Skip to main content
Top
Published in: Behavioral and Brain Functions 1/2010

Open Access 01-12-2010 | Research

Role of the trigeminal mesencephalic nucleus in rat whisker pad proprioception

Authors: Ombretta Mameli, Stefania Stanzani, Gabriele Mulliri, Rosalia Pellitteri, Marcello A Caria, Antonella Russo, Pierluigi De Riu

Published in: Behavioral and Brain Functions | Issue 1/2010

Login to get access

Abstract

Background

Trigeminal proprioception related to rodent macrovibrissae movements is believed to involve skin receptors on the whisker pad because pad muscles operate without muscle spindles. This study was aimed to investigate in rats whether the trigeminal mesencephalic nucleus (TMnu), which provides proprioceptive feedback for chewing muscles, may be also involved in whisker pad proprioception.

Methods

Two retrograde tracers, Dil and True Blue Chloride, were injected into the mystacial pad and the masseter muscle on the same side of deeply anesthetized rats to label the respective projecting sensory neurons. This double-labeling technique was used to assess the co-innervation of both structures by the trigeminal mesencephalic nucleus (TMnu).
In a separate group of anesthetized animals, the spontaneous electrical activities of TMnu neurons were analyzed by extracellular recordings during spontaneous movements of the macrovibrissae. Mesencephalic neurons (TMne) were previously identified by their responses to masseter muscle stretching. Changes in TMne spontaneous electrical activities, analyzed under baseline conditions and during whisking movements, were statistically evaluated using Student's t-test for paired observations.

Results

Neuroanatomical experiments revealed different subpopulations of trigeminal mesencephalic neurons: i) those innervating the neuromuscular spindles of the masseter muscle, ii) those innervating the mystacial pad, and iii) those innervating both structures. Extracellular recordings made during spontaneous movements of the macrovibrisae showed that whisking neurons similar to those observed in the trigeminal ganglion were located in the TMnu. These neurons had different patterns of activation, which were dependent on the type of spontaneous macrovibrissae movement. In particular, their spiking activity tonically increased during fan-like movements of the vibrissae and showed phasic bursting during rhythmic whisking. Furthermore, the same neurons may also respond to masseter muscle stretch.

