Sensorimotor trigeminal unbalance modulates pupil size
Abstract
In order to verify the possible existence of a tonic trigeminal control on autonomic centres, we studied whether patients affected by Temporo-Mandibular Disorder (TMD), showing asymmetric electromyographic (EMG) activity of masticatory muscles also display asymmetries in pupil size. In 30 pain free TMD patients a highly significant, positive correlation was found between left-right differences in EMG and pupil size. The asymmetry in pupil size was induced by the asymmetric sensorimotor signals arising from the orofacial region, since pupils became of about the same size following orthotic correction, which greatly reduced the EMG asymmetry. Moreover, bite wearing bilaterally increased the mydriasis induced by performing haptic tasks. Finally, unbalancing the occlusion by a precontact increased the diameter of the ipsilateral pupil and abolished the mydriasis induced by haptic tasks. In conclusion, trigeminal sensorimotor signals may exert a tonic control on autonomic structures regulating pupil size at rest and during sensorimotor tasks. Since task-associated mydriasis is correlated with task performance and is strictly proportional to the phasic release of noradrenaline at cerebral cortical level, the present findings may suggest an impact of unbalanced trigeminal activity on brain processing not directly related to the orofacial region.
Keywords
Full Text:
PDFReferences
Bartsch T., Jänig W., Häbler H.J Reflex patterns in preganglionic sympathetic neurons projecting to the superior cervical ganglion in the rat. Auton. Neurosci., 83: 66-74, 2000.
Bourque M.J., Kolta A. Properties and interconnections of trigeminal interneurons of the lateral pontine reticular formation in the rat. J. Neurophysiol., 86: 2583-2596, 2001.
Bradley M.M., Miccoli L., Escrig M.A., Lang P.J. The pupil as a misure of emotional arousal and autonomic activation. Psychophysiology, 45: 602-607, 2008.
Bradshaw J. Pupil size as a measure of arousal during information processing. Nature, 216: 515-516, 1967.
Breen L.A., Burde R.M., Loewy A.D. Brainstem connections to the Edinger-Westphal nucleus of the cat: a retrograde tracer study. Brain Res., 261: 303-306, 1983.
Carter M., Yizhar O., Chikahisa S., Nguyen H., Adamantidis A., Nishino S., Deisseroth K., De Lecea L. Tuning arousal with optogenetic modulation of Locus Coeruleus neurons. Nat. Neurosci., 13: 1526-1533, 2010.
Cedarbaum J.M., Aghajanian G.K. Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique. J. Comp. Neurol., 178: 1-16, 1978.
Cooper B.C., Cooper D.L., Lucente F.E. Electromyography of masticatory muscles in cranio-mandibular disorders. Laryngoscope, 101: 150-157, 1991.
Dao T.T., Lavigne G.J., Charbonneau A., Feine J.S., Lund J.P. The efficacy of oral splints in the treatment of myofascial pain of the jaw muscles: a controlled clinical trial. Pain, 56: 85-94, 1994.
De Cicco V. Blood flow variations of cerebro-afferent vessels and of pupillary basal diameters induced by stomatognathic trigeminal proprioception: a case report. J. Med. Case Rep., 6: 275-282, 2012a.
De Cicco V. Central syntropic effects elicited by trigeminal proprioceptive equilibrium in subjects affected by Alzheimer Disease: a case report. J. Med. Case Rep., 6: 161-169, 2012b.
Diagne M., Valla J., Delfini C., Buisseret-Delmas C., Diague P.B. Trigeminovestibular and trigeminospinal pathways in rats: Retrograde tracing compared with glutamic acid decarboxylase and glutamate immunohistochemistry. J. Comp. Neurol., 496: 759-772, 2006.
Dworkin S.F., Fricton J., Hollender L., Huggins K., LeResche L., Lund J., Mohi N., Ohrbach R., Palla S., Sommers E.E., Stohler C., Von Korff M., Widmer C.G. Research diagnostica criteria for temporomandibolar disorders: review, criteria, examinations and specifications critique. J. Craniomandib. Disord., 6: 301-355, 1992.
Elam M., Svensson T.H., Thoren P. Locus coeruleus neurons and sympathetic nerves: activation by cutaneous sensory afferents. Brain Res., 366: 254-261, 1986.
Esser M.J., Pronych S.P., Allen G.V. Trigeminal-reticular connections: Possible pathways for nociception-induced cardiovascular reflex responses in the rat. J. Comp. Neurol., 391: 526-544, 1998.
Gabay S., Pertzov Y., Henik A. Orienting of attention, pupil size and the norepinephrine system. Atten. Percept. Psichophys., 73: 123-129, 2011.
Gilzenrat M.S., Nieuwenhuis S., Jepma M., Cohen J.D. Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function. Cogn. Affect. Behav. Neurosci., 10: 252-269, 2010.
