Trigeminal projections on gustatory neurons of the nucleus of the solitary tract: A double-label strategy using electrical stimulation of the chorda tympani and tracer injection in the lingual nerve

Brain Research

Volumn 1288, Issue , 2009, Pages 60-68

  Felizardo, Rufino ^a   Boucher, Yves ^a   Braud, Adeline ^a   Carstens, Earl ^b   Dauvergne, Céline ^a   Zerari Mailly, Fawzia ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anterograde labelling; Fos protein; Gustatory afferents; Immunocytochemistry; NST; Oral afferents

Indexed keywords

BIOTINYLATED DEXTRAN AMINE; DEXTRAN DERIVATIVE; TRACER; TRANSCRIPTION FACTOR FRA 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CHORDA TYMPANI; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROSTIMULATION; GUSTATORY NERVOUS SYSTEM; HISTOLOGY; IMMUNOREACTIVITY; LINGUAL NERVE; MALE; NERVE PROJECTION; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS; SYNAPSE; TASTE; TRIGEMINAL NERVE;

ANIMALS; CHORDA TYMPANI NERVE; ELECTRIC STIMULATION; IMMUNOHISTOCHEMISTRY; LINGUAL NERVE; MALE; NEURONS, AFFERENT; PROTO-ONCOGENE PROTEINS C-FOS; RATS; SOLITARY NUCLEUS; STAINING AND LABELING; TRIGEMINAL NERVE;

ANIMALIA; CHORDA; CRICETINAE; RATTUS;

EID: 69049112713     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.07.002     Document Type: Article

References (56)

