Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Click here to sign up for SAGE Journal Email Alerts today!

Sign In to gain access to subscriptions and/or personal tools.
Journal of Dental Research
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Ishiwata, Y.
Right arrow Articles by Nakamura, Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ishiwata, Y.
Right arrow Articles by Nakamura, Y.
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

Jaw-Tongue Reflex: Afferents, Central Pathways, and Synaptic Potentials in Hypoglossal Motoneurons in the Cat

Y. Ishiwata

Maxillofacial Orthognathics and Department of Physiology, Maxillofacial Reconstruction, Division of Maxillofacial/Neck Reconstruction, Graduate School, Tokyo Medical and Dental University, 5-45 Yushima 1-chome, Bunkyo-ku, Tokyo 113-8549, Japan

T. Ono

Maxillofacial Orthognathics and Department of Physiology, Maxillofacial Reconstruction, Division of Maxillofacial/Neck Reconstruction, Graduate School, Tokyo Medical and Dental University, 5-45 Yushima 1-chome, Bunkyo-ku, Tokyo 113-8549, Japan, t=ono.ort2{at}dent.tmd.ac.jp

T. Kuroda

Maxillofacial Orthognathics and Department of Physiology, Maxillofacial Reconstruction, Division of Maxillofacial/Neck Reconstruction, Graduate School, Tokyo Medical and Dental University, 5-45 Yushima 1-chome, Bunkyo-ku, Tokyo 113-8549, Japan

Y. Nakamura

Department of Welfare Information Science, Teikyo Heisei University, Ichihara, Chiba Prefecture 290-0193, Japan

The tongue position is reflexively controlled by the jaw position (the jaw-tongue reflex). The purpose of this study was to clarify the mechanism of this reflex in terms of afferents, central pathways, and synaptic potentials in hypoglossal motoneurons in the cat. Intracellular recordings from hypoglossal motoneurons revealed that electrical stimulation of the temporalis muscle nerve evoked excitatory and inhibitory post-synaptic potentials in hypoglossal motoneurons. The threshold of temporalis muscle nerve stimulation for evoking the synaptic potentials was higher than 2.0 times the nerve threshold. The amplitude of the potentials increased with stimulus intensity up to 5.0 times the nerve threshold. Punctate light pressure applied to the temporalis muscle induced a tonic depolarizing potential in hypoglossal motoneurons on which action potentials as well as depolarizing synaptic activation noise were superimposed. On the other hand, electrical stimulation of the temporalis muscle during jaw-opening could slightly inhibit the electromyographic activities in the genioglossus and styloglossus muscles. Lesions including the Probst's tract at the level caudal to the trigeminal motor nucleus abolished both excitation and inhibition in hypoglossal motoneurons induced by tonic depression of the lower jaw, but exerted no effects on either the tonic stretch reflex or the trigemino-hypoglossal reflex. In contrast, lesions including the trigeminal spinal tract produced no changes in either excitation or inhibition of hypoglossal motoneurons induced by temporalis muscle afferents, whereas the excitation of hypoglossal motoneurons was abolished by the lesions. We conclude that the group II muscle spindle afferents from the temporalis muscle are primarily responsible for evoking the jaw-tongue reflex.

Key Words: jaw-tongue reflex • temporalis muscle • muscle spindle • group II fiber • hypoglossal motoneuron.