Conclusions

results strongly support the hypothesis that the TMnu also contains first-order neurons specialized for relaying spatial information related to whisker movement and location to trigeminal-cortical pathways. In fact, the TMnu projects to second-order trigeminal neurons, thus allowing the rat brain to deduce higher-order information regarding executed movements of the vibrissae by combining touch information carried by trigeminal ganglion neurons with proprioceptive information carried by mesencephalic neurons.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mameli O, Pellitteri R, Russo A, Stanzani S, Caria MA, De Riu PL: Role of trigeminal nerve in regrowth of hypoglossal motoneurons after hypoglossal-facial anastomosis. Acta Oto-Laryngol. 2006, 126: 1334-1338. 10.1080/00016480600801332.CrossRef Mameli O, Pellitteri R, Russo A, Stanzani S, Caria MA, De Riu PL: Role of trigeminal nerve in regrowth of hypoglossal motoneurons after hypoglossal-facial anastomosis. Acta Oto-Laryngol. 2006, 126: 1334-1338. 10.1080/00016480600801332.CrossRef
2.
go back to reference Mameli O, Stanzani S, Russo A, Romeo R, Pellitteri R, Spatuzza M, Caria MA, De Riu PL: Hypoglossal nuclei participation in rat mystacial pad control. Pflügers Arch-Eur J Physiol. 2008, 456: 1189-1198. 10.1007/s00424-008-0472-y.CrossRef Mameli O, Stanzani S, Russo A, Romeo R, Pellitteri R, Spatuzza M, Caria MA, De Riu PL: Hypoglossal nuclei participation in rat mystacial pad control. Pflügers Arch-Eur J Physiol. 2008, 456: 1189-1198. 10.1007/s00424-008-0472-y.CrossRef
3.
go back to reference Mameli O, Stanzani S, Russo A, Pellitteri R, Spatuzza M, Caria MA, Mulliri G, De Riu PL: Hypoglossal nucleus projections to the rat masseter muscle. Brain Res. 2009, 1283: 34-40. 10.1016/j.brainres.2009.06.004.CrossRefPubMed Mameli O, Stanzani S, Russo A, Pellitteri R, Spatuzza M, Caria MA, Mulliri G, De Riu PL: Hypoglossal nucleus projections to the rat masseter muscle. Brain Res. 2009, 1283: 34-40. 10.1016/j.brainres.2009.06.004.CrossRefPubMed
4.
go back to reference Waite PME, Tracey DJ: Trigeminal sensory system. The rat nervous system. Edited by: Paxinos G. 1995, San Diego: Academic Press, 705-724. 2 Waite PME, Tracey DJ: Trigeminal sensory system. The rat nervous system. Edited by: Paxinos G. 1995, San Diego: Academic Press, 705-724. 2
5.
go back to reference Lingenhöhl K, Friauf E: Sensory neurons and motoneurons of the jaw-closing reflex pathway in rats: a combined morphological and physiological study using the intracellular horseradish peroxidase technique. Exp Brain Res. 1991, 83: 385-396. 10.1007/BF00231163.CrossRefPubMed Lingenhöhl K, Friauf E: Sensory neurons and motoneurons of the jaw-closing reflex pathway in rats: a combined morphological and physiological study using the intracellular horseradish peroxidase technique. Exp Brain Res. 1991, 83: 385-396. 10.1007/BF00231163.CrossRefPubMed
6.
go back to reference Clarke WB, Bowsher D: Terminal distribution of primary afferent trigeminal fibers in the rat. Exp Neurol. 1962, 6: 372-383. 10.1016/0014-4886(62)90019-5.CrossRefPubMed Clarke WB, Bowsher D: Terminal distribution of primary afferent trigeminal fibers in the rat. Exp Neurol. 1962, 6: 372-383. 10.1016/0014-4886(62)90019-5.CrossRefPubMed
7.
go back to reference Torvik A: 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. 1956, 106: 51-141. 10.1002/cne.901060104.CrossRefPubMed Torvik A: 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. 1956, 106: 51-141. 10.1002/cne.901060104.CrossRefPubMed
8.
go back to reference Travers JB, Norgren R: Afferent projections to the oral motor nuclei in the rat. J Comp Neurol. 1983, 220: 280-298. 10.1002/cne.902200303.CrossRefPubMed Travers JB, Norgren R: Afferent projections to the oral motor nuclei in the rat. J Comp Neurol. 1983, 220: 280-298. 10.1002/cne.902200303.CrossRefPubMed
