Electromyography and Fos immunostaining study establish a possible functional link between trigeminal proprioception and the oculomotor system in rats

Abstract

The objective of this study was to explore whether there was a functional link between trigeminal proprioception and the oculomotor system mediated through jaw muscle afferents. Electromyography (EMG) was undertaken of the levator palpebrae (LP) and superior rectus (SR), and Fos expression was detected in the brainstem following consecutive down-stretching of the lower jaw at 2-4 Hz in rats. Retrograde tracing was undertaken of the interstitial nucleus of Cajal and Darkschewitsch nucleus (INC/DN) pre-oculomotor neurons. EMG-like responses were recorded from the LP/SR during down-stretching of the lower jaw at 2-4 Hz in 3 out of 11 rats. Fos expression was induced by consecutive down-stretching of the lower jaw at 2-4 Hz for 20-30 seconds. Interestingly, Fos expression was distributed mainly in the bilateral INC/DN area. We also examined Fos-like immunoreactivity in central mesencephalic and paramedian pontine reticular formation that harbors premotor neurons controlling horizontal eye movement, but no Fos-like staining was observed therein. By injection of retrograde tracers into the oculomotor nucleus combined with Fos immunostaining, double labeled pre-oculomotor neurons were visualized to distribute in the INC/DN. In conclusions, there may exist a trigeminal proprioceptive – oculomotor system neural circuit through jaw muscle afferents in rats. Judging from Fos distribution pattern, this pathway might be related to vertical and torsional eye movements.

Keywords

Marcus Gunn syndrome / down-stretching lower jaw / levator and superior rectus / electromyography / interstitial nucleus of Cajal and Darkschewitsch nucleus / Fos expression

References

[1] Brodsky CM. Pediatric Neuro-Ophthalmology[M]. Second ed. New York, Dordrecht, Heidelberg, London: Springer; 2010.

[2] Pratt SG, Beyer  CK, Johnson CC . The Marcus Gunn phenomenon. A review of 71 cases[J]. Ophthalmology, 1984, 91(1): 27–30.

[3] Saitkowski RM, Glaser  JS. Pediatric neuro-ophthalmology: General considerations and congenital motor and sensory anomalies[M]. 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 1999.

[4] Engle EC. Oculomotility disorders arising from disruptions in brainstem motor neuron development[J]. Arch Neurol, 2007, 64(5): 633–637.

[5] Hotchkiss MG, Miller  NR, Clark AW , Bilateral Duane's retraction syndrome[J]. A clinical-pathologic case report. Arch Ophthalmol, 1980, 98(5): 870–874.

[6] Volk AE, Fricke  J, Strobl J , Analysis of the CHN1 gene in patients with various types of congenital ocular motility disorders[J]. Graefes Arch Clin Exp Ophthalmol, 2010, 248(9): 1351–1357.

[7] Tischfield MA, Baris  HN, Wu C , Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance[J]. Cell, 2010, 140(1): 74–87.

[8] Pieh C, Goebel  HH, Engle EC , Congenital fibrosis syndrome associated with central nervous system abnormalities[J]. Graefes Arch Clin Exp Ophthalmol, 2003, 241(7): 546–553

[9] Conte A, Brancati  F, Garaci F , Kinematic and diffusion tensor imaging definition of familial Marcus Gunn jaw-winking synkinesis[J]. PLoS One, 2012, 7(12): e51749

[10] Basu AP, Bellis  P, Whittaker RG , Teaching NeuroImages: alternating ptosis and Marcus Gunn jaw-winking phenomenon with PHOX2B mutation[J]. Neurology, 2012, 79(17): e153

[11] Nakano M, Yamada  K, Fain J , Homozygous mutations in ARIX(PHOX2A) result in congenital fibrosis of the extraocular muscles type 2[J]. Nat Genet, 2001, 29(3): 315–320.

[12] Pattyn A, Morin  X, Cremer H , Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis[J]. Development, 1997, 124: 4065–4075.

[13] Sona K. Trigemino-oculomotor synkinesis[J]. Neurologia, 1959, 1: 29–51.

[14] Wartenberg R. Winking-jaw phenomenon[J]. Arch Neurol Psychiatry, 1948, 59(6): 734–753.

[15] Sona K. Section of the portio minor of the trigeminal nerve for the treatment of the Marcus Gunn phenomenon[J]. Mod Probl Paediatr, 1977, 18: 258–262.

[16] Lehman AM, Dong  CC, Harries AM , Evidence of ancillary trigeminal innervation of levator palpebrae in the general population[J]. J Clin Neurosci, 2014, 21(2): 301–304.

[17] Hiscock J, Straznicky  C. Peripheral and central terminations of axons of the mesencephalic trigeminal neurons in Xenopus[J]. Neurosci Lett, 1982, 32(3): 235–240.

