{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T15:09:47Z","timestamp":1773155387774,"version":"3.50.1"},"reference-count":56,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T00:00:00Z","timestamp":1669593600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003819","name":"Natural Science Foundation of Hubei Province","doi-asserted-by":"publisher","award":["No. 2019CFB411"],"award-info":[{"award-number":["No. 2019CFB411"]}],"id":[{"id":"10.13039\/501100003819","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>In studies of vestibulo-ocular reflex (VOR), the horizontal VOR circuit is much clearer than vertical-torsional VOR. The circuit and mechanism of gravity-related vertical-torsional VOR is probably weak. \u201cSomatosensory vestibular interaction\u201d is a known extra source to facilitate VOR, and cervico-ocular reflex is a representative for torsional VOR compensation. Whereas, how the cervical afferents finally reach the oculomotor system is less documented. Actually, when the head tilts, which generates cervico-ocular reflex, not only the neck muscle is activated, but also the jaw muscle is stretched by gravity dragged mandible and\/or tissue-muscle connection between the mandible and clavicle. We have previously identified a projection from the jaw muscle afferent mesencephalic trigeminal nucleus (Vme) neurons to oculomotor nuclei (III\/IV) and their premotor neurons in interstitial nucleus of Cajal (INC)\u2013a well-known pre-oculomotor center manipulating vertical-torsional eye movements. We hypothesized that these projections may interact with vestibulo-ocular signals during vertical-torsional VOR, because effects of gravity on jaw muscles and bones has been reported. Thus, we injected different anterograde tracers into the Vme and medial vestibular nucleus (MVN)\u2014the subnuclear area particularly harboring excitatory vestibulo-ocular neurons, and immunostained III\/IV motoneurons. Retrograde tracer was injected into the III in the same animals after dual anterograde tracers\u2019 injections. Under confocal microscope, we observed the Vme and MVN neuronal endings simultaneously terminated onto the same III\/IV motoneurons and the same INC pre-oculomotor neurons. We consider that jaw muscle proprioceptive Vme neurons projecting to the III\/IV and INC would sense spindle activity if the jaw muscle is stretched by gravity dragged mandible or connection between mandible and clavicle during head rolling. Therefore, the convergent innervation of the Vme and MVN neurons onto the oculomotor and pre-oculomotor nuclei would be a neuroanatomic substrate for interaction of masticatory proprioception with the vestibulo-ocular signals upon the oculomotor system during vertical-torsional VOR.<\/jats:p>","DOI":"10.1371\/journal.pone.0278205","type":"journal-article","created":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T18:36:13Z","timestamp":1669660573000},"page":"e0278205","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":2,"title":["Convergent innervations of mesencephalic trigeminal and vestibular nuclei neurons onto oculomotor and pre-oculomotor neurons\u2014Tract tracing and triple labeling in rats"],"prefix":"10.1371","volume":"17","author":[{"given":"Yongmei","family":"Chen","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xinrui","family":"Gong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shaimaa I. 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Leigh","year":"2015","edition":"5"},{"key":"pone.0278205.ref003","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1152\/jn.1994.71.3.950","article-title":"Monosynaptic and disynaptic connections in the utriculo-ocular reflex arc of the cat","volume":"71","author":"Y Uchino","year":"1994","journal-title":"Journal of neurophysiology"},{"key":"pone.0278205.ref004","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/0304-3940(80)90334-1","article-title":"Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system","volume":"16","author":"N Ishizuka","year":"1980","journal-title":"Neuroscience letters"},{"key":"pone.0278205.ref005","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/0006-8993(69)90189-9","article-title":"Postsynaptic potentials in abducens motoneurons induced by vestibular stimulation","volume":"15","author":"RG Baker","year":"1969","journal-title":"Brain 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neurophysiology"},{"key":"pone.0278205.ref009","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1007\/s002219900292","article-title":"Sacculo-ocular reflex connectivity in cats","volume":"131","author":"N Isu","year":"2000","journal-title":"Experimental brain research"},{"key":"pone.0278205.ref010","doi-asserted-by":"crossref","first-page":"1896","DOI":"10.1152\/jn.1996.76.3.1896","article-title":"Utriculoocular