Asymmetries in vestibular evoked myogenic potentials in chronic stroke survivors with spastic hypertonia: Evidence for a vestibulospinal role

OBJECTIVE Indirect evidence suggests that lateralized changes in motoneuron behavior post-stroke are potentially due to a depolarizing supraspinal drive to the motoneuron pool, but the pathways responsible are unknown. In this study, we assessed vestibular evoked myogenic potentials (VEMPs) in the neck muscles of hemispheric stroke survivors with contralesional spasticity to quantify the relative levels of vestibular drive to the spastic-paretic and contralateral motoneuron pools. METHODS VEMPs were recorded from each sternocleidomastoid muscle in chronic stroke survivors. Side-to-side differences in cVEMP amplitude were calculated and expressed as an asymmetry ratio, a proxy for the relative amount of vestibular drive to each side. RESULTS Spastic-paretic VEMPs were larger than contralateral VEMPs in 13/16 subjects. There was a strong positive relationship between the degree of asymmetry and the severity of spasticity in this subset of subjects. Remaining subjects had larger contralateral responses. CONCLUSION Vestibular drive to cervical motoneurons is asymmetric in spastic stroke survivors, supporting our hypothesis that there is an imbalance in descending vestibular drive to motoneuron pools post-stroke. We speculate this imbalance is a consequence of the unilateral disruption of inhibitory corticobulbar projections to the vestibular nuclei. SIGNIFICANCE This study sheds new light on the underlying mechanisms of post-stroke spasticity.

[1]  Y. Uchino,et al.  Saccular and utricular inputs to sternocleidomastoid motoneurons of decerebrate cats , 1999, Experimental Brain Research.

[2]  M. Leathley,et al.  Prevalence of spasticity post stroke , 2002, Clinical rehabilitation.

[3]  Louise Ada,et al.  The Tardieu Scale differentiates contracture from spasticity whereas the Ashworth Scale is confounded by it , 2006, Clinical rehabilitation.

[4]  E. Liddell,et al.  THE INFLUENCE OF UNILATERAL DESTRUCTION OF THE VESTIBULAR NUCLEI UPON POSTURE AND THE KNEE-JERK , 1930 .

[5]  D Burke,et al.  Spasticity, decerebrate rigidity and the clasp-knife phenomenon: an experimental study in the cat. , 1972, Brain : a journal of neurology.

[6]  Robert Teasell,et al.  Plasticity and Reorganization of the Brain Post Stroke , 2005, Topics in stroke rehabilitation.

[7]  G. Sobue,et al.  Course and distribution of facial corticobulbar tract fibres in the lower brain stem , 2000, Journal of neurology, neurosurgery, and psychiatry.

[8]  J. C. Rothwell,et al.  Motor unit excitability changes mediating vestibulocollic reflexes in the sternocleidomastoid muscle , 2004, Clinical Neurophysiology.

[9]  J. Colebatch,et al.  Galvanic evoked vestibulospinal and vestibulocollic reflexes in stroke , 2004, Clinical Neurophysiology.

[10]  P Molina-Negro,et al.  The role of the vestibular system in relation to muscle tone and postural reflexes in man. , 1980, Acta oto-laryngologica.

[11]  O. Grüsser,et al.  Corticofugal projections to the vestibular nuclei in squirrel monkeys: Further evidence of multiple cortical vestibular fields , 1993, The Journal of comparative neurology.

[12]  D. Basta,et al.  Normative data for P1/N1-latencies of vestibular evoked myogenic potentials induced by air- or bone-conducted tone bursts , 2005, Clinical Neurophysiology.

[13]  D. Denny-Brown.  The extrapyramidal system and postural mechanisms , 1964 .

[14]  K. Kaga,et al.  The effect of sternocleidomastoid electrode location on vestibular evoked myogenic potential. , 2001, Auris, nasus, larynx.

[15]  N. Isu,et al.  Cortical influences on the vestibular nuclei of the cat , 1999, Experimental Brain Research.

[16]  J. Marsden,et al.  The vestibular control of balance after stroke , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[17]  Marc H Schieber,et al.  Bilateral Spike-Triggered Average Effects in Arm and Shoulder Muscles from the Monkey Pontomedullary Reticular Formation , 2007, The Journal of Neuroscience.

[18]  J. Colebatch,et al.  Galvanic and acoustic vestibular stimulation activate different populations of vestibular afferents , 2003, Clinical Neurophysiology.

[19]  C. Heckman,et al.  Adjustable Amplification of Synaptic Input in the Dendrites of Spinal Motoneurons In Vivo , 2000, The Journal of Neuroscience.

[20]  A. Brodal,et al.  Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. , 1968, Brain research.

[21]  P. Nathan,et al.  The rubrospinal and central tegmental tracts in man. , 1982, Brain : a journal of neurology.

[22]  O. Grüsser,et al.  Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey , 1994, The Journal of comparative neurology.

[23]  T. Proffitt,et al.  The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. , 2004, Journal of rehabilitation research and development.

[24]  J. Büttner-Ennever,et al.  Patterns of Connectivity in the Vestibular Nuclei a , 1992, Annals of the New York Academy of Sciences.

[25]  X. Li,et al.  Spastic long-lasting reflexes of the chronic spinal rat studied in vitro. , 2004, Journal of neurophysiology.

[26]  J. Guinan,et al.  Sound-evoked activity in primary afferent neurons of a mammalian vestibular system. , 1997, The American journal of otology.

[27]  W. Rymer,et al.  Spastic hypertonia: mechanisms and measurement. , 1989, Archives of physical medicine and rehabilitation.

[28]  David Burke,et al.  Pathophysiology of spasticity in stroke , 2013, Neurology.

