Online citations, reference lists, and bibliographies.
← Back to Search

Neuronal Circuitry And Synaptic Organization Of Trigeminal Proprioceptive Afferents Mediating Tongue Movement And Jaw–tongue Coordination Via Hypoglossal Premotor Neurons

P. Luo, J. Zhang, R. Yang, W. Pendlebury
Published 2006 · Medicine, Biology

Cite This
Download PDF
Analyze on Scholarcy
Share
The neural framework and synaptic organization of trigeminal proprioceptive afferent‐mediated jaw–tongue coordination were studied in rats using multiple electrophysiological and neuroanatomical approaches. Electrostimulation of the masseter nerve evoked short‐latency responses (5.86 ± 2.59 ms) in hypoglossal premotor pools including the parvocellular (PCRt) and intermediate (IRt) reticular nuclei and the dorsomedial part of the spinal trigeminal nucleus oralis (Vodm) and interpolaris (Vidm). Biocytin‐labelled axon terminals from these areas traveled into the hypoglossal nucleus (XII) and contacted motoneurons. Double labelling of biotinylated dextran amine (BDA) tracing and cholera toxin B (CTB) transport demonstrated that labelled axons and terminals from the mesencephalic trigeminal nucleus (Vme) overlapped with XII premotor neurons in the alpha division and in PCRt, IRt, Vodm and Vidm. Confocal microscopic observations revealed that Vme terminals closely contacted XII premotor neurons. Dual labelling of intracellular neurobiotin staining of jaw‐muscle spindle afferents (JMSAs) combined with horseradish peroxidase (HRP) retrograde transport revealed that 498 JMSA boutons apposed to 146 HRP‐labelled premotor neurons. Electron microscopic observations demonstrated that 127 JMSA boutons made both axodendritic (68%) and axosomatic (32%) synapses with XII premotor neurons. Eighty‐three per cent of synapses were asymmetric and the rest (17%) were symmetric. Thirty‐nine per cent of JMSA boutons received presynaptic contacts from P‐type terminals. Varieties of synaptic organizations were found. These results provide evidence that trigeminal proprioceptive afferents mediate jaw–tongue coordination through XII premotor neurons. Ultrastructural findings demonstrated that synapses between JMSA boutons and XII premotor neurons are predominantly excitatory, and synaptic transmission to XII motoneurons is modified on XII premotor neurons by presynaptic mechanisms. These frameworks and synaptic organizations are most probably the neural substrate for trigeminal proprioceptive afferent‐mediated jaw–tongue coordination.
This paper references
10.1002/CA.10156
Morphological studies for retrusive movement of the human adult tongue
H. Saigusa (2004)
10.1097/00005072-199105000-00013
The Fine Structure of the Nervous System: Neurons and Their Supporting Cells
A. Peters (1991)
10.1016/S1385-299X(01)00065-4
Elucidation of neuronal circuitry: protocol(s) combining intracellular labeling, neuroanatomical tracing and immunocytochemical methodologies.
P. Luo (2001)
10.1016/S0006-8993(01)02848-7
Tongue and jaw muscle activities during chewing and swallowing in freely behaving rabbits
K. Naganuma (2001)
A histochemical study of the neuro-muscular spindles in the tongue of some rodents.
Purwar Rs (1979)
10.1016/S0166-2236(84)80278-7
The Rat Brain in Stereotaxic Coordinates
L. Swanson (1984)
10.1152/PHYSREV.2001.81.2.929
Brain stem control of swallowing: neuronal network and cellular mechanisms.
A. Jean (2001)
10.1016/S0006-8993(02)03662-4
Convergence of selected inputs from sensory afferents to trigeminal premotor neurons with possible projections to masseter motoneurons in the rabbit
M. Inoue (2002)
10.1152/AJPREGU.2001.280.4.R1085
Muscimol infusions in the brain stem reticular formation reversibly block ingestion in the awake rat.