REFERENCES

  • Amri M., Lamkadem M., Car A. (1991). Effects of lingual nerve and chewing cortex stimulation upon activity of the swallowing neurons located in the region of the hypoglossal motor nucleus. Brain Res 548:149-155.[CrossRef][Medline] [Order article via Infotrieve]
  • Barker D. (1967). The innervation of the mammalian skeletal muscle. In: Kinesthetic and vestibular mechanisms. deReuck AVS, Knight J, editors. London: Churchill, pp. 3-15.
  • Beaudreau DE, Jerge CR (1968). Somatotopic representation in Gasserian ganglion of tactile peripheral fields in the cat. Arch Oral Biol 13:247-256.[CrossRef][Medline] [Order article via Infotrieve]
  • Blom S. ( 1960). Afferent influence on tongue muscle activity. Acta Physiol Scand 49(Suppl 170): 1-97.[Medline] [Order article via Infotrieve]
  • Boyd IA, Davey MR (1968). The composition of peripheral nerves. Edinburgh: Livingstone.
  • Bradley K., Eccles JC (1953). Analysis of the fast afferent impulses from thigh muscles. J Physiol 122:462-473.[Free Full Text]
  • Corbin KB (1940). Observation on the peripheral distribution of the fibres arising in the mesencephalic nucleus of the fifth cranial nerve. J Comp Neurol 73:153-177.[CrossRef]
  • Corbin KB (1942). Probst's tract in the cat. J Comp Neurol 77:455-467.[CrossRef]
  • Corbin KB, Harrison F. (1940). Function of mesencephalic root of the fifth cranial nerve. J Neurophysiol 3:423-435.[Free Full Text]
  • Dinardo LA, Travers JB (1994). Hypoglossal neural activity during ingestion and rejection in the awake rat. J Neurophysiol 72:1181 -1191.[Abstract/Free Full Text]
  • Duggan AW, Lodge D., Biscoe TJ (1973). The inhibition of hypoglossal motoneurones by impulses in the glossopharyngeal nerve of the rat. Exp Brain Res 17:261-270.[Medline] [Order article via Infotrieve]
  • Eccles JC (1964). The physiology of synapses. Berlin: Springer.
  • Eccles JC, Eccles RM, Lundberg A. (1957). Synaptic actions on motoneurons caused by impulses in Golgi tendon organ afferents. J Physiol 138:227-252.[Free Full Text]
  • Edgley SA, Jankowska E. (1987). Field potentials generated by group II muscle afferents in the middle lumbar segments of the cat spinal cord. J Physiol 385:393-413.[Abstract/Free Full Text]
  • Gordon KR, Herring SW (1987). Activity patterns within the genioglossus during suckling in domestic dogs and pigs: interspecific and intraspecific plasticity. Brain Behav Evol 30:249-262.[Medline] [Order article via Infotrieve]
  • Granit R. (1950). Reflex self-regulation of muscle contraction and autogenetic inhibition. J Neurophysiol 13:351-372.[Free Full Text]
  • Grillner S., Hongo T., Lund S. ( 1970). The vestibulospinal tract. Effects on alpha-motoneurones in the lumbosacral spinal cord in the cat. Exp Brain Res 10:94-120.[CrossRef][Medline] [Order article via Infotrieve]
  • Hamada T., Takata M., Kawamura Y. (1974). Interrelation of afferent impulses from different bellies of the temporal muscle of the cat. J Dent Res 53:889-896.
  • Hongo T., Jankowska E., Lundberg A. (1972). The rubrospinal tract. IV. Effects on intemeurons. Exp Brain Res 15:54-78.[Medline] [Order article via Infotrieve]
  • Hunt CC ( 1954). Relation of function to diameter in afferent fibres of muscle nerves. J Gen Physiol 38:117-131.[Abstract/Free Full Text]
  • Hunt CC, Kuffler SW (1951). Stretch receptor discharges during muscle contraction. J Physiol 113:298-315.[Free Full Text]
  • Hunt CC, McIntyre AK (1960). Characteristics of responses from receptors from the flexor longus digitorum muscle and the adjoining interosseous region of the cat. J Physiol 153:74-87.[Free Full Text]
  • Inoue H., Morimoto T., Kawamura Y. (1981). Response characteristics and classification of muscle spindles of the masseter muscle in the cat. Exp Neurol 74:548-560.[CrossRef][Medline] [Order article via Infotrieve]
  • Ishiwata Y., Hiyama S., Igarashi K., Ono T., Kuroda T. (1997). Human jaw-tongue reflex as revealed by intraoral surface recording. J Oral Rehabil 24:857-862.[Medline] [Order article via Infotrieve]
  • Jack Jjb (1978). Some methods for selective activation of muscle afferent fibres. In: Studies in neurophysiology. Porter R, editor. Cambridge: Cambridge University Press, pp. 155-176.
  • Kawamura Y., Takata M., Kato I. ( 1968). The role of spontaneous firing of the trigeminal motoneuron. Jpn J Physiol 18:7-14.[Medline] [Order article via Infotrieve]
  • Klüver H., Barrera E. (1953). A method for the combined staining of cells and fibres in the nervous system. J Neuropathol 12:400-413.[Medline] [Order article via Infotrieve]
  • Kubota K., Masegi T., Quanbunchan K. (1974). Muscle spindle distribution in masticatory muscles of the tree shrew. J Dent Res 53:538-546.
  • Lowe AA ( 1978a). Excitatory and inhibitory inputs to hypoglossal motoneurons and adjacent reticular formation neurons in cats. Exp Neurol 62:30-47.[CrossRef][Medline] [Order article via Infotrieve]
  • Lowe AA ( 1978b). Mandibular joint control of genioglossus muscle activity in the cat (Felis domesticus) and monkey (Macaca irus). Arch Oral Biol 23:787-793.[CrossRef][Medline] [Order article via Infotrieve]
  • Lowe AA ( 1980). The neural regulation of tongue movements. Prog Neurobiol 15:295-344.[CrossRef][Medline] [Order article via Infotrieve]
  • Lowe AA, Johnston WD (1979). Tongue and jaw muscle activity in response to mandibular rotations in a sample of normal and anterior open-bite subjects. Am J Orthod 76:565-576.[Medline] [Order article via Infotrieve]
  • Lowe AA, Sessle BJ (1973). Tongue activity during respiration, jaw opening, and swallowing in cat. Can J Physiol Pharmacol 51:1009-1011.[Medline] [Order article via Infotrieve]