reflex arc of the cat","volume":"76","author":"Y Uchino","year":"1996","journal-title":"Journal of neurophysiology"},{"key":"pone.0278205.ref011","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1111\/j.1749-6632.1999.tb09175.x","article-title":"A review of otolith pathways to brainstem and cerebellum","volume":"871","author":"JA Buttner-Ennever","year":"1999","journal-title":"Annals of the New York Academy of Sciences"},{"key":"pone.0278205.ref012","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.neulet.2009.07.090","article-title":"Somatosensory input influences the vestibulo-ocular reflex","volume":"463","author":"A Sugita-Kitajima","year":"2009","journal-title":"Neuroscience letters"},{"key":"pone.0278205.ref013","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1007\/s002210050418","article-title":"Eye movements evoked by proprioceptive stimulation along the body axis in humans","volume":"120","author":"T Mergner","year":"1998","journal-title":"Experimental brain research"},{"key":"pone.0278205.ref014","first-page":"2258","article-title":"The role of extraocular proprioception in vestibulo-ocular reflex of rabbits","volume":"30","author":"S Kashii","year":"1989","journal-title":"Investigative ophthalmology & visual science"},{"key":"pone.0278205.ref015","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1113\/jphysiol.1989.sp017529","article-title":"Interactions of cervico-ocular and vestibulo-ocular fast-phase signals in the control of eye position in rabbits","volume":"410","author":"NH Barmack","year":"1989","journal-title":"The Journal of physiology"},{"key":"pone.0278205.ref016","doi-asserted-by":"crossref","first-page":"456","DOI":"10.3109\/00016489109138369","article-title":"Ocular rotation and perception of the horizontal under static tilt conditions in patients without labyrinthine function","volume":"111","author":"W Bles","year":"1991","journal-title":"Acta oto-laryngologica"},{"key":"pone.0278205.ref017","doi-asserted-by":"crossref","first-page":"15","DOI":"10.3233\/VES-1992-2102","article-title":"Influence of visual, vestibular, cervical, and somatosensory tilt information on ocular rotation and perception of the horizontal","volume":"2","author":"B de Graaf","year":"1992","journal-title":"Journal of vestibular research"},{"key":"pone.0278205.ref018","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1002\/cne.903530405","article-title":"Cervical primary afferent input to vestibulospinal neurons projecting to the cervical dorsal horn: an anterograde and retrograde tracing study in the cat","volume":"353","author":"S Bankoul","year":"1995","journal-title":"The Journal of comparative neurology"},{"key":"pone.0278205.ref019","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1002\/cne.903610210","article-title":"Spinovestibular projections in the rat, with particular reference to projections from the central cervical nucleus to the lateral vestibular nucleus","volume":"361","author":"M Matsushita","year":"1995","journal-title":"The Journal of comparative neurology"},{"key":"pone.0278205.ref020","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1007\/s002210100867","article-title":"Ipsilateral and contralateral projections from upper cervical segments to the vestibular nuclei in the rat","volume":"141","author":"G Xiong","year":"2001","journal-title":"Experimental brain research"},{"key":"pone.0278205.ref021","first-page":"141","article-title":"Trigeminal motoneuron responses to vestibular stimulation in the guinea pig","volume":"134","author":"E Tolu","year":"1996","journal-title":"Archives italiennes de biologie"},{"key":"pone.0278205.ref022","doi-asserted-by":"crossref","first-page":"163","DOI":"10.3233\/VES-1993-3205","article-title":"The vestibular system modulates masseter muscle activity","volume":"3","author":"E Tolu","year":"1993","journal-title":"Journal of vestibular research"},{"key":"pone.0278205.ref023","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1113\/jphysiol.2003.047274","article-title":"A short latency vestibulomasseteric reflex evoked by electrical stimulation over the mastoid in healthy humans","volume":"553","author":"F Deriu","year":"2003","journal-title":"The Journal of physiology"},{"key":"pone.0278205.ref024","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1016\/0014-4886(85)90103-7","article-title":"Effects of whole-body rotation on masseteric motoneuron excitability","volume":"89","author":"RS Hickenbottom","year":"1985","journal-title":"Experimental neurology"},{"key":"pone.0278205.ref025","doi-asserted-by":"crossref","first-page":"29","DOI":"10.18240\/ijo.2020.01.05","article-title":"Is there a primitive reflex residue underlying Marcus Gunn Syndrome? Rat electrophysiology.","volume":"13","author":"Y