Z. Chen (2001)
Elucidation of neuronal circuitry
P. Luo (2001)
10.1177/00220345000790081701
Jaw-Tongue Reflex: Afferents, Central Pathways, and Synaptic Potentials in Hypoglossal Motoneurons in the Cat
Y. Ishiwata (2000)
10.1098/rspb.1985.0067
Understanding the intrinsic circuitry of the cat’s lateral geniculate nucleus: electrical properties of the spine-triad arrangement
C. Koch (1985)
1963a) Organization and function of the trigeminal mesencephalic nucleus
C. R. Jerge (1963)
10.1007/BF00229103
Hypoglossal premotor neurons with rhythmical inspiratory-related activity in the cat: localization and projection to the phrenic nucleus
T. Ono (2004)
10.1159/000118858
Tongue movements--brainstem mechanisms and clinical postulates.
A. Lowe (1984)
10.1159/000118860
A study of jaw reflexes of the awake cat during mastication and locomotion.
J. Lund (1984)
10.1016/c2009-0-63235-9
The Rat Brain in Stereotaxic Coordinates
G. Paxinos (1983)
Identification of sensory neurons supplying receptors in lingual muscles of the rat: histochemical and retrograde labeling study with horseradish peroxidase.
M. F. Sherif (1991)
10.1007/BF00229659
Serotonin innervation patterns differ among the various medullary motoneuronal groups involved in upper airway control
H. Arita (2004)
10.1159/000014956
An analysis of meiotic pairing in trisomy 21 oocytes using fluorescent in situ hybridization
E. Cheng (1998)
10.1007/s00221-002-1187-5
Association of orofacial with laryngeal and respiratory motor output during speech
M. McClean (2002)
Axonal projections and synapses
P. Luo (2001)
10.1002/CNE.902200303
Afferent projections to the oral motor nuclei in the rat
J. Travers (1983)
10.1044/JSHR.2404.601
Muscle activity for jaw closing during speech.
J. Folkins (1981)
10.1016/S0168-0102(96)01080-2
Hypoglossal premotor neurons in the rostral medullary parvocellular reticular formation participate in cortically-induced rhythmical tongue movements
Y. Sahara (1996)
10.1016/j.brainres.2005.06.074
Involvement of reticular neurons located dorsal to the facial nucleus in activation of the jaw-closing muscle in rats
J. Takamatsu (2005)
10.1159/000167760
Buchbesprechungen – Book Reviews – Livres Nouveaux
M. Holzmann (2004)
Jaw-muscle spindle afferent
P. Luo (2001)
10.1007/BF00247896
Sensory and motor responses of trigeminal and reticular neurons during ingestive behavior in rats
T. Yamamoto (2004)
10.1152/JN.1992.67.5.1171
Hypoglossal neural activity during licking and swallowing in the awake rat.
J. Travers (1992)
10.4449/AIB.V131I2.822
Responses of hypoglossal motoneurons to mechanical stimulation of the teeth in rats.
E. Tolu (1993)
10.1016/S0301-0082(01)00021-1
Comparative analysis of the chemical neuroanatomy of the mammalian trigeminal ganglion and mesencephalic trigeminal nucleus
N. Lazarov (2002)
10.1152/AJPREGU.00054.2003
Inactivation of amino acid receptors in medullary reticular formation modulates and suppresses ingestion and rejection responses in the awake rat.
Z. Chen (2003)
10.1016/0006-8993(89)91413-3
Evidence for excitatory amino acid transmission between mesencephalic nucleus of V afferents and jaw-closer motoneurons in the guinea pig
S. Chandler (1989)
10.1016/0006-8993(93)91156-M
Location and axonal projection of one type of swallowing interneurons in cat medulla
K. Ezure (1993)
10.1152/JN.1995.74.4.1509
Modification of mastication and respiration during swallowing in the adult human.