9.
go back to reference Travers JB: Oromotor nuclei. The rat nervous system. Edited by: Paxinos G. 1995, San Diego: Academic Press, 239-255. 2 Travers JB: Oromotor nuclei. The rat nervous system. Edited by: Paxinos G. 1995, San Diego: Academic Press, 239-255. 2
10.
go back to reference Szwed M, Bagdasarian K, Ahissar E: Encoding of vibrissal active touch. Neuron. 2003, 40: 621-630. 10.1016/S0896-6273(03)00671-8.CrossRefPubMed Szwed M, Bagdasarian K, Ahissar E: Encoding of vibrissal active touch. Neuron. 2003, 40: 621-630. 10.1016/S0896-6273(03)00671-8.CrossRefPubMed
11.
go back to reference Szwed M, Bagdasarian K, Blumenfeld B, Barak O, Derdikman D, Ahissar E: Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J Neurophysiol. 2006, 95: 791-802. 10.1152/jn.00571.2005.CrossRefPubMed Szwed M, Bagdasarian K, Blumenfeld B, Barak O, Derdikman D, Ahissar E: Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J Neurophysiol. 2006, 95: 791-802. 10.1152/jn.00571.2005.CrossRefPubMed
12.
go back to reference Rice FL, Fundin BT, Pfaller K, Arvidsson J: The innervation of the mystacial pad in the adult rat studied by anterograde transport of HRP conjugates. Exp Brain Res. 1994, 99: 233-246.PubMed Rice FL, Fundin BT, Pfaller K, Arvidsson J: The innervation of the mystacial pad in the adult rat studied by anterograde transport of HRP conjugates. Exp Brain Res. 1994, 99: 233-246.PubMed
13.
go back to reference Lund JP, Olsson KA: The importance of reflexes and their control during jaw movement. Trends in Neurosci. 1983, 6: 458-463. 10.1016/0166-2236(83)90219-9.CrossRef Lund JP, Olsson KA: The importance of reflexes and their control during jaw movement. Trends in Neurosci. 1983, 6: 458-463. 10.1016/0166-2236(83)90219-9.CrossRef
14.
go back to reference Brecht M, Preilowski B, Merzenich MM: Functional architecture of the mystacial vibrissae. Behav Brain Res. 1997, 84: 81-97. 10.1016/S0166-4328(97)83328-1.CrossRefPubMed Brecht M, Preilowski B, Merzenich MM: Functional architecture of the mystacial vibrissae. Behav Brain Res. 1997, 84: 81-97. 10.1016/S0166-4328(97)83328-1.CrossRefPubMed
15.
go back to reference Kleinfeld D, Berg RW, O'Connor SM: Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens & Motor Res. 1999, 16: 69-88.CrossRef Kleinfeld D, Berg RW, O'Connor SM: Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens & Motor Res. 1999, 16: 69-88.CrossRef
16.
go back to reference Dörfl J: The innervation of the mystacial region of the white mouse. A topographical study. J Anat. 1985, 142: 173-184.PubMedCentralPubMed Dörfl J: The innervation of the mystacial region of the white mouse. A topographical study. J Anat. 1985, 142: 173-184.PubMedCentralPubMed
17.
go back to reference Erzurumlu RS, Killackey HP: Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat. J Comp Neurol. 1979, 188: 75-86. 10.1002/cne.901880107.CrossRefPubMed Erzurumlu RS, Killackey HP: Efferent connections of the brainstem trigeminal complex with the facial nucleus of the rat. J Comp Neurol. 1979, 188: 75-86. 10.1002/cne.901880107.CrossRefPubMed
18.
go back to reference Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1997, New York, London, Sydney, Tokyo, Toronto, San Diego: Academic Press, Inc Paxinos G, Watson C: The rat brain in stereotaxic coordinates. 1997, New York, London, Sydney, Tokyo, Toronto, San Diego: Academic Press, Inc
19.
go back to reference Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E: "Where" and "what" in the whisker sensorimotor system. Nature Review Neurosci. 2008, 9: 601-612. 10.1038/nrn2411.CrossRef Diamond ME, von Heimendahl M, Knutsen PM, Kleinfeld D, Ahissar E: "Where" and "what" in the whisker sensorimotor system. Nature Review Neurosci. 2008, 9: 601-612. 10.1038/nrn2411.CrossRef