Qiao","year":"2020","journal-title":"International journal of ophthalmology"},{"key":"pone.0278205.ref026","first-page":"382","article-title":"Is Marcus Gunn jaw winking a primitive reflex? Rat neuroanatomy.","volume":"11","author":"HC Liang","year":"2018","journal-title":"International journal of ophthalmology"},{"key":"pone.0278205.ref027","first-page":"280","article-title":"Unraveling a masticatory\u2014oculomotor neural pathway in rat: Implications for a pathophysiological neural circuit in human","volume":"3","author":"J Zhang","year":"2011","journal-title":"International journal of physiologypathophysiology and pharmacology"},{"key":"pone.0278205.ref028","doi-asserted-by":"crossref","first-page":"110210","DOI":"10.1016\/j.mehy.2020.110210","article-title":"A reformed \"release hypothesis\" for Marcus Gunn Syndrome, based on newer clinic observations and experimental evidences","volume":"144","author":"H Liang","year":"2020","journal-title":"Medical hypotheses"},{"key":"pone.0278205.ref029","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1126\/science.2047862","article-title":"Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal","volume":"252","author":"JD Crawford","year":"1991","journal-title":"Science"},{"key":"pone.0278205.ref030","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1196\/annals.1303.011","article-title":"Neural control of three-dimensional eye and head posture","volume":"1004","author":"EM Klier","year":"2003","journal-title":"Annals of the New York Academy of Sciences"},{"key":"pone.0278205.ref031","first-page":"517","article-title":"A study on the relationships between imbalance of stomatognathic function and asymmetry of craniofacial morphology, and the center of gravity of the upright posture","volume":"35","author":"H Ishii","year":"1990","journal-title":"[Osaka Daigaku shigaku zasshi] The journal of Osaka University Dental Society"},{"key":"pone.0278205.ref032","doi-asserted-by":"crossref","first-page":"3012","DOI":"10.1152\/jn.00796.2005","article-title":"Physiological and anatomical properties of mouse medial vestibular nucleus neurons projecting to the oculomotor nucleus","volume":"95","author":"C Sekirnjak","year":"2006","journal-title":"Journal of neurophysiology"},{"key":"pone.0278205.ref033","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1002\/1096-9861(20000911)425:1<97::AID-CNE9>3.0.CO;2-N","article-title":"The normal distribution and projections of constitutive NADPH-d\/NOS neurons in the brainstem vestibular complex of the rat","volume":"425","author":"DW Saxon","year":"2000","journal-title":"The Journal of comparative neurology"},{"key":"pone.0278205.ref034","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1159\/000114352","article-title":"Distribution of the vestibular neurons projecting to the oculomotor and trochlear nuclei in rabbits","volume":"37","author":"JL Labandeira-Garcia","year":"1991","journal-title":"Brainbehavior and evolution"},{"key":"pone.0278205.ref035","volume-title":"The rat brain altlas in stereotaxic coordinates.","author":"G Paxinos","year":"1998","edition":"4"},{"key":"pone.0278205.ref036","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/0301-0082(87)90016-5","article-title":"The interstitial nucleus of Cajal and its role in the control of movements of head and eyes","volume":"29","author":"K Fukushima","year":"1987","journal-title":"Progress in neurobiology"},{"key":"pone.0278205.ref037","doi-asserted-by":"crossref","first-page":"256","DOI":"10.7555\/JBR.31.20160127","article-title":"Electromyography and Fos immunostaining study establish a possible functional link between trigeminal proprioception and the oculomotor system in rats","volume":"31","author":"H Liang","year":"2017","journal-title":"Journal of biomedical research"},{"key":"pone.0278205.ref038","doi-asserted-by":"crossref","first-page":"428","DOI":"10.3171\/jns.1987.67.3.0428","article-title":"Oculomotor nerve regeneration in rats. Functional, histological, and neuroanatomical studies","volume":"67","author":"E Fernandez","year":"1987","journal-title":"Journal of neurosurgery"},{"key":"pone.0278205.ref039","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0006-8993(80)90556-9","article-title":"Localization of motoneurons controlling the extraocular muscles of the rat","volume":"188","author":"MA Glicksman","year":"1980","journal-title":"Brain research"},{"issue":"Pt 2","key":"pone.0278205.ref040","first-page":"247","article-title":"Localisation of motoneurons supplying the extra-ocular muscles of the rat using horseradish peroxidase and fluorescent double labelling","volume":"137","author":"JL Labandeira Garcia","year":"1983","journal-title":"Journal of anatomy"},{"key":"pone.0278205.ref041","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1016\/0006-8993(85)91442-8","article-title":"Differential