D. McFarland (1995)
10.1002/cne.1034
Jaw‐muscle spindle afferent pathways to the trigeminal motor nucleus in the rat
P. Luo (2001)
10.1016/0006-8993(94)90257-7
Immunohistochemical localization of glutamate and glutaminase in guinea pig trigeminal premotoneurons
J. Turman (1994)
10.1016/S0006-8993(01)02911-0
Light and electron microscopic observations of a direct projection from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat
J. Zhang (2001)
10.1113/jphysiol.1985.sp015890
Morphological and electrophysiological determination of the projections of jaw‐elevator muscle spindle afferents in rats.
K. Appenteng (1985)
10.1152/JN.1993.69.2.595
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.
S. Nozaki (1993)
10.1113/jphysiol.1972.sp009983
A functional analysis of the components of the mesencephalic nucleus of the fifth nerve in the cat
F. Cody (1972)
10.1016/S0002-9343(01)00849-X
Central neurocircuitry associated with emesis.
P. Hornby (2001)
10.1046/J.1365-2842.2000.00560.X
Genioglossus muscle activity during rhythmic open-close jaw movements.
S. Hiyama (2000)
10.1016/j.brainres.2004.05.005
Coordination of jaw and extrinsic tongue muscle activity during rhythmic jaw movements in anesthetized rabbits
S. Ariyasinghe (2004)
Reflex activation
H. Takebe (1978)
10.1523/JNEUROSCI.11-11-03539.1991
Brainstem enkephalinergic projections to spinal autonomic nuclei
M. Romagnano (1991)
10.1152/jn.1963.26.3.393
The function of the nucleus supratrigeminalis.
C. Jerge (1963)
Organization and function of the trigeminal mesencephalic nucleus
C R Jerge (1963)
10.1002/CNE.903580104
Projection of jaw‐muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide
P. Luo (1995)
10.1016/j.brainres.2004.06.047
Extrinsic tongue and suprahyoid muscle activities during mastication in freely feeding rabbits
M. Inoue (2004)
10.1002/(SICI)1096-9861(19990412)406:3<384::AID-CNE7>3.0.CO;2-7
Ultrastructural anatomy of physiologically identified jaw‐muscle spindle afferent terminations onto retrogradely labeled jaw‐elevator motoneurons in the rat
P. Luo (1999)
Ultrastructural anatomy of physiologically
P. Luo (1999)
10.5357/KOUBYOU.63.108
[Neurophysiological mechanism of jaw-tongue reflex in man].
K. Igarashi (1996)
10.1016/0006-8993(93)91789-U
Identification of premotor interneurons which project bilaterally to the trigeminal motor, facial or hypoglossal nuclei: a fluorescent retrograde double-labeling study in the rat
Y. Li (1993)
10.1152/JN.1993.69.1.95
An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit.
D. McFarland (1993)
10.1016/0006-8993(91)91189-8
Genioglossus EMG activity during rhythmic jaw movements in the anesthetized guinea pig
G. Gerstner (1991)
10.1002/JMOR.1052100302
Functional morphological interpretation of the distribution of muscle spindles in the jaw muscles of the mallard (Anas platyrhynchos)
R. Bout (1991)
10.1121/1.385828
Jaw-muscle activity during speech with the mandible fixed.
J. Folkins (1981)
Trigeminal premotor neurons
S. Nozaki (1993)
10.1007/BF00228130
Axonal branching of medullary swallowing neurons projecting on the trigeminal and hypoglossal motor nuclei: demonstration by electrophysiological and fluorescent double labeling techniques
M. Amri (2004)
10.1177/00220345980770020301
Swallowing-related Perihypoglossal Neurons Projecting to Hypoglossal Motoneurons in the Cat
T. Ono (1998)
10.1002/SYN.10227
Synaptic organization of monosynaptic connections from mesencephalic trigeminal nucleus neurons to hypoglossal motoneurons in the rat
J. Zhang (2003)
10.1177/00220345990780110901
Suppression of Jaw-opening and Trigemino-hypoglossal Reflexes during Swallowing in the Cat
T. Ono (1999)
10.1016/j.resp.2005.03.015
Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors
C. Gestreau (2005)
10.1152/JN.1998.80.1.48
Modulation of the inspiratory-related activity of hypoglossal premotor neurons during ingestion and rejection in the decerebrate cat.