20.
go back to reference Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA: Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci. 2001, 21: 5752-5763.PubMed Krupa DJ, Matell MS, Brisben AJ, Oliveira LM, Nicolelis MA: Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci. 2001, 21: 5752-5763.PubMed
21.
go back to reference Schuler MG, Krupa DJ, Nicolelis MAL: Integration of bilateral whisker stimuli in rats: role of the whisker barrel cortices. Cereb Cortex. 2002, 12: 86-97. 10.1093/cercor/12.1.86.CrossRef Schuler MG, Krupa DJ, Nicolelis MAL: Integration of bilateral whisker stimuli in rats: role of the whisker barrel cortices. Cereb Cortex. 2002, 12: 86-97. 10.1093/cercor/12.1.86.CrossRef
22.
go back to reference Solomon JH, Hartmann MJ: Biomechanics: Robotic whiskers used to sense features. Nature. 2006, 443: 525-525. 10.1038/443525a.CrossRefPubMed Solomon JH, Hartmann MJ: Biomechanics: Robotic whiskers used to sense features. Nature. 2006, 443: 525-525. 10.1038/443525a.CrossRefPubMed
23.
go back to reference Metha SB, Kleinfeld D: Frisking the whiskers: patterned sensory input in the rat vibrissa system. Neuron. 2004, 41: 181-184. 10.1016/S0896-6273(04)00002-9.CrossRef Metha SB, Kleinfeld D: Frisking the whiskers: patterned sensory input in the rat vibrissa system. Neuron. 2004, 41: 181-184. 10.1016/S0896-6273(04)00002-9.CrossRef
24.
go back to reference Berg RW, Kleinfeld D: Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol. 2003, 89: 104-117. 10.1152/jn.00600.2002.CrossRefPubMed Berg RW, Kleinfeld D: Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol. 2003, 89: 104-117. 10.1152/jn.00600.2002.CrossRefPubMed
25.
go back to reference Kleinfeld D, Ahissar E, Diamond ME: Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol. 2006, 16: 435-444. 10.1016/j.conb.2006.06.009.CrossRefPubMed Kleinfeld D, Ahissar E, Diamond ME: Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol. 2006, 16: 435-444. 10.1016/j.conb.2006.06.009.CrossRefPubMed
26.
go back to reference Hentschke H, Haiss F, Schwarz C: Central signals rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb Cortex. 2006, 16: 1142-1156. 10.1093/cercor/bhj056.CrossRefPubMed Hentschke H, Haiss F, Schwarz C: Central signals rapidly switch tactile processing in rat barrel cortex during whisker movements. Cereb Cortex. 2006, 16: 1142-1156. 10.1093/cercor/bhj056.CrossRefPubMed
27.
go back to reference Ahrens KF, Kleinfeld D: Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. J Neurophysiol. 2004, 92: 1700-1707. 10.1152/jn.00020.2004.CrossRefPubMed Ahrens KF, Kleinfeld D: Current flow in vibrissa motor cortex can phase-lock with exploratory rhythmic whisking in rat. J Neurophysiol. 2004, 92: 1700-1707. 10.1152/jn.00020.2004.CrossRefPubMed
28.
go back to reference Veinante P, Deschènes M: Single-cell study of motor cortex projections to the barrel field in rats. J Comp Neurol. 2003, 464: 98-103. 10.1002/cne.10769.CrossRefPubMed Veinante P, Deschènes M: Single-cell study of motor cortex projections to the barrel field in rats. J Comp Neurol. 2003, 464: 98-103. 10.1002/cne.10769.CrossRefPubMed
29.
go back to reference Yu C, Derdikman D, Haidarliu S, Ahissar E: Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 2006, 4: e124-10.1371/journal.pbio.0040124.PubMedCentralCrossRefPubMed Yu C, Derdikman D, Haidarliu S, Ahissar E: Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol. 2006, 4: e124-10.1371/journal.pbio.0040124.PubMedCentralCrossRefPubMed
30.
go back to reference Ahissar E, Arieli A: Figuring space by time. Neuron. 2001, 32: 185-201. 10.1016/S0896-6273(01)00466-4.CrossRefPubMed Ahissar E, Arieli A: Figuring space by time. Neuron. 2001, 32: 185-201. 10.1016/S0896-6273(01)00466-4.CrossRefPubMed
31.