Gomez C.E., Christensen L.V. Stimulus-response latencies of two instruments delivering transcutaneous electrical neuromuscular stimulation (TENS). J. Oral Rehabil., 18: 87-94, 1991.
Hess E.H., Polt J.M. Pupil size in relation to mental activity during simple problem-solving. Science, 143: 1190-1192, 1964.
Karnath H.O., Christ K., Hartje W. Decrease of contralateral neglect by neck muscle vibration and spatial orientation of trunk midline. Brain, 116: 383-396, 1993.
Korszun A., Young E.A., Singer K., Carlson N.E., Brown M.B., Crofford L. Basal circadian cortisol secretion in women with Temporo-mandibular disorders. J. Dental. Res., 81: 279-283, 2002.
Light K., Bragdon E., Grewen K., Brownley K., Girdler S., Maixner W. Adrenergic dysregulation and pain with and without acute beta-blockade in women with fibromyalgia and temporomandibular disorder. J. Pain, 10: 542-252, 2009.
Lomber S.G., Payne B.R. Removal of two halves restores the whole: reversal of visual hemineglect during bilateral cortical or collicular inactivation in the cat. Vis. Neurosci., 13: 1143-1156, 1996.
Matsutani K., Tsuruoka M., Shinya A., Furuya R., Kawawa T. Stimulation of the Locus Coeruleus suppresses trigeminal sensorimotor function in the rat. Brain Res. Bull., 53: 827-832, 2000.
Monaco A., Cattaneo R., Mesin L., Ciarrocchi I., Sgolastra F., Pietropaoli D. Dysregulation of the autonomous nervous system in patients with temporomandibular disorder: a pupillometric study. Plos One, 7: e45424, 2012.
Murphy P.R., O'Connell R.G., O'Sullivan M., Robertson I.H., Balsters J.H. Pupil diameter covaries with BOLD activity in human locus coeruleus. Hum. Brain Mapp., [Epub ahead of print], 2014.
Nnoaham K.E., Kumbang J. Transcutaneous electrical nerve stimulation (TENS) for chronic pain. Cochrane Database Syst. Rev., Issue 3, 2008.
Notsu K., Tumori T., Yokota S., Semine J., Yasui Y. Posterior lateral hypothalamic axon terminal are in contact with trigeminal premotor neurons in the parvicellular reticular formation of the rat medulla oblongata. Brain Res., 1244: 71-81, 2008.
Rajkoski J., Kubiak P., Aston-Jones G. Correlations between locus coeruleus (LC) neural activity, pupil diameter and behaviour in monkey support a role of LC in attention. Pro. Soc. Neurosci. Abs., 19: 974, 1993.
Rorsman I., Magnusson M., Johansson B. Reduction of visuo-spatial neglect with vestibular galvanic stimulation. Scand. J. Rehabil. Med., 31: 117-124, 1999.
Samuels E.R., Szabadi E. Functional neuroanatomy of the noradrenergic locus coeruleus: its roles in the regulation of arousal and autonomic function part I: principles of functional organisation. Curr. Neuropharmacol., 6: 235-253, 2008.
Sato A., Schmidt R.F. Somatosympathetic reflexes: afferent fibers, central pathways, discharge characteristics. Physiol. Rev., 53: 916-947, 1973.
Shammah-Lagnado S.J., Costa M.S., Ricardo J.A. Afferent connections of the parvocellular reticular formation: a horseradish peroxidase study in the rat. Neuroscience, 50: 403-425, 1992.
Sterpenich V., D’Argembeau A., Desseilles M., Balteau E., Albouy G., Vandewalle G., Degueldre C., Luxen A., Collette F., Maquet P. The Locus Coeruleus is involved in the successful retrieval of emotional memories in humans. J. Neurosci., 26: 7416-7423, 2006.
Szabadi E., Bradshaw C. Autonomic pharmacology of α2-adrenoceptors. J. Physicopharmacol., 10 (Suppl 3): s6-18, 1996.
Vallar G., Sterzi R., Bottini G., Cappa S., Rusconi M. Temporary remission of left hemianesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex, 26: 123-131, 1990.
Van Bockstaele E.J., Aston-Jones G. Integration in the ventral medulla and coordination of sympathetic, pain and arousal functions. Clin. Exp. Hypertens., 17: 153-165, 1995.
Yoshihara T., Yawaka Y. Lesion of the ventral ascending noradrenergic bundles decrease the stress response to occlusal disharmony in rats. Neurosci. Lett., 503: 43-47, 2011.
Wilhelm B., Giedke H., Lüdtke H., Bitter E., Hofmann A., Wilheim H. Daytime variations in central nervous system activation measured by a pupillographic sleepness test. J. Sleep Res., 10: 1-7, 2001.
Zhang J., Guan Z. Pathways involved in somatosensory electrical modulation of dorsal cochlear nucleus activity. Brain Res., 1184: 121-131, 2007.
DOI: https://doi.org/10.4449/aib.v152i1.1567
Refbacks
- There are currently no refbacks.