T. Ono (1998)
10.1046/J.1471-4159.2000.0741335.X
Expression of 15 glutamate receptor subunits and various splice variants in tissue slices and single neurons of brainstem nuclei and potential functional implications.
I. Paarmann (2000)
An investigation of the coupling
D. H. McFarland (1993)
A histochemical study of the neuro-muscular spindles in the tongue of some rodents.
R. Purwar (1979)
10.1002/CNE.901840407
Electron microscopic studies of serially sectioned cat spinal α‐motoneurons. II. A method for the description of architecture and synaptology of the cell body and proximal dendritic segments
S. Conradi (1979)
10.2170/JJPHYSIOL.28.461
Reflex activation of extrinsic tongue muscles by jaw closing muscle proprioceptors.
T. Morimoto (1978)
10.1016/0168-0102(95)90003-9
Generation of masticatory rhythm in the brainstem
Y. Nakamura (1995)
10.1016/S0034-5687(99)00058-4
Premotor input to hypoglossal motoneurons from Kölliker-Fuse neurons in decerebrate cats.
S. Kuna (1999)
10.1038/220301A0
Behaviour of Jaw Muscle Stretch Receptors during Active and Passive Movements in the Cat
A. Taylor (1968)
10.1002/AR.1091610410
Muscle spindles in the intrinsic and extrinsic muscles of the Rhesus monkey's (Macaca mulatta) tongue
J. P. Bowman (1968)
10.1002/(SICI)1096-9861(19970210)378:2<283::AID-CNE10>3.0.CO;2-T
Distribution of GABAergic and glycinergic premotor neurons projecting to the facial and hypoglossal nuclei in the rat
Y. Li (1997)
10.1016/S0006-8993(00)03183-8
Axonal projections and synapses from the supratrigeminal region to hypoglossal motoneurons in the rat
P. Luo (2001)
Projection of jaw-muscle spindle
P. 341–353. Luo (1995)
10.1097/00005072-199811000-00015
The Synaptic Organization of the Brain, 4th Ed
Carol M. Petito (1998)
10.1016/0304-3940(81)90198-1
Peripheral and central distribution of fibres of the mesencephalic trigeminal root in the rat
C. Matesz (1981)
10.1177/00220345960750081201
Tongue, Jaw, and Lip Muscle Activity and Jaw Movement during Experimental Chewing Efforts in Man
K. Takada (1996)
10.1016/0003-9969(89)90091-5
Histological demonstration of muscle spindles in the tongue of the rat.
K. K. Smith (1989)
10.1597/1545-1569(1996)033<0213:PROTLV>2.3.CO;2
Proprioceptive representation of the levator veli palatini muscle in the solitary nucleus of the rat.
K. Furusawa (1996)
Topological distribution of muscle spindles in the human tongue and its significance in proprioception.
K. Kubota (1975)
Suppression of jaw
J. Dent. Res (1999)
The Synaptic Organization of the Brain
G. Shepherd (1979)
10.1016/0006-8993(94)91871-6
Morphological study of long axonal projections of ventral medullary inspiratory neurons in the rat
J. Lipski (1994)
Identification of sensory neurons supplying receptors in lingual muscles of the rat: histochemical and retrograde labeling study with horseradish peroxidase.
Sherif Mf (1991)
10.1016/S0003-9969(97)00020-4
Tongue-jaw linkages in human feeding: a preliminary videofluorographic study.