[18] Luo PF, Wang  BR, Peng ZZ , Morphological characteristics and terminating patterns of masseteric neurons of the mesencephalic trigeminal nucleus in the rat: an intracellular horseradish peroxidase labeling study[J]. J Comp Neurol, 1991, 303(2): 286–299.

[19] Zhang J, Liang  H, Luo P , Unraveling a masticatory- oculomotor neural pathway in rat: Implications for a pathophysiological neural circuit in human[J]? Int J Physiol Pathophysiol Pharmacol, 2011, 3: 280–287.

[20] Fukushima K. The interstitial nucleus of Cajal and its role in the control of movements of head and eyes[J]. Prog Neurobiol, 1987, 29(2): 107–192.

[21] Sharpe JA. Neural control of ocular motor system: Walsh and Hoyt’s Clinical neuroophthalmology[M]. Baltimore, New York, London, Buenos Aires, Hong Kong, Sydney, Tokyo: Lippincott Williams & Wilkins, 1998.

[22] Buttner-Ennever JA . Neuroanatomy of the oculomotor system[M].Amsterdam: Elsevier, 1988.

[23] Iliff CE. The optimum time for surgery in the Marcus Gunn phenomenon[J]. Trans Am Acad Ophthalmol Otolaryngol, 1970, 74: 1005–1010.

[24] Awan KJ. Marcus gunn (jaw-winking) syndrome[J]. Am J Ophthalmol, 1976, 82(3): 503–504.

[25] Liang H, Song  J, Shen D , Co-firing of levator palpebrae and masseter muscles links the masticatory and oculomotor system in humans[J]. J Biomed Res, 2015, 29: 316–320.

[26] Cody FW, Harrison  LM. Responses of cat jaw muscle spindles to passive stretching over the masticatory range[J]. J Physiol, 1975, 245: 67–68.

[27] Luo P, Dessem  D. Inputs from identified jaw-muscle spindle afferents to trigeminothalamic neurons in the rat: a double-labeling study using retrograde HRP and intracellular biotinamide[J]. J Comp Neurol, 1995, 353(1): 50–66.

[28] Dessem D, Donga  R, Luo P . Primary- and secondary-like jaw-muscle spindle afferents have characteristic topographic distributions[J]. J Neurophysiol, 1997, 77: 2925–2944.

[29] Hunt SP, Pini  A, Evan G . Induction of c-Fos-like protein in spinal cord neurons following sensory stimulation[J]. Nature, 1987, 328(6131): 632–634.

[30] King CT, Garcea  M, Spector AC . 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[J]. J Comp Neurol, 2014, 522(11): 2498–2517.

[31] Travers SP, Travers  JB. Taste-evoked Fos expression in nitrergic neurons in the nucleus of the solitary tract and reticular formation of the rat[J]. J Comp Neurol, 2007, 500(4): 746–760.

[32] Ferrini F, Russo  A, Salio C . Fos and pERK immunoreactivity in spinal cord slices: Comparative analysis of in vitro models for testing putative antinociceptive molecules[J]. Ann Anat, 2014, 196(4): 217–223.

[33] Chen YK, Lei  J, Jin L , Dynamic variations of c-Fos expression in the spinal cord exposed to intramuscular hypertonic saline-induced muscle nociception[J]. Eur J Pain, 2013, 17(3): 336–346.

[34] Carpenter MB, Harbison  JW, Peter P . Accessory oculomotor nuclei in the monkey: projections and effects of discrete lesions[J]. J Comp Neurol, 1970, 140(2): 131–153.

[35] Fujita K, Matsuo  K, Yuzuriha S , Cell bodies of the trigeminal proprioceptive neurons that transmit reflex contraction of the levator muscle are located in the mesencephalic trigeminal nucleus in rats[J]. J Plast Surg Hand Surg, 2012, 46(6): 383–388.

[36] Ban R, Matsuo  K, Osada Y , Reflexive contraction of the levator palpebrae superioris muscle to involuntarily sustain the effective eyelid retraction through the transverse trigeminal proprioceptive nerve on the proximal Mueller's muscle: verification with evoked electromyography[J]. J Plast Reconstr Aesthet Surg, 2010, 63(1): 59–64.

[37] Wang N, May  PJ. Peripheral muscle targets and central projections of the mesencephalic trigeminal nucleus in macaque monkeys[J]. Anat Rec (Hoboken), 2008, 291(8): 974–987.

[38] Baker R, Llinas  R. Electrotonic coupling between neurones in the rat mesencephalic nucleus[J]. J Physiol, 1971, 212(1): 45–63.

[39] Curti S, Hoge  G, Nagy JI , Synergy between electrical coupling and membrane properties promotes strong synchronization of neurons of the mesencephalic trigeminal nucleus[J]. J Neurosci, 2012, 32(13): 4341–4359.

Acknowledgments

This work was partially supported by Natural Sciences Research Funding 2006C225 and 2009K01-74 from Shaanxi Province awarded to Dr. Liang HC.

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