  • Lund JP, Richmond FJ, Touloumis C., Patry Y., Lamarre Y. (1978). The distribution of Golgi tendon organs and muscle spindles in masseter and temporalis muscles of the cat. Neuroscience 3:259-270.[CrossRef][Medline] [Order article via Infotrieve]
  • Matthews Pbc (1972). Mammalian muscle receptors and their central actions. London: Arnold.
  • Matthews PB (1981). Evolving views on the internal operation and functional role of the muscle spindle. J Physiol 320:1-30.[Free Full Text]
  • Mizuno N., Sauerland EK (1970). Trigeminal proprioceptive projections to the hypoglossal nucleus and the cervical ventral gray column. J Comp Neurol 139:215-226.[CrossRef][Medline] [Order article via Infotrieve]
  • Morimoto T., Kawamura Y. (1972). Inhibitory postsynaptic potentials of hypoglossal motoneurons of the cat. Exp Neurol 37:188-198.[Medline] [Order article via Infotrieve]
  • Morimoto T., Takata M., Kawamura Y. (1968). Effect of lingual nerve stimulation on hypoglossal motoneurons. Exp Neurol 22:174-190.[Medline] [Order article via Infotrieve]
  • Morimoto T., Takata M., Kawamura Y. (1972). Inhibition of hypoglossal motoneurons by a masseteric nerve volley. Brain Res 43:285-288.[CrossRef][Medline] [Order article via Infotrieve]
  • Morimoto T., Takebe H., Sakan I., Kawamura Y. (1978). Reflex activation of extrinsic tongue muscles by jaw closing muscle proprioceptors. Jpn J Physiol 28:461-471.[Medline] [Order article via Infotrieve]
  • Nakamura Y., Wu CY (1970). Presynaptic inhibition of jaw-opening reflex by high threshold afferents from the masseter muscle of the cat. Brain Res 23:193-211.[CrossRef][Medline] [Order article via Infotrieve]
  • Nakamura Y., Mori S., Nagashima H. (1973). Origin and central pathways of crossed inhibitory effects of afferents from the masseteric muscle on the masseteric motoneuron of the cat. Brain Res 57:29-42.[CrossRef][Medline] [Order article via Infotrieve]
  • Nishimori T., Sera M., Suemune S., Yoshida A., Tsuru K., Tsuiki Y., et al. (1986). The distribution of muscle primary afferents from the masseter nerve to the trigeminal sensory nuclei. Brain Res 372:375-381.[CrossRef][Medline] [Order article via Infotrieve]
  • Nomura S., Mizuno N. (1985). Differential distribution of the cell bodies and central axons of mesencephalic trigeminal nucleus neurons supplying the jaw-closing muscles and periodontal tissue: a transganglionic tracer study in the cat. Brain Res 359:311-319.[CrossRef][Medline] [Order article via Infotrieve]
  • Ono T., Ishiwata Y., Inaba N., Kuroda T., Nakamura Y. (1994). Hypoglossal premotor neurons with rhythmical inspiratory-related activity in the cat: localization and projection to the phrenic nucleus. Exp Brain Res 98:1-12.[Medline] [Order article via Infotrieve]
  • Ono T., Ishiwata Y., Inaba N., Kuroda T., Nakamura Y. (1998). Modulation of the inspiratory-related activity of hypoglossal premotor neurons during ingestion and rejection in the decerebrate cat. J Neurophysiol 80:48-58.[Abstract/Free Full Text]
  • Ro JY, Capra NF (1999). Physiological evidence for caudal brainstem projections of jaw muscle spindle afferents. Exp Brain Res 128:425-434.[Medline] [Order article via Infotrieve]
  • Romfh JH, Capra NF, Gatipon GB (1979). Trigeminal nerve and temporomandibular joint of the cat: a horseradish peroxidase study. Exp Neurol 65:99-106.[Medline] [Order article via Infotrieve]
  • Ruggiero DA, Ross CA, Kumada M., Reis DJ ( 1982). Reevaluation of projections from the mesencephalic trigeminal nucleus to the medulla and spinal cord: new projections. A combined retrograde and anterograde horseradish peroxidase study. J Comp Neurol 206:278-292.[Medline] [Order article via Infotrieve]
  • Rye DB, Lee HJ, Saper CB, Wainer BH (1988). Medullary and spinal efferents of the pedunculopontine tegmental nucleus and adjacent mesopontine tegmentum in the rat. J Comp Neurol 269:315-341.[CrossRef][Medline] [Order article via Infotrieve]
  • Sahara Y., Hashimoto N., Kato M., Nakamura Y. (1988). Synaptic bases of cortically-induced rhythmical hypoglossal motoneuronal activity in the cat. Neurosci Res 5:439-452.[Medline] [Order article via Infotrieve]
  • Schoen R. (1931). Untersuchungen iiber Zungen- und Kieferreflexe: I. Mitteilung der Kieferzungen Reflex und andere proprioceptive Reflex der Zunge und der Kiefermuskulatur. Arch Exp Pathol Pharmakoll 160:29-48.
  • Sokoloff AJ, Deacon TW (1992). Musculotopic organization of the hypoglossal nucleus in the cynomolgus monkey, Macaca fascicularis. J Comp Neurol 324:81-93.[CrossRef][Medline] [Order article via Infotrieve]
  • Stacey MJ (1969). Free nerve endings in skeletal muscle of the cat. J Anat 105:231-254.[Medline] [Order article via Infotrieve]
  • Sumino R., Nakamura Y. (1974). Synaptic potentials of hypoglossal motoneurons and a common inhibitory interneuron in the trigemino-hypoglossal reflex. Brain Res 73:439-454.[CrossRef][Medline] [Order article via Infotrieve]
  • Szentagothai J. (1948). Anatomical consideration of monosynaptic reflex arc. J Neurophysiol 11:445-454.[Free Full Text]
  • 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.[CrossRef][Medline] [Order article via Infotrieve]
  • Thelander HE (1924). The course and distribution of the radix mesencephalica trigemini in the cat. J Comp Neurol 37:207-220.
  • Travers JB, Norgren R. (1983). Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280-298.[CrossRef][Medline] [Order article via Infotrieve]
  • Travers JB, Montgomery N., Sheridan J. (1995). Transneuronal labeling in hamster brainstem following lingual injections with herpes simplex virus-1. Neuroscience 68:1277-1293.[CrossRef][Medline] [Order article via Infotrieve]
  • Walberg F., Dietrichs E., Nordby T. (1984). The medullary projection from the mesencephalic trigeminal nucleus. An experimental study with comments on the intrinsic trigeminal connections. Exp Brain Res 556:377-383.