J. Palmer (1997)
10.1007/BF00230967
Vocalization-correlated single-unit activity in the brain stem of the squirrel monkey
A. Kirzinger (2004)
10.1016/0006-8993(94)91767-1
Supra- and juxtatrigeminal inhibitory premotor neurons with bifurcating axons projecting to masseter motoneurons on both sides
H. Kamogawa (1994)
10.1016/0006-8993(88)91389-3
Projections from the medullary swallowing center to the hypoglossal motor nucleus: a neuroanatomical and electrophysiological study in sheep
M. Amri (1988)
10.1002/CNE.903630110
Ultrastructural basis for synaptic transmission between jaw muscle spindle afferents and trigeminothalamic neurons in the rostral trigeminal sensory nuclei of the rat
P. Luo (1995)
10.1016/j.neures.2004.10.005
Efferent and afferent connections of GABAergic neurons in the supratrigeminal and the intertrigeminal regions: An immunohistochemical tract-tracing study in the GAD67-GFP knock-in mouse
J. Li (2005)
10.1016/S0165-0173(97)00027-1
Identification of rat brainstem multisynaptic connections to the oral motor nuclei in the rat using pseudorabies virus: II. Facial muscle motor systems
Richard A Fay (1997)
10.1177/154411130201300505
Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue.
A. Miller (2002)
10.1152/JN.1993.70.2.529
Multifunctional properties of ambiguous neurons identified electrophysiologically during vocalization in the awake monkey.
Y. Yajima (1993)
10.4449/AIB.V132I2.790
Muscle spindle and periodontal trigeminal afferents modulate the hypoglossal motoneuronal activity.
E. Tolu (1994)
10.1016/0006-8993(88)90085-6
Distribution of medullary respiratory neurons in the rat
K. Ezure (1988)
10.1111/J.1365-2842.1997.TB00286.X
Human jaw-tongue reflex as revealed by intraoral surface recording.
Y. Ishiwata (1997)
10.1002/(SICI)1096-9861(20000313)418:3<323::AID-CNE7>3.0.CO;2-Y
Pontomedullary distribution of 5‐HT2A receptor‐like protein in the rat
Richard A Fay (2000)
10.1016/S0006-8993(02)04046-5
Ultrastructural features of synapse from dorsal parvocellular reticular formation neurons to hypoglossal motoneurons of the rat
J. Zhang (2003)
Journal Compilation a Federation of European Neuroscience Societies and Blackwell Publishing Ltd
P. Luo (2006)
10.1152/JN.1993.69.2.569
Coordination of cortically induced rhythmic jaw and tongue movements in the rabbit.
Z. Liu (1993)



This paper is referenced by
10.1007/978-1-4614-8794-4_23
Techniques for Extracellular Recordings
J. Zhang (2014)
Unraveling a masticatory - oculomotor neural pathway in rat: Implications for a pathophysiological neural circuit in human?
J. Zhang (2011)
10.1007/978-1-4614-4466-4
Craniofacial Muscles
L. McLoon (2013)
10.1016/j.neuroscience.2017.08.034
Circuits in the Rodent Brainstem that Control Whisking in Concert with Other Orofacial Motor Actions
Lauren McElvain (2018)
10.1371/journal.pone.0207069
Characterization of sensory neuronal subtypes innervating mouse tongue
Ping Wu (2018)
10.1007/s00455-012-9432-y
New Directions for Understanding Neural Control in Swallowing: The Potential and Promise of Motor Learning
I. Humbert (2012)
10.1186/1752-1947-6-275
Cerebro-afferent vessel and pupillary basal diameter variation induced by stomatognathic trigeminal proprioception: a case report
Vincenzo De Cicco (2012)
10.23736/S0026-4970.18.04156-0
Clinical association between dental malocclusion and strabismus in adolescents: a retrospective dental cast analysis.