go back to reference Ahissar E, Sosnik R, Haidarliu S: Transformation from temporal to rate coding in the somatosensory thalamocortical pathway. Nature. 2000, 406: 302-306. 10.1038/35018568.CrossRefPubMed Ahissar E, Sosnik R, Haidarliu S: Transformation from temporal to rate coding in the somatosensory thalamocortical pathway. Nature. 2000, 406: 302-306. 10.1038/35018568.CrossRefPubMed
32.
go back to reference Ahissar E, Zacksenhouse M: Temporal and spatial coding in the rat vibrissal system. Prog Brain Res. 2001, 130: 75-88. full_text.CrossRefPubMed Ahissar E, Zacksenhouse M: Temporal and spatial coding in the rat vibrissal system. Prog Brain Res. 2001, 130: 75-88. full_text.CrossRefPubMed
33.
go back to reference Knutsen PM, Ahissar E: Orthogonal coding of object location. Trends in Neurosci. 2008, 32: 101-109. 10.1016/j.tins.2008.10.002.CrossRef Knutsen PM, Ahissar E: Orthogonal coding of object location. Trends in Neurosci. 2008, 32: 101-109. 10.1016/j.tins.2008.10.002.CrossRef
34.
go back to reference Fee MS, Mitra PP, Kleinfeld D: Central versus peripheral determinates of patterned spike activity in rat vibrissa cortex during whisking. J Neurophysiol. 1997, 78: 1144-1149.PubMed Fee MS, Mitra PP, Kleinfeld D: Central versus peripheral determinates of patterned spike activity in rat vibrissa cortex during whisking. J Neurophysiol. 1997, 78: 1144-1149.PubMed
35.
go back to reference Gandieva SC, Burke D: Does the nervous system depend on kinaesthetic information to control natural limb movements. Motor contro. Edited by: Cordo P, Harnard S. 1994, New York, Cambridge: University Press, 12-30. Gandieva SC, Burke D: Does the nervous system depend on kinaesthetic information to control natural limb movements. Motor contro. Edited by: Cordo P, Harnard S. 1994, New York, Cambridge: University Press, 12-30.
36.
go back to reference Nicolelis MA, Ghazanfar AA, Faggin BM, Votaw S, Oliveira LM: Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron. 1977, 18: 529-537. 10.1016/S0896-6273(00)80295-0.CrossRef Nicolelis MA, Ghazanfar AA, Faggin BM, Votaw S, Oliveira LM: Reconstructing the engram: simultaneous, multisite, many single neuron recordings. Neuron. 1977, 18: 529-537. 10.1016/S0896-6273(00)80295-0.CrossRef
37.
go back to reference Nicolelis MAL, Baccala LA, Lin RCS, Chapin JK: Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the sensorymotor system. Science. 1995, 268: 1353-1358. 10.1126/science.7761855.CrossRefPubMed Nicolelis MAL, Baccala LA, Lin RCS, Chapin JK: Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the sensorymotor system. Science. 1995, 268: 1353-1358. 10.1126/science.7761855.CrossRefPubMed
38.
go back to reference Sharp FR, Evans K: Regional (14C) 2-deoxyglucose uptake during vibrissae movement evoked by rat motor cortex stimulation. J Comp Neurol. 1982, 208: 255-287. 10.1002/cne.902080305.CrossRefPubMed Sharp FR, Evans K: Regional (14C) 2-deoxyglucose uptake during vibrissae movement evoked by rat motor cortex stimulation. J Comp Neurol. 1982, 208: 255-287. 10.1002/cne.902080305.CrossRefPubMed
39.
go back to reference Lichtenstein SH, Carvell GE, Simons DJ: Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens & Motor Res. 1990, 7: 47-65.CrossRef Lichtenstein SH, Carvell GE, Simons DJ: Responses of rat trigeminal ganglion neurons to movements of vibrissae in different directions. Somatosens & Motor Res. 1990, 7: 47-65.CrossRef
40.
go back to reference Pali J, Rencz B, Hamori J: Innervation of a single vibrissa in the whisker-pad of rat. Neuroreport. 2000, 11: 849-851. 10.1097/00001756-200003200-00038.CrossRefPubMed Pali J, Rencz B, Hamori J: Innervation of a single vibrissa in the whisker-pad of rat. Neuroreport. 2000, 11: 849-851. 10.1097/00001756-200003200-00038.CrossRefPubMed
41.
