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Characterizing high-velocity angular vestibulo-ocular reflex function in service members post-blast exposure

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Abstract

Blasts (explosions) are the most common mechanism of injury in modern warfare. Traumatic brain injury (TBI) and dizziness are common sequelae associated with blasts, and many service members (SMs) report symptoms worsen with activity. The purpose of this study was to measure angular vestibulo-ocular reflex gain (aVOR) of blast-exposed SMs with TBI during head impulse testing. We also assessed their symptoms during exertion. Twenty-four SMs recovering from TBI were prospectively assigned to one of two groups based on the presence or absence of dizziness. Wireless monocular scleral search coil and rate sensor were used to characterize active and passive yaw and pitch head and eye rotations. Visual analog scale (VAS) was used to monitor symptoms during fast walking/running. For active yaw head impulses, aVOR gains were significantly lower in the symptomatic group (0.79 ± 0.15) versus asymptomatic (0.87 ± 0.18), but not for passive head rotation. For pitch head rotation, the symptomatic group had both active (0.915 ± 0.24) and passive (0.878 ± 0.22) aVOR gains lower than the asymptomatic group (active 1.03 ± 0.27, passive 0.97 ± 0.23). Some SMs had elevated aVOR gain. VAS scores for all symptoms were highest during exertion. Our data suggest symptomatic SMs with TBI as a result of blast have varied aVOR gain during high-velocity head impulses and provide compelling evidence of pathology affecting the vestibular system. Potential loci of injury in this population include the following: disruption of pathways relaying vestibular efference signals, differential destruction of type I vestibular hair cells, or selective damage to irregular afferent pathways—any of which may explain the common discrepancy between reports of vestibular-like symptoms and laboratory testing results. Significantly reduced pitch aVOR in symptomatic SMs and peak symptom severity during exertional testing support earlier findings in the chronic blast-exposed active duty SMs.

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References

  • Abeln W, Bienhold H, Flohr H (1981) Influence of cholinomimetics and cholinolytics on vestibular compensation. Brain Res 222:458–462

    Article  CAS  PubMed  Google Scholar 

  • Aw S, Fetter M, Cremer P, Karlburg M, Halmagyi G (2001) Individual semicircular canal function in superior and inferior vestibular neuritis. Neurology 57:768–774

    CAS  PubMed  Google Scholar 

  • Black FO, Wade SW, Nashner LM (1996) What is the minimal vestibular function required for compensation? Am J Otology 17:401–409

    Article  CAS  PubMed  Google Scholar 

  • Brandtberg K, Magnusson M (1990) The dynamics of the vestibulo-ocular reflex in patients with vestibular neuritis. Am J Otolaryngol 11:345–351

    Article  Google Scholar 

  • Cernak I, Savic J, Malicevic Z, Zunic G, Radosevic P, Ivanovic I, Davidovic L (1996) Involvement of the central nervous system in the general response to pulmonary blast injury. J Trauma 40(3 Suppl):S100–S104

    Article  CAS  PubMed  Google Scholar 

  • Cernak I, Wang Z, Jiang J, Bian X, Savic J (2001a) Ultrastructural and functional characteristics of blast injury-induced neurotrauma. J Trauma 50(4):695–706

    Article  CAS  PubMed  Google Scholar 

  • Cernak I, Wang Z, Jiang J, Bian X, Savic J (2001b) Cognitive deficits following blast injury-induced neurotrauma: possible involvement of nitric oxide. Brain Inj 15(7):593–612

    Article  CAS  PubMed  Google Scholar 

  • Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706

    Article  CAS  PubMed  Google Scholar 

  • Della Santina CC, Cremer PD, Carey JP, Minor LB (2002) Comparison of head thrust test with head autorotation test reveals that the vestibulo-ocular reflex is enhanced during voluntary head movements. Arch Otolaryngol Head Neck Surg 128(9):1044–1054

    Google Scholar 

  • Eggert T (2007) Eye movement recordings: methods. Dev Ophthalmol 40:15–34

    Article  PubMed  Google Scholar 

  • Furman JM, Whitney SL (2000) Central causes of dizziness. Phys Ther 80:179–187

    CAS  PubMed  Google Scholar 

  • Goldberg JM, Fernandez C (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey I. Response to static tilts and to long-duration centrifugal force. J Neurophysiol 39(5):970–984