[29]  D. Burke,et al.  Are spinal "presynaptic" inhibitory mechanisms suppressed in spasticity? , 1972, Journal of the neurological sciences.

[30]  C. D. De Luca,et al.  Effects of muscle fiber type and size on EMG median frequency and conduction velocity. , 1995, Journal of applied physiology.

[31]  Richard W. Bohannon,et al.  Interrater reliability of a modified Ashworth scale of muscle spasticity. , 1987, Physical therapy.

[32]  J. Colebatch,et al.  The acoustic startle reflex in ischemic stroke , 2004, Neurology.

[33]  P. Neilson,et al.  Spasticity and muscle contracture following stroke. , 1996, Brain : a journal of neurology.

[34]  H. Barbeau,et al.  Effects of agonists and antagonists of serotonin on spontaneous hindlimb EMG activity in chronic spinal rats , 1981, Neuropharmacology.

[35]  S C Gandevia,et al.  Muscle spindle activity in the affected upper limb after a unilateral stroke. , 1999, Brain : a journal of neurology.

[36]  D. Burke,et al.  Tonic vibration reflex in the cat. , 1971, Journal of neurophysiology.

[37]  Thomas Bauermann,et al.  Occurence and Clinical Predictors of Spasticity After Ischemic Stroke , 2010, Stroke.

[38]  J A Burne,et al.  The spasticity paradox: movement disorder or disorder of resting limbs? , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[39]  Y. Young.  Vestibular evoked myogenic potentials: optimal stimulation and clinical application. , 2006, Journal of biomedical science.

[40]  Trevor Drew,et al.  Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. , 2006, Journal of neurophysiology.

[41]  K Matsuyama,et al.  Organization of the projections from the pericruciate cortex to the pontomedullary brainstem of the cat: A study using the anterograde tracer Phaseolus vulgaris‐leucoagglutinin , 1997, The Journal of comparative neurology.

[42]  R. Nyberg‐hansen,et al.  Sites and mode of termination of fibers of the vestibulospinal tract in the cat. An experimental study with silver impregnation methods , 1964, The Journal of comparative neurology.

[43]  N. Furuya,et al.  Neurotransmitters in the Vestibular Commissural System of the Cat , 1992, Annals of the New York Academy of Sciences.

[44]  D. Burke,et al.  The supraspinal control of the tonic vibration reflex. , 1971, Proceedings of the Australian Association of Neurologists.

[45]  R. Katz,et al.  Impaired efficacy of spinal presynaptic mechanisms in spastic stroke patients. , 2009, Brain : a journal of neurology.

[46]  T. Murofushi,et al.  Effect of head position on vestibular evoked myogenic potentials with toneburst stimuli , 2007, Acta oto-laryngologica.

[47]  M. McCue,et al.  Acoustically responsive fibers in the vestibular nerve of the cat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  H. Hoffman,et al.  The neural substrate of the startle response , 1980, Physiology & Behavior.

[49]  M. Carpenter,et al.  Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey , 1983, Brain Research.

[50]  R. Nyberg‐hansen.  Sites and mode of termination of reticulo‐spinal fibers in the cat. An experimental study with silver impregnation methods , 1965, The Journal of comparative neurology.

[51]  C S Sherrington,et al.  Decerebrate Rigidity, and Reflex Coordination of Movements , 1898, The Journal of physiology.

[52]  Jun Kimura,et al.  Electrodiagnosis in Diseases of Nerve and Muscle: Principles and Practice , 1983 .

[53]  R. Macko,et al.  Muscle molecular phenotype after stroke is associated with gait speed , 2004, Muscle & nerve.

[54]  Richard W. Bohannon,et al.  Relationship between static muscle strength deficits and spasticity in stroke patients with hemiparesis. , 1987, Physical therapy.

[55]  O. Kiehn,et al.  Bistability of alpha‐motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5‐hydroxytryptophan. , 1988, The Journal of physiology.

[56]  H. Magoun,et al.  The vestibular nuclei as an excitatory mechanism for the cord. , 1947, Journal of neurophysiology.

[57]  G M Halmagyi,et al.  Myogenic potentials generated by a click-evoked vestibulocollic reflex. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[58]  D. Denny-Brown,et al.  The nature of dystonia. , 1965, Proceedings of the Australian Association of Neurologists.

[59]  H. Kuypers,et al.  Distribution of corticospinal neurons with collaterals to lower brain stem reticular formation in cat , 2004, Experimental Brain Research.

[60]  Ji Soo Kim,et al.  Medial vestibulospinal tract lesions impair sacculo-collic reflexes , 2010, Journal of Neurology.

[61]  M. Rang,et al.  The spastic mouse. And the search for an animal model of spasticity in human beings. , 1990, Clinical orthopaedics and related research.

[62]  M. V. von Arbin,et al.  Spasticity After Stroke: Its Occurrence and Association With Motor Impairments and Activity Limitations , 2003, Stroke.

[63]  P. Clouston,et al.  The influence of voluntary emg activity and click intensity on the vestibular click evoked myogenic potential , 1995, Muscle & nerve.

[64]  T. Drew,et al.  Organization of the projections from the pericruciate cortex to the pontomedullary reticular formation of the cat: A quantitative retrograde tracing study , 1997, The Journal of comparative neurology.

[65]  William Z Rymer,et al.  Origins of abnormal excitability in biceps brachii motoneurons of spastic-paretic stroke survivors. , 2009, Journal of neurophysiology.

[66]  P. Nathan,et al.  Vestibulospinal, reticulospinal and descending propriospinal nerve fibres in man. , 1996, Brain : a journal of neurology.