shown in serial reconstructions. J Neurocytol 14:203-220.
68. Saxon DW, Hopkins DA. 1998. Efferent and collateral organization of paratrigeminal nucleus projections: an anterograde and retrograde fluorescent tracer study in the rat. J Comp Neurol 402:93-110.
69. Shigenaga Y, Chen IC, Suemune S, Nishimori T, Nasution ID, Yoshida A, Sato H, Okamoto T, Sera M, Hosoi M. 1986. Oral and facial representation within the medullary and upper cervical dorsal horns in the cat. J Comp Neurol 243:388-408.
70. Shigenaga Y, Sera M, Nishimori T, Suemune S, Nishimura M, Yoshida A, Tsuru K. 1988. The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 268:489-507.
71. Shults RC. 1992. Nociceptive neural organization in the trigeminal nucleus. In:Light AR, editor. The Initial Processing of Pain and its Descending Control: Spinal and Trigeminal Systems. Basel: Karger.
72. Shults RC, Light AR, Donaghy S. 1985. Interstitial nucleus of the spinal trigeminal tract: a specific nociceptive relay for oral and peri-oral structures. Proc Soc Neurosci 11:578.
73. South EH, Ritter RC. 1986. Substance P-containing trigeminal sensory neurons project to the nucleus of the solitary tract. Brain Res 372:283-289.
74. Sugimoto T, Fujiyoshi Y, Xiao C, He YF, Ichikawa H. 1997. Central projection of calcitonin gene-related peptide (CGRP)- and substance P (SP)-immunoreactive trigeminal primary neurons in the rat. J Comp Neurol 378:425-442.
75. Sweazey RD, Bradley RM. 1986. Central connections of the lingual-tonsillar branch of the glossopharyngeal nerve and the superior laryngeal nerve in lamb. J Comp Neurol 245:471-482.
76. Torvik A. 1956. Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures; an experimental study in the rat. J Comp Neurol 106:51-141.
77. Uchizono K. 1965. Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature 207:642-643.
78. Zhu CG, Sandri C, Akert K. 1981. Morphological identification of axo-axonic and dendro-dendritic synapses in the rat substantia gelatinosa. Brain Res 230:25-40.