    PubMed  Google Scholar 

  • Goldberg JM, Baird RA, Fernandez C (1985) Morphological studies of the mammalian vestibular labyrinth. Prog Clin Biol Res 176:231–245

    CAS  PubMed  Google Scholar 

  • Gottshall K (2009) Vestibular-visual-cognitive interaction tests in patients with blast trauma. Abstract #180. Association for research in otolaryngology midwinter meeting. Baltimore, Md. 14–19 Feb

  • Gottshall KR, Hoffer ME (2010) Tracking recovery of vestibular function in individuals with blast-induced head trauma using vestibular-visual-cognitive interaction tests. J Neurol Phys Ther 34(2):94–97

    Google Scholar 

  • Grossman GE, Leigh RJ, Abel LA, Lanska DJ, Thurston SE (1988) Frequency and velocity of rotational head perturbations during locomotion. Exp Brain Res 70:470–476

    Article  CAS  PubMed  Google Scholar 

  • Herdman S, Hall C, Schubert M, Das V, Tusa R (2003) Recovery of dynamic visual acuity in unilateral vestibular hypofunction. Arch Otolaryngol Head Neck Surg 129:819–824

    Article  PubMed  Google Scholar 

  • Hoffer M, Gottshall K, Balough B, Balaban C (2008) Vestibular difference between blast and blunt head trauma. 2008. Association for research in otolaryngology abstract number 964. Phoenix Az. 14–18 Feb

  • Hoffer ME, Donaldson C, Gottshall KR, Balaban C, Balough B (2009) Blunt and blast head trauma: different entities. Int Tinnitus J 15(2):115–118

    PubMed  Google Scholar 

  • Hoffer ME, Balaban C, Gottshall K, Balough B, Maddox M, Penta J (2010) Blast exposure: vestibular consequences and associated characteristics. Otol Neurotol 31:232–236

    Article  PubMed  Google Scholar 

  • Hullar TE, Della Santina CC, Hirvonen TP, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93(5):2777–2786

    Article  PubMed  Google Scholar 

  • Husni EA, Bell HS, Storer J (1966) Mechanical occlusion of the vertebral artery. JAMA 196(6):101–104

    Article  Google Scholar 

  • Klam F, Graf W (2003) Vestibular signals of posterior parietal cortex neurons during active and passive head movements in macaque monkeys. Ann NY Acad Sci 1004:271–282

    Article  PubMed  Google Scholar 

  • Kocsis J, Tessler A (2009) Pathology of blast-related brain injury. JRRD 46(6):667–672

    Article  Google Scholar 

  • Leigh J, Zee D (2006) The neurology of eye movements, fourth edition. Oxford University Press, Oxford

    Google Scholar 

  • Mitchell J, Keene D, Dyson C, Harvey L, Pruvey C, Phillips R (2004) Is cervical spine rotation is cervical spine rotation, as used in the standard vertebrobasilar insufficiency test, associated with a measureable change in intracranial vertebral artery blood flow? Man Ther 9:220–227

    Article  PubMed  Google Scholar 

  • Nadol J (1995) Vestibular neuritis. Arch Otolaryngol Head Neck Surg 112:162–172

    Article  Google Scholar 

  • Paige GD (1989) Nonlinearity and asymmetry in the human vestibuloocular reflex. Acta Otolaryngol 108:1–8

    Article  CAS  PubMed  Google Scholar 

  • Park HJ, Migliaccio AA, Della Santina CC, Minor LB, Carey JP (2005) Search-coil head-thrust and caloric tests in Meniere’s disease. Acta Otolaryngol 125:852–857

    PubMed  Google Scholar 

  • Roberts D, Shelhamer M, Wong M (2008) A new “wireless” search-coil system. In: Proceedings of the eye tracking research & applications symposium, Savannah, Georgia, 26–28 March, pp 197–204

  • Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Electron BME 10:137–145

    CAS  Google Scholar 

  • Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142

    CAS  PubMed  Google Scholar 

  • Roy JE, Cullen KE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933

    Article  PubMed  Google Scholar 

  • Roy FD, Tomlinson RD (2004) Characterization of the vestibulo-ocular reflex evoked by high-velocity movements. Laryngoscope 114(7):1190–1193