1. Astrom K.E. The central course of afferent fibers in the trigeminal, facial, glossopharyngeal and vagal nerves and their nuclei in the mouse. Acta Physiol. Scand. 29 (1953) 209-320
2. Beckstead R.M., and Norgren R. An autoradiographic examination of the central distribution of the trigeminal, facial, glossopharyngeal, and vagal nerves in the monkey. J. Comp. Neurol. 190 (1979) 259-282
3. Berridge K.C., and Fentress J.C. Trigeminal-taste interaction in palatability processing. Science 228 (1985) 747-750
4. Boucher Y., Simons C.T., Faurion A., Azerad J., and Carstens E. Trigeminal modulation of gustatory neurons in the nucleus of the solitary tract. Brain Res. 973 (2003) 265-274
5. Boucher Y., Simons C.T., Cuellar J.M., Jung S.W., Carstens M.I., and Carstens E. Activation of brain stem neurons by irritant chemical stimulation of the throat assessed by c-fos immunohistochemistry. Exp. Brain Res. 148 (2003) 211-218
6. Boucher Y., Berteretche MV., Farhang F., Arvy MP., Azerad J., and Faurion A. Taste deficits related to dental deafferentation: an electrogustometric study in humans. Eur. J. Oral Sci. 114 (2006) 456-464
7. Cerf-Ducastel B., Van de Moortele P.F., MacLeod P., Le Bihan D., and Faurion A. Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chem. Senses 26 (2001) 371-383
8. Contreras R.J., Beckstead R.M., and Norgren R. The central projections of the trigeminal, facial, glossopharyngeal and vagus nerves: an autoradiographic study in the rat. J. Auton. Nerv. Syst. 6 (1982) 303-322
9. Danilova V., Danilov Y., Roberts T., Elmer D., and Hellekant G. Methods in chemosensory research. In: Simon S.A., and Nicolelis M.A.L. (Eds). CRC Press (2002) 247-248
10. Davis B.J. Synaptic relationships between the chorda tympani and tyrosine hydroxylase-immunoreactive dendritic processes in the gustatory zone of the nucleus of the solitary tract in the hamster. J. Comp. Neurol. 392 (1998) 78-91
11. De Chazeron I., Raboisson P., and Dallel R. Organization of diencephalic projections from the spinal trigeminal nucleus oralis: an anterograde tracing study in the rat. Neuroscience 127 (2004) 921-928
12. DiNardo L.A., and Travers J.B. Distribution of fos-like immunoreactivity in the medullary reticular formation of the rat after gustatory elicited ingestion and rejection behaviors. J. Neurosci. 17 (1997) 3826-3839
13. Dragunow M., and Faull R. The use of c-fos as a metabolic marker in neuronal pathway tracing. J. Neurosci. Methods 29 (1989) 261-265
14. Faurion A. Sensory interactions through neural pathways. Physiol. Behav. 89 (2006) 44-46
15. Faurion A., Cerf B., Le Bihan D., and Pillias A.M. fMRI study of taste cortical areas in humans. Ann. N. Y. Acad. Sci. 30 (1998) 535-545
16. Finger T. Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallate papilla of the rat. Chem. Senses 11 (1986) 135-144
17. Friauf E. C-fos immunocytochemical evidence for acoustic pathway mapping in rats. Behav. Brain Res. 66 (1995) 217-224
18. Grant R., Ferguson M.M., Strang R., Turner J.W., and Bone I. Evoked taste thresholds in a normal population and the application of electrogustometry to trigeminal nerve disease. J. Neurol. Neurosurg. Psychiatry 50 (1987) 12-21
19. Guthrie K.M., and Gall C.M. Functional mapping of odor-activated neurons in the olfactory bulb. Chem. Senses 20 (1995) 271-282
20. Halpern B.P., and Nelson L.M. Bulbar gustatory responses to anterior and to posterior tongue stimulation in the rat. Am. J. Physiol. 209 (1965) 105-110
21. Halsell C.B., Travers J.B., and Travers S.P. Gustatory and tactile stimulation of the posterior tongue activate overlapping but distinctive regions within the nucleus of the solitary tract. Brain Res. 632 (1993) 161-173
22. Hamilton R.B., and Norgren R. Central projections of gustatory nerves in the rat. J. Comp. Neurol. 222 (1984) 560-577
23. Hanamori T., Kunitake T., Kato K., and Kannan H. Convergence of afferent inputs from the chorda tympani, lingual-tonsillar and pharyngeal branches of the glossopharyngeal nerve, and superior laryngeal nerve on the neurons in the insular cortex in rats. Brain Res. 763 (1997) 267-270
24. Harrer M.I., and Travers S.P. Topographic organization of Fos-like immunoreactivity in the rostral nucleus of the solitary tract evoked by gustatory stimulation with sucrose and quinine. Brain Res. 711 (1996) 125-137
25. Harrison T.A. Tympani nerve stimulation evokes Fos expression in regionally limited neuron populations within the gustatory nucleus of the solitary tract. Brain Res. 904 (2001) 54-66
26. Harrison T.A., and Miller N.W. Fos labeling in the parabrachial nucleus after electrical stimulation of taste nerves in lightly-anesthetized rats. Chem. Senses 19 (1994) 482
27. Hunt S.P., Pini A., and Evan G. Induction of c-Fos-like protein in spinal cord neurons following sensory stimulation. Nature 328 (1987) 632-634
28. Jacquin M.F., Semba K., Rhoades R.W., and Egger M.D. Trigeminal primary afferents project bilaterally to dorsal horn and ipsilaterally to cerebellum, reticular formation, and cuneate, solitary, supratrigeminal and vagal nuclei. Brain Res. 246 (1982) 285-291
