Download PDF
Semin Neurol 2019; 39(06): 775-784
DOI: 10.1055/s-0039-1698742
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Eye Movement Recordings: Practical Applications in Neurology

John-Ross Rizzo
1   Department of Physical Medicine and Rehabilitation, Department of Neurology, Department of Biomedical Engineering, Department of Mechanical and Aerospace Engineering, New York University School of Medicine and New York University Tandon School of Engineering, New York
,
Mahya Beheshti
2   Department of Physical Medicine and Rehabilitation, New York University School of Medicine, New York, New York
,
Weiwei Dai
3   Department of Electrical and Computer Engineering, New York University Tandon School of Engineering, Brooklyn, New York
,
Janet C. Rucker
4   Departments of Neurology and Ophthalmology, New York University School of Medicine, New York, New York
› Author Affiliations
Further Information

Publication History

Publication Date:
17 December 2019 (online)

    Permissions and Reprints

Abstract

Accurate detection and interpretation of eye movement abnormalities often guides differential diagnosis, discussions on prognosis and disease mechanisms, and directed treatment of disabling visual symptoms and signs. A comprehensive clinical eye movement examination is high yield from a diagnostic standpoint; however, skillful recording and quantification of eye movements can increase detection of subclinical deficits, confirm clinical suspicions, guide therapeutics, and generate expansive research opportunities. This review encompasses an overview of the clinical eye movement examination, provides examples of practical diagnostic contributions from quantitative recordings of eye movements, and comments on recording equipment and related challenges.