    Article  PubMed  Google Scholar 

  • Scherer M, Schubert M (2009) TBI and vestibular pathology as co-morbidity following blast exposure. Phys Ther 89(9):980–992

    Article  PubMed  Google Scholar 

  • Scherer M, Burrows H, Pinto H, Somrack E (2007) Characterizing self reported dizziness and otovestibular impairment among blast injured traumatic amputees, a pilot study. Mil Med 172:731–738

    PubMed  Google Scholar 

  • Scherer MR, Migliaccio A, Schubert MC (2008) Effect of vestibular rehabilitation on passive dynamic visual acuity. J Vestib Res 18(2–3):147–157

    PubMed  Google Scholar 

  • Schubert M (2009) Variability in the aVOR to head impulse testing. Association for Research in Otolaryngology Midwinter Meeting. Baltimore, Md. 14–19 Feb

  • Schubert MC, Minor LB (2004) Vestibulo-ocular physiology underlying vestibular hypofunctiton. Phys Ther 84:373–385

    PubMed  Google Scholar 

  • Schubert M, Migliaccio A, Della Santina C (2006) Dynamic visual acuity during passive head thrusts in canal planes. J Assoc Res Otolaryngol 7(4):329–338

    Article  PubMed  Google Scholar 

  • Schubert M, Migliaccio A, Clendaniel R, Allak A, Carey J (2008) Mechanism of dynamic visual acuity recovery with vestibular rehabilitation. Arch Phys Med Rehabil 89:500–507

    Article  PubMed  Google Scholar 

  • Strupp M, Arbusow V, Maag KP, Gall C, Brandt T (1998) Vestibular exercises improve central vestibulospinal compensation after vestibular neuritis. Neurology 51(3):838–845

    CAS  PubMed  Google Scholar 

  • Terrio H, Brenner L, Ivins B et al (2009) Traumatic brain injury screening: preliminary findings in a US army brigade combat team. J Head Trauma Rehabil 24(1):14–23

    Article  PubMed  Google Scholar 

  • VA/DoD Clinical Practice Guideline for Management of Concussion/mTBI (2009) Accessed at http://www.dcoe.health.mil/ForHealthPros/TBIInformation.aspx on 26 July 2010

  • Von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschafften 37:464–476

    Article  Google Scholar 

  • Walker MF, Zee DS (1999) Directional abnormalities of vestibular and optokinetic responses in cerebellar disease. Ann NY Acad Sci 871:205–220

    Article  CAS  PubMed  Google Scholar 

  • Warden D (2006) Military TBI during the Iraq and Afghanistan wars. J Head Trauma Rehabil 21:398–402

    Article  PubMed  Google Scholar 

  • Wiener SI, Berthoz A, Zugaro MB (2002) Multisensory processing in the elaboration of place and head direction responses by limbic system neurons. Brain Res Cogn Brain Res 14:75–90

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We owe a hearty thanks to Dr Americo Migliaccio for his expertise developing the eye movement analysis software, Dr Frank Siewerdt for expertise with the statistical analysis, and to Kara Beaton, Dale Roberts, and Aaron Wong for their expertise implementing the wireless search coil.

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Authors and Affiliations

  1. Department of Physical Therapy and Rehabilitation Science, University of Maryland School of Medicine, Baltimore, MD, USA

    Matthew R. Scherer

  2. Department of Biomedical Engineering, Johns Hopkins School of Medicine, Baltimore, MD, USA

    Mark J. Shelhamer

  3. Department of Otolaryngology Head and Neck Surgery, Johns Hopkins School of Medicine, Baltimore, MD, 21287, USA

    Matthew R. Scherer, Mark J. Shelhamer & Michael C. Schubert

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  1. Matthew R. Scherer
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  2. Mark J. Shelhamer
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  3. Michael C. Schubert
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Correspondence to Michael C. Schubert.

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The views expressed in this manuscript are those of the authors and do not necessarily reflect the official policy or position of the Department of the Army, nor the US Government.

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Scherer, M.R., Shelhamer, M.J. & Schubert, M.C. Characterizing high-velocity angular vestibulo-ocular reflex function in service members post-blast exposure. Exp Brain Res 208, 399–410 (2011). https://doi.org/10.1007/s00221-010-2490-1

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