go back to reference Leiser S, Moxon KA: Response properties of rat trigeminal ganglion neurons during natural whisking behaviors. Neuron. 2007, 53: 117-133. 10.1016/j.neuron.2006.10.036.CrossRefPubMed Leiser S, Moxon KA: Response properties of rat trigeminal ganglion neurons during natural whisking behaviors. Neuron. 2007, 53: 117-133. 10.1016/j.neuron.2006.10.036.CrossRefPubMed
42.
go back to reference Khatri V, Bermejo R, Brumberg JC, Keller A, Zeigler HP: Whisking in air: encoding of kinematics by trigeminal ganglion neurons in awake rats. J Neurophysiol. 2009, 101: 1836-1846. 10.1152/jn.90655.2008.PubMedCentralCrossRefPubMed Khatri V, Bermejo R, Brumberg JC, Keller A, Zeigler HP: Whisking in air: encoding of kinematics by trigeminal ganglion neurons in awake rats. J Neurophysiol. 2009, 101: 1836-1846. 10.1152/jn.90655.2008.PubMedCentralCrossRefPubMed
43.
go back to reference Brodal A: Neurological Anatomy in Relation to Clinical Medicine. 1981, New York: Oxford University Press Brodal A: Neurological Anatomy in Relation to Clinical Medicine. 1981, New York: Oxford University Press
44.
go back to reference Byers MR, O'Connor TA, Martin RF, Dong WK: Mesencephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol. 1986, 250: 181-191. 10.1002/cne.902500205.CrossRefPubMed Byers MR, O'Connor TA, Martin RF, Dong WK: Mesencephalic trigeminal sensory neurons of cat: axon pathways and structure of mechanoreceptive endings in periodontal ligament. J Comp Neurol. 1986, 250: 181-191. 10.1002/cne.902500205.CrossRefPubMed
45.
go back to reference Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana Y, Hosoi M, Yoshida A, Kagawa K: Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat--intra-axonal staining with HRP. Brain Res. 1989, 505: 91-110. 10.1016/0006-8993(89)90119-4.CrossRefPubMed Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana Y, Hosoi M, Yoshida A, Kagawa K: Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat--intra-axonal staining with HRP. Brain Res. 1989, 505: 91-110. 10.1016/0006-8993(89)90119-4.CrossRefPubMed
46.
go back to reference Linden RWA, Scott BJJ: Distribution of mesencephalic nucleus and trigeminal ganglion mechanoreceptors in the periodontal ligament of the cat. J Physiol. 1989, 410: 35-44.PubMedCentralCrossRefPubMed Linden RWA, Scott BJJ: Distribution of mesencephalic nucleus and trigeminal ganglion mechanoreceptors in the periodontal ligament of the cat. J Physiol. 1989, 410: 35-44.PubMedCentralCrossRefPubMed
47.
go back to reference Linden RWA, Millar BJ, Halata Z: A comparative physiological and morphological study of periodontal ligament mechanoreceptors represented in the trigeminal ganglion and the mesencephalic nucleus of the cat. Anat Embryol. 1994, 190: 127-135. 10.1007/BF00193410.CrossRefPubMed Linden RWA, Millar BJ, Halata Z: A comparative physiological and morphological study of periodontal ligament mechanoreceptors represented in the trigeminal ganglion and the mesencephalic nucleus of the cat. Anat Embryol. 1994, 190: 127-135. 10.1007/BF00193410.CrossRefPubMed
48.
go back to reference Darian-Smith I: The trigeminal system. Handbook of Sensory Physiology (vol. II). Somatosensory System. Edited by: Iggo A. 1973, Berlin, Heidelberg, New York: Springer-Verlag, 271-314. Darian-Smith I: The trigeminal system. Handbook of Sensory Physiology (vol. II). Somatosensory System. Edited by: Iggo A. 1973, Berlin, Heidelberg, New York: Springer-Verlag, 271-314.
49.
go back to reference Luo P, Wong R, Dessem D: Projection of jaw-muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide. J Comp Neurol. 1995, 358: 63-78. 10.1002/cne.903580104.CrossRefPubMed Luo P, Wong R, Dessem D: Projection of jaw-muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide. J Comp Neurol. 1995, 358: 63-78. 10.1002/cne.903580104.CrossRefPubMed
50.