Keywords

saccades - ocular flutter - nystagmus - video-oculography - eye movements
 

  • References

  • 1 Kerr NM, Chew SS, Eady EK, Gamble GD, Danesh-Meyer HV. Diagnostic accuracy of confrontation visual field tests. Neurology 2010; 74 (15) 1184-1190
    CrossrefPubMedGoogle Scholar
  • 2 Leigh RJ, Zee DS. The Neurology of Eye Movements. 5th ed. New York: Oxford University Press; 2015
    Google Scholar
  • 3 Rucker JC, Tomsak RL. Binocular diplopia. A practical approach. Neurologist 2005; 11 (02) 98-110
    CrossrefPubMedGoogle Scholar
  • 4 Bahill AT, Clark MR, Stark L. The main sequence, a tool for studying human eye movements. Math Biosci 1975; 24: 191-204
    CrossrefPubMedGoogle Scholar
  • 5 Boghen D, Troost BT, Daroff RB, Dell'Osso LF, Birkett JE. Velocity characteristics of normal human saccades. Invest Ophthalmol 1974; 13 (08) 619-623
    PubMedGoogle Scholar
  • 6 Horn AK, Leigh RJ. The anatomy and physiology of the ocular motor system. Handb Clin Neurol 2011; 102: 21-69
    PubMedGoogle Scholar
  • 7 Horn AK, Büttner-Ennever JA, Suzuki Y, Henn V. Histological identification of premotor neurons for horizontal saccades in monkey and man by parvalbumin immunostaining. J Comp Neurol 1995; 359 (02) 350-363
    CrossrefPubMedGoogle Scholar
  • 8 Horn AK, Büttner-Ennever JA. Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification by parvalbumin immunostaining. J Comp Neurol 1998; 392 (04) 413-427
    CrossrefPubMedGoogle Scholar
  • 9 Feldon SE, Unsöld R. Graves' ophthalmopathy evaluated by infrared eye-movement recordings. Arch Ophthalmol 1982; 100 (02) 324-328
    CrossrefPubMedGoogle Scholar
  • 10 Wong AM, McReelis K, Sharpe JA. Saccade dynamics in peripheral vs central sixth nerve palsies. Neurology 2006; 66 (09) 1390-1398
    CrossrefPubMedGoogle Scholar
  • 11 Hardwick A, Rucker JC, Cohen ML. , et al. Evolution of oculomotor and clinical findings in autopsy-proven Richardson syndrome. Neurology 2009; 73 (24) 2122-2124
    CrossrefPubMedGoogle Scholar
  • 12 Leigh RJ, Riley DE. Eye movements in parkinsonism: it's saccadic speed that counts. Neurology 2000; 54 (05) 1018-1019
    CrossrefPubMedGoogle Scholar
  • 13 Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Höglinger GU. Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol 2017; 16 (07) 552-563
    CrossrefPubMedGoogle Scholar
  • 14 West T, Hu Y, Verghese PB. , et al. Preclinical and clinical development of ABBV-8E12, a humanized anti-tau antibody, for treatment of alzheimer's disease and other tauopathies. J Prev Alzheimers Dis 2017; 4 (04) 236-241
    PubMedGoogle Scholar
  • 15 Lloyd-Smith Sequeira A, Rizzo JR, Rucker JC. Clinical approach to supranuclear brainstem saccadic gaze palsies. Front Neurol 2017; 8: 429
    CrossrefPubMedGoogle Scholar
  • 16 Frohman TC, Frohman EM, O'Suilleabhain P. , et al. Accuracy of clinical detection of INO in MS: corroboration with quantitative infrared oculography. Neurology 2003; 61 (06) 848-850
    CrossrefPubMedGoogle Scholar
  • 17 Crane TB, Yee RD, Baloh RW, Hepler RS. Analysis of characteristic eye movement abnormalities in internuclear ophthalmoplegia. Arch Ophthalmol 1983; 101 (02) 206-210
    CrossrefPubMedGoogle Scholar
  • 18 Frohman EM, O'Suilleabhain P, Dewey Jr RB, Frohman TC, Kramer PD. A new measure of dysconjugacy in INO: the first-pass amplitude. J Neurol Sci 2003; 210 (1-2): 65-71
    CrossrefPubMedGoogle Scholar
  • 19 Collewijn H, Erkelens CJ, Steinman RM. Binocular co-ordination of human horizontal saccadic eye movements. J Physiol 1988; 404: 157-182
    CrossrefPubMedGoogle Scholar
  • 20 Foroozan R, Brodsky MC. Microsaccadic opsoclonus: an idiopathic cause of oscillopsia and episodic blurred vision. Am J Ophthalmol 2004; 138 (06) 1053-1054
    CrossrefPubMedGoogle Scholar
  • 21 Pinnock RA, McGivern RC, Forbes R, Gibson JM. An exploration of ocular fixation in Parkinson's disease, multiple system atrophy and progressive supranuclear palsy. J Neurol 2010; 257 (04) 533-539
    CrossrefPubMedGoogle Scholar
  • 22 Otero-Millan J, Serra A, Leigh RJ, Troncoso XG, Macknik SL, Martinez-Conde S. Distinctive features of saccadic intrusions and microsaccades in progressive supranuclear palsy. J Neurosci 2011; 31 (12) 4379-4387
    CrossrefPubMedGoogle Scholar
  • 23 Fahey MC, Cremer PD, Aw ST. , et al. Vestibular, saccadic and fixation abnormalities in genetically confirmed Friedreich ataxia. Brain 2008; 131 (Pt 4): 1035-1045
    CrossrefPubMedGoogle Scholar
  • 24 Brokalaki C, Kararizou E, Dimitrakopoulos A, Evdokimidis I, Anagnostou E. Square-wave ocular oscillation and ataxia in an anti-GAD-positive individual with hypothyroidism. J Neuroophthalmol 2015; 35 (04) 390-395
    CrossrefPubMedGoogle Scholar
  • 25 Rosini F, Federighi P, Pretegiani E. , et al. Ocular-motor profile and effects of memantine in a familial form of adult cerebellar ataxia with slow saccades and square wave saccadic intrusions. PLoS One 2013; 8 (07) e69522
    CrossrefPubMedGoogle Scholar
  • 26 Pretegiani E, Rosini F, Rocchi R. , et al. GABAAergic dysfunction in the olivary-cerebellar-brainstem network may cause eye oscillations and body tremor. Clin Neurophysiol 2017; 128 (03) 408-410
    CrossrefPubMedGoogle Scholar
  • 27 Zee DS, Leigh RJ, Mathieu-Millaire F. Cerebellar control of ocular gaze stability. Ann Neurol 1980; 7 (01) 37-40
    CrossrefPubMedGoogle Scholar
  • 28 Barton JJ, Sharpe JA. Oscillopsia and horizontal nystagmus with accelerating slow phases following lumbar puncture in the Arnold-Chiari malformation. Ann Neurol 1993; 33 (04) 418-421
    CrossrefPubMedGoogle Scholar
  • 29 Bakaeva T, Desai N, Dai W, Rizzo JR, Rucker JC. Increasing velocity slow phases in acquired nystagmus. J Neuroophthalmol 2018; 38 (04) 479-482
    CrossrefPubMedGoogle Scholar
  • 30 Collewijn H, van der Mark F, Jansen TC. Precise recording of human eye movements. Vision Res 1975; 15 (03) 447-450
    CrossrefPubMedGoogle Scholar
  • 31 Sprenger A, Neppert B, Köster S. , et al. Long-term eye movement recordings with a scleral search coil-eyelid protection device allows new applications. J Neurosci Methods 2008; 170 (02) 305-309
    CrossrefPubMedGoogle Scholar
  • 32 van der Geest JN, Frens MA. Recording eye movements with video-oculography and scleral search coils: a direct comparison of two methods. J Neurosci Methods 2002; 114 (02) 185-195
    CrossrefPubMedGoogle Scholar
  • 33 McCamy MB, Otero-Millan J, Leigh RJ. , et al. Simultaneous recordings of human microsaccades and drifts with a contemporary video eye tracker and the search coil technique. PLoS One 2015; 10 (06) e0128428
    CrossrefPubMedGoogle Scholar
  • 34 Raynowska J, Rizzo JR, Rucker JC. , et al. Validity of low-resolution eye-tracking to assess eye movements during a rapid number naming task: performance of the eyetribe eye tracker. Brain Inj 2018; 32 (02) 200-208
    CrossrefPubMedGoogle Scholar
  • 35 Akhand O, Rizzo JR, Rucker JC. , et al. History and future directions of vision testing in head trauma. J Neuroophthalmol 2019; 39 (01) 68-81
    CrossrefPubMedGoogle Scholar
  • 36 Dai W, Selesnick I, Rizzo JR, Rucker J, Hudson T. A nonlinear generalization of the Savitzky-Golay filter and the quantitative analysis of saccades. J Vis 2017; 17 (09) 10
    PubMedGoogle Scholar
  • 37 Nyström M, Holmqvist K. An adaptive algorithm for fixation, saccade, and glissade detection in eyetracking data. Behav Res Methods 2010; 42 (01) 188-204
    CrossrefPubMedGoogle Scholar
  • 38 Dai W, Selesnick I, Rizzo JR. , et al. A parametric model for saccadic eye movement. Paper presented at: Signal Processing in Medicine and Biology Symposium (SPMB), IEEE; December 1–6, 2016
    PubMed