Journal of Dental Research, Vol. 79, No. 8, 1626-1634 (2000)
DOI: 10.1177/00220345000790081701
Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
 J. Appl. Physiol.Home page
S. Ryan and P. Nolan
Superior laryngeal and hypoglossal afferents tonically influence upper airway motor excitability in anesthetized rats
J Appl Physiol, September 1, 2005; 99(3): 1019 - 1028.
[Abstract] [Full Text] [PDF]

Home page
 J. Appl. Physiol.Home page
S. Ryan, W. T. McNicholas, R. G. O'Regan, and P. Nolan
Upper airway muscle paralysis reduces reflex upper airway motor response to negative transmural pressure in rat
J Appl Physiol, April 1, 2003; 94(4): 1307 - 1316.
[Abstract] [Full Text] [PDF]

Home page
 CROBMHome page
A.J. Miller
ORAL AND PHARYNGEAL REFLEXES IN THE MAMMALIAN NERVOUS SYSTEM: THEIR DIVERSE RANGE IN COMPLEXITY AND THE PIVOTAL ROLE OF THE TONGUE
Critical Reviews in Oral Biology & Medicine, September 1, 2002; 13(5): 409 - 425.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Ishiwata, Y.
Right arrow Articles by Nakamura, Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ishiwata, Y.
Right arrow Articles by Nakamura, Y.
Social Bookmarking
Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?