distribution of 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","volume":"359","author":"S Nomura","year":"1985","journal-title":"Brain research"},{"key":"pone.0278205.ref042","first-page":"P31","article-title":"Gravity-dependent modulation of Ia afferent in human","volume":"6","author":"T Sato","year":"1999","journal-title":"Journal of gravitational physiology"},{"key":"pone.0278205.ref043","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1113\/jphysiol.2003.050443","article-title":"Control of human mandibular posture during locomotion","volume":"554","author":"TS Miles","year":"2004","journal-title":"The Journal of physiology"},{"key":"pone.0278205.ref044","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1016\/S0021-9290(03)00009-5","article-title":"Postural stability of the human mandible during locomotion","volume":"36","author":"SC Flavel","year":"2003","journal-title":"Journal of biomechanics"},{"key":"pone.0278205.ref045","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1002\/cne.903030210","article-title":"Morphological characteristics and terminating patterns of masseteric neurons of the mesencephalic trigeminal nucleus in the rat: an intracellular horseradish peroxidase labeling study","volume":"303","author":"PF Luo","year":"1991","journal-title":"The Journal of comparative neurology"},{"key":"pone.0278205.ref046","volume-title":"Atlas of Human Anatomy","author":"HN Frank","year":"2019","edition":"7"},{"key":"pone.0278205.ref047","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/0165-0173(89)90013-1","article-title":"Mechanisms of recovery following unilateral labyrinthectomy: a review","volume":"14","author":"PF Smith","year":"1989","journal-title":"Brain research Brain research reviews"},{"key":"pone.0278205.ref048","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1097\/WCO.0b013e328341e2b2","article-title":"Ocular torsion and vertical misalignment","volume":"24","author":"JA Sharpe","year":"2011","journal-title":"Current opinion in neurology"},{"key":"pone.0278205.ref049","doi-asserted-by":"crossref","first-page":"171","DOI":"10.3233\/VES-2009-0357","article-title":"Neural substrates underlying vestibular compensation: contribution of peripheral versus central processing","volume":"19","author":"KE Cullen","year":"2009","journal-title":"Journal of vestibular research: equilibrium & orientation"},{"key":"pone.0278205.ref050","doi-asserted-by":"crossref","first-page":"267","DOI":"10.3109\/00016488909139059","article-title":"Ocular counter-rolling as a test of otolith function","volume":"468","author":"SG Diamond","year":"1989","journal-title":"Acta oto-laryngologica Supplementum"},{"key":"pone.0278205.ref051","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1097\/00129492-200401000-00013","article-title":"Cervico-ocular reflex in normal subjects and patients with unilateral vestibular hypofunction","volume":"25","author":"MC Schubert","year":"2004","journal-title":"Otology & neurotology"},{"key":"pone.0278205.ref052","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1007\/BF00234137","article-title":"Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys","volume":"18","author":"J Dichgans","year":"1973","journal-title":"Experimental brain research"},{"key":"pone.0278205.ref053","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1152\/jn.1993.70.1.117","article-title":"Otolith-brain stem connectivity: evidence for differential neural activation by vestibular hair cells based on quantification of FOS expression in unilateral labyrinthectomized rats","volume":"70","author":"GD Kaufman","year":"1993","journal-title":"Journal of neurophysiology"},{"key":"pone.0278205.ref054","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1038\/328632a0","article-title":"Induction of c-fos-like protein in spinal cord neurons following sensory stimulation","volume":"328","author":"SP Hunt","year":"1987","journal-title":"Nature"},{"key":"pone.0278205.ref055","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1002\/cne.23546","article-title":"Restoration of quinine-stimulated Fos-immunoreactive neurons in the central nucleus of the amygdala and gustatory cortex following reinnervation or cross-reinnervation of the lingual taste nerves in rats","volume":"522","author":"CT King","year":"2014","journal-title":"The Journal of comparative neurology"},{"key":"pone.0278205.ref056","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1002\/cne.21213","article-title":"Taste-evoked Fos expression in nitrergic neurons in the nucleus of the solitary tract and reticular formation of the rat","volume":"500","author":"SP Travers","year":"2007","journal-title":"The Journal of comparative neurology"}],"container-title":["PLOS 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