Maria Rita Giuca (2019)
10.1016/j.brainresbull.2014.01.007
Involvement of trigeminal mesencephalic nucleus in kinetic encoding of whisker movements
Ombretta Mameli (2014)
10.1186/1752-1947-6-161
Central syntropic effects elicited by trigeminal proprioceptive equilibrium in Alzheimer’s disease: a case report
Vincenzo De Cicco (2012)
Role of Synaptic and Non-Synaptic Mechanisms Underlying Motor Neuron Control
A. L. Revill (2011)
10.1007/s00429-014-0988-1
Neural circuits underlying tongue movements for the prey-catching behavior in frog: distribution of primary afferent terminals on motoneurons supplying the tongue
Szilvia Kecskés (2014)
10.1152/japplphysiol.00398.2019
Unilateral lingual nerve transection alters jaw-tongue coordination during mastication in pigs.
S. Montuelle (2020)
10.14814/phy2.13206
Neurons within the trigeminal mesencephalic nucleus encode for the kinematic parameters of the whisker pad macrovibrissae
O. Mameli (2017)
10.1007/978-1-4614-4466-4_13
Tongue Biomechanics and Motor Control
Mary Snyder Shall (2012)
10.1186/1752-1947-6-161
Central syntropic effects elicited by trigeminal proprioceptive equilibrium in Alzheimer’s disease: a case report
Vincenzo De Cicco (2012)
10.1016/j.expneurol.2014.07.016
Injection of WGA-Alexa 488 into the ipsilateral hemidiaphragm of acutely and chronically C2 hemisected rats reveals activity-dependent synaptic plasticity in the respiratory motor pathways
Janelle L. Buttry (2014)
Face Motor Cortex Neuroplasticity Associated with Alterations in the Oral Environment of the Adult Rat
L. Avivi-Arber (2009)
10.1113/jphysiol.2008.165324
Involvement of ERK phosphorylation in brainstem neurons in modulation of swallowing reflex in rats
T. Tsujimura (2009)
10.1007/978-1-4614-8794-4_3
Neuronal Tract Tracing with Light and Electron Microscopy
J. Zhang (2014)
10.1002/mus.24349
Trigeminal‐hypoglossal silent period: A pontomedullary brainstem reflex
P. Urban (2015)
10.1016/j.brainres.2009.08.024
Anatomical organization of brainstem circuits mediating feeding motor programs in the marine toad, Bufo marinus
R. Mandal (2009)
10.1186/1752-1947-6-275
Cerebro-afferent vessel and pupillary basal diameter variation induced by stomatognathic trigeminal proprioception: a case report
Vincenzo De Cicco (2012)
10.11154/PAIN.24.1
Swallowing reflex is inhibited by orofacial noxious stimulation through ERK phosphorylation in NTS and Pa5 neurons in rats
Takanori Tsujimura (2009)
10.1186/1744-9081-6-69
Role of the trigeminal mesencephalic nucleus in rat whisker pad proprioception
Ombretta Mameli (2010)
Orthodontic tooth movement is associated with orofacial mechanical and thermal hypersensitivities and face sensorimotor cortex neuroplasticity
Mandeep Sood (2014)
10.1016/j.brainres.2012.10.021
Jaw muscle spindle afferents coordinate multiple orofacial motoneurons via common premotor neurons in rats: An electrophysiological and anatomical study
J. Zhang (2012)
10.1016/j.neuroscience.2008.02.034
Inspiratory-phase short time scale synchrony in the brainstem slice is generated downstream of the pre-Bötzinger complex
J. Sebe (2008)
10.18240/ijo.2020.01.05
Is there a primitive reflex residue underlying Marcus Gunn Syndrome? Rat electrophysiology.
Y. Qiao (2020)
10.1016/j.resp.2013.06.004
Central and peripheral factors contributing to obstructive sleep apneas
J. Ramirez (2013)
10.1016/j.jneumeth.2014.08.023
A novel slice preparation to study medullary oromotor and autonomic circuits in vitro
J. Nasse (2014)
An analysis of plasticity in the rat respiratory system following cervical spinal cord injury and the application of nanotechnology to induce or enhance recovery of diaphragm function
J. Walker (2016)
See more
Semantic Scholar Logo Some data provided by SemanticScholar