29. Jacquin M.F., Semba K., Egger M.D., and Rhoades R.W. Organization of HRP-labeled trigeminal mandibular primary afferent neurons in the rat. J. Comp. Neurol. 215 (1983) 397-420
30. King C.T., Travers S.P., Rowland N.E., Garcea M., and Spector A.C. Glossopharyngeal nerve transection eliminates quinine-stimulated fos-like immunoreactivity in the nucleus of the solitary tract: implications for a functional topography of gustatory nerve input in rats. J. Neurosci. 19 (1999) 3107-3121
31. King C.T., Deyrup L.D., Dodson S.E., Galvin K.E., Garcea M., and Spector A.C. Effects of gustatory nerve transection and regeneration on quinine-stimulated Fos-like immunoreactivity in the parabrachial nucleus of the rat. J. Comp. Neurol. 465 (2003) 296-308
32. Kinnman E., and Aldskogius H. The role of substance P and calcitonin gene-related peptide containing nerve fibers in maintaining fungiform taste buds in the rat after a chronic chorda tympani nerve injury. Exp. Neurol. 113 (1991) 85-91
33. Marfurt C.F., and Rajchert D.M. Trigeminal primary afferent projections to "non-trigeminal" areas of the rat central nervous system. J. Comp. Neurol. 303 (1991) 483-511
34. May O.L., and Hill D.L. Gustatory terminal field organization and developmental plasticity in the nucleus of the solitary tract revealed through triple-fluorescence labelling. J. Comp. Neurol. 497 (2006) 658-669
35. May O.L., Erisir A., and Hill D.L. Ultrastructure of primary afferent terminals and synapses in the rat nucleus of the solitary tract: comparison among the greater superficial petrosal, chorda tympani, and glossopharyngeal nerves. J. Comp. Neurol. 502 (2007) 1066-1078
36. McPheeters M., Hettinger T.P., Nuding S.C., Savoy L.D., Whitehead M.C., and Frank M.E. Taste-responsive neurons and their locations in the solitary nucleus of the hamster. Neuroscience 34 (1990) 745-758
37. Menetrey D., and Basbaum A.I. Spinal and trigeminal projections to the nucleus of the solitary tract: a possible substrate for somatovisceral and viscerovisceral reflex activation. J. Comp. Neurol. 255 (1987) 439-450
38. Nagy J.I., Goedert M., Hunt S.P., and Bond A. The nature of the substance P-containing nerve fibres in taste papillae of the rat tongue. Neuroscience 7 (1982) 3137-3151
39. Nomura T., and Ogawa H. The taste and mechanical response properties of neurons in the parvicellular part of the thalamic posteromedial ventral nucleus of the rat. Neurosci. Res. 3 (1985) 91-105
40. Ogawa H., Imoto T., and Hayama T. Responsiveness of solitario-parabrachial relay neurons to taste and mechanical stimulation applied to the oral cavity in rats. Exp. Brain Res. 54 (1982) 349-358
41. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1986), Academic Press, San Diego
42. Scala A., Checchi L., Montevecchi M., Marini I., and Giamberardino MA. Update on burning mouth syndrome: overview and patient management. Crit. Rev. Oral Biol. Med. 14 (2003) 275-291
43. Simons C.T., Boucher Y., and Carstens E. Suppression of central taste transmission by oral capsaicin. J. Neurosci. 23 (2003) 978-985
44. Streefland C., Farkas E., Maes F.W., and Bohus B. C-fos expression in the brainstem after voluntary ingestion of sucrose in the rat. Neurobiology 4 (1996) 85-102
45. Takayama K., Suzuki T., and Miura M. The comparison of effects of various anesthetics on expression of Fos protein in the rat brain. Neurosci. Lett. 176 (1994) 59-62
46. Takemura M., Tsujio A., Iwase K., Shimada T., and Shigenaga Y. Central terminals of orofacial primary afferents and NADPH-diaphorase activity in the trigemino-solitary complex of rats. Brain Res. 781 (1998) 77-89
47. Travers S.P., and Norgren R. Organization of orosensory responses in the nucleus of the solitary tract of rat. J. Neurophysiol. 73 (1995) 2144-2162
48. Van Buskirk R.L., and Erickson R.P. Odorant responses in taste neurons of the rat NTS. Brain Res. 135 (1977) 287-303
49. Wang Y., Erickson R.P., and Simon S.A. Modulation of rat chorda tympani nerve activity by lingual nerve stimulation. J. Neurophysiol. 73 (1995) 1468-1483
50. Whitehead M.C. Normal architecture of nucleus of solitary tract in hamster. J. Comp. Neurol. 276 (1988) 547-572
51. Whitehead M.C., and Frank M.E. Anatomy of the gustatory system in the hamster: central projections of the chorda tympani and the lingual nerve. J. Comp. Neurol. 220 (1983) 378-395
52. Whitehead M.C., Bergula A., and Holliday K. Forebrain projections to the rostral nucleus of the solitary tract in the hamster. J. Comp. Neurol. 422 (2000) 429-447
53. Yamamoto T., Shimura T., Sako N., Yasoshima Y., and Sakai N. Neural substrates for conditioned taste aversion in the rat. Behav. Brain Res. 65 (1994) 123-137
54. Yamasaki H., Kubota Y., Takagi H., and Tohyama M. Immunoelectron-microscopic study on the fine structure of substance-P-containing fibers in the taste buds of the rat. J. Comp. Neurol. 227 (1984) 380-392
55. Zerari-Mailly F., Dauvergne C., Buisseret P., and Buisseret-Delmas C. Localization of trigeminal, spinal, and reticular neurons involved in the rat blink reflex. J. Comp. Neurol. 467 (2003) 173-184
56. Zerari-Mailly F., Buisseret P., Buisseret-Delmas C., and Nosjean A. Trigemino-solitarii-facial pathway in rats. J. Comp. Neurol. 487 (2005) 176-189