go back to reference Luo P, Zhang J, Yang R, Pendlebury W: Neuronal circuitry and synaptic organization of trigeminal proprioceptive afferents mediating tongue movement and jaw-tongue coordination via hypoglossal premotor neurons. Eur J Neurosci. 2006, 23: 3269-3283. 10.1111/j.1460-9568.2006.04858.x.CrossRefPubMed Luo P, Zhang J, Yang R, Pendlebury W: Neuronal circuitry and synaptic organization of trigeminal proprioceptive afferents mediating tongue movement and jaw-tongue coordination via hypoglossal premotor neurons. Eur J Neurosci. 2006, 23: 3269-3283. 10.1111/j.1460-9568.2006.04858.x.CrossRefPubMed
51.
go back to reference Wang N, May J: Peripheral muscle targets and central projections of the mesencephalic trigeminal nucleus in macaque monkeys. The Anat Rec. 2008, 291: 974-987. 10.1002/ar.20712.CrossRef Wang N, May J: Peripheral muscle targets and central projections of the mesencephalic trigeminal nucleus in macaque monkeys. The Anat Rec. 2008, 291: 974-987. 10.1002/ar.20712.CrossRef
52.
go back to reference Somana R, Kotchabhakdi N, Walberg F: Cerebellar afferents from trigeminal sensory nuclei in the cat. Exp Brain Res. 1980, 38: 57-64. 10.1007/BF00237931.CrossRefPubMed Somana R, Kotchabhakdi N, Walberg F: Cerebellar afferents from trigeminal sensory nuclei in the cat. Exp Brain Res. 1980, 38: 57-64. 10.1007/BF00237931.CrossRefPubMed
53.
go back to reference Billig I, Yatim N, Compoint C, Buisseret-Delmas C, Buisseret P: Cerebellar afferences from the mesencephalic trigeminal nucleus in the rat. Neuroreport (Somatosensory System and Pain). 1995, 6: 2293-2296.CrossRef Billig I, Yatim N, Compoint C, Buisseret-Delmas C, Buisseret P: Cerebellar afferences from the mesencephalic trigeminal nucleus in the rat. Neuroreport (Somatosensory System and Pain). 1995, 6: 2293-2296.CrossRef
54.
go back to reference Szentàgothai J: Anatomical considerations of monosynaptic reflex arcs. J Neurophysiol. 1948, 11: 445-453.PubMed Szentàgothai J: Anatomical considerations of monosynaptic reflex arcs. J Neurophysiol. 1948, 11: 445-453.PubMed
55.
go back to reference Mizuno N, Sauerland EK: Trigeminal proprioceptive projections to the hypoglossal nucleus and the cervical ventral gray column. J Comp Neurol. 1970, 139: 215-226. 10.1002/cne.901390205.CrossRefPubMed Mizuno N, Sauerland EK: Trigeminal proprioceptive projections to the hypoglossal nucleus and the cervical ventral gray column. J Comp Neurol. 1970, 139: 215-226. 10.1002/cne.901390205.CrossRefPubMed
56.
go back to reference Zhang J, Luo P, Pendlebury WW: Light and electron microscopic observations of a direct projection from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Brain Res. 2001, 917: 67-80. 10.1016/S0006-8993(01)02911-0.CrossRefPubMed Zhang J, Luo P, Pendlebury WW: Light and electron microscopic observations of a direct projection from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Brain Res. 2001, 917: 67-80. 10.1016/S0006-8993(01)02911-0.CrossRefPubMed
57.
go back to reference Zhang J, Pendlebury WW, Luo P: Synaptic organization of monosynaptic connections from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Synapse. 2003, 49: 157-169. 10.1002/syn.10227.CrossRefPubMed Zhang J, Pendlebury WW, Luo P: Synaptic organization of monosynaptic connections from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat. Synapse. 2003, 49: 157-169. 10.1002/syn.10227.CrossRefPubMed
Metadata
Title
Role of the trigeminal mesencephalic nucleus in rat whisker pad proprioception
Authors
Ombretta Mameli
Stefania Stanzani
Gabriele Mulliri
Rosalia Pellitteri
Marcello A Caria
Antonella Russo
Pierluigi De Riu
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Behavioral and Brain Functions / Issue 1/2010
Electronic ISSN: 1744-9081
DOI
https://doi.org/10.1186/1744-9081-6-69

Other articles of this Issue 1/2010

Behavioral and Brain Functions 1/2010 Go to the issue