By Marcello Cherchi, MD PhD
For patients
The ophthalmoscope test of the horizontal vestibulo-ocular reflex is a bedside examination that assesses the neurological circuits that connect part of the inner ear’s gyroscope function to certain eye movements. During this test your doctor will look in one of your eyes using an ophthalmoscope, while you use your other eye to stare at a target in the distance. The doctor will gently wiggle the head, turning it from side to side with small movements, while looking in your eye. The test is not uncomfortable. The test takes about 30 seconds to perform. If you normally wear glasses or contact lenses, then you should also wear them for this test. You do not otherwise need any special preparation for this test.
For clinicians
Overview
The rotational vestibulo-ocular reflex (rVOR) maintains an image stable on the retina despite rotational movements of the head. The middle frequency range of the vestibular tuning spectrum can be evaluated at the bedside with the ophthalmoscope test. This test is more sensitive for bilateral vestibular weakness than for unilateral vestibular weakness.
Introduction
There are several methods for assessing the rVOR at the bedside, including the ophthalmoscope test, dynamic visual acuity testing and the head impulse test. The ophthalmoscope test and dynamic visual acuity testing assess the middle frequency range of the vestibular tuning spectrum, while the head impulse test assesses the high range. Assessment of the low range of the rVOR requires instrumented vestibular testing (such as rotatory chair testing).
Physiology and neuroanatomy
The function of the vestibulo-ocular reflex (VOR) is to stabilize an image on the retina despite rotational and/or translational movements of the head (Rinaudo et al. 2019). Ideally the rotational VOR (rVOR) should rotate the eyes within the orbits by an amount that is equal in magnitude, but opposite in direction, to that of the head, thereby offsetting the head movement and maintaining the point of regard stable on the fovea (in other words, the gain of eye rotation to head rotation is 1.0).
The neuroanatomy of the rVOR is well understood (Bronstein et al. 2015). The ophthalmoscope test (to be described in greater detail below) assesses the component of the rotational vestibulo-ocular reflex mediated by the lateral semicircular canals, also called the horizontal rVOR (hrVOR).
Note that the VOR can be assessed for any pair of coplanar semicircular canals; the relevant neuroanatomy is different for each canal (Bronstein et al. 2015).
Equipment needed
This test can be performed with a standard ophthalmoscope.
How to perform the test
In simple terms, the ophthalmoscope test (Eggers and Zee 2003; Hain and Cherchi 2021; Kheradmand and Zee 2012) involves instructing the patient to maintain gaze fixed on a distant target while the examiner uses an ophthalmoscope to view the optic disc, and the examiner oscillates the patient’s head slightly (around 5 – 10 degrees) around the vertical axis. Note that this oscillatory motion is passive (Eggers and Zee 2003). If the patient’s horizontal rVOR is intact, then the retina should appear stable to the examiner. If the patient’s horizontal rVOR is deficient (hypoactive), then the examiner will observe the retina oscillating opposite the direction of the patient’s head. If the patient’s horizontal rVOR is excessive (hyperactive), then the examiner will observe the retina oscillating in the same direction as the patient’s head. Kheradmand and Zee explain it thus:
“The rVOR can… be evaluated during ophthalmoscopy. The head is oscillated horizontally or vertically (about two cycles per second), the subject fixes on a distant target, and then one eye is covered and the disc of the other is observed while the subject imagines still looking at the distant target. The observer notes the direction of motion of the optic disc relative to the direction of motion of the head. If the VOR is intact the optic disc does not move, as movement of the eye in the orbit is equal and opposite to the movement of the head. If the disc appears to move in the opposite direction to the head the reflex is hypoactive, and if it moves in the same direction the reflex is hyperactive. Finally, one must remember that if subjects habitually wear corrective spectacles their VOR gains will be adaptively adjusted to their habitual viewing condition, so during head rotation the VOR can appear hyperactive if the spectacles correct for farsightedness (hyperopia), or hypoactive if the spectacles correct for nearsightedness (myopia). Alternatively, one can rotate the head during ophthalmoscopy while subjects wear their corrective spectacles” (Kheradmand and Zee 2012).
The VOR adapts by altering its gain (Watanabe et al. 2003). The most common circumstance in which such adaptation occurs is when a patient dons refractive lenses (spectacles or contact lenses) to correct for hyperopia (farsightedness) or myopia (nearsightedness) (Cannon et al. 1985). Such adaptive changes in the rVOR gain occur relatively quickly and can be durable even after the refraction is discontinued (Mahfuz et al. 2020). This phenomenon applies mostly to spectacles, because contact lenses move with the eyeball and thus do not induce adaptive changes to the rVOR (Eggers and Zee 2003).
Because of this, if a patient habitually uses lenses (whether spectacles or contact lenses) for visual correction, then they should also wear them during the ophthalmoscope test (Hain and Cherchi 2021; Kheradmand and Zee 2012), otherwise the examiner may elicit false positive results.
The ophthalmoscope test described above induces activity in the lateral semicircular canals. This test can also be performed to assess the vertical semicircular canals, though this movement is more difficult to execute at the bedside and is less commonly used.
What this tests
The ophthalmoscope test as described above assesses the middle frequency range of the horizontal rVOR, and thus the underlying neuroanatomical pathways of the vestibulo-ocular reflex. A lesion anywhere along this pathway can reduce or abolish the horizontal rVOR.
How to interpret the test results
If the patient’s rVOR is deficient (hypoactive), then the examiner will observe the retina oscillating opposite the direction of the patient’s head. If the patient’s rVOR is excessive (hyperactive), then the examiner will observe the retina oscillating in the same direction as the patient’s head.
The ophthalmoscope test is more sensitive for bilateral vestibular weakness than for unilateral vestibular weakness.
Limitations
This test requires that the patient have sufficient cervical rotational motion. Patients with cervical vertebral fusions, or significant cervical arthritis or cervicalgia, or other limitations on cervical range of motion, may be unable to perform this test.
Pitfalls
This test will be difficult to interpret, or uninterpretable, in patients with strabismus, or in patients whose visual impairment precludes them from foveating a target adequately.
Note that the oscillatory motion in this test is passive (Eggers and Zee 2003); the examiner moves the patient’s head passively because active rotation (i.e., movement under the patient’s volition) slightly improves gain (Della Santina et al. 2002; Goebel et al. 2000), though whether this meaningfully influences test results is unclear (Furmen and Durrant 1998).
If a patient habitually uses corrective refractive lenses (whether spectacles or contact lenses), then they should also wear these during the ophthalmoscope test, otherwise there may be false positive results.
Diseases that may be diagnosed by this test
The ophthalmoscope test of the horizontal rotational vestibulo-ocular reflex is particularly helpful in identifying bilateral vestibular weakness, of which there are many etiologies. It is less helpful in identifying unilateral vestibular weakness, which in turn may have many etiologies.
References
Bronstein AM, Patel M, Arshad Q (2015) A brief review of the clinical anatomy of the vestibular-ocular connections-how much do we know? Eye (Lond) 29: 163-70. doi: 10.1038/eye.2014.262
Cannon SC, Leigh RJ, Zee DS, Abel LA (1985) The effect of the rotational magnification of corrective spectacles on the quantitative evaluation of the VOR. Acta Otolaryngol 100: 81-8. doi: 10.3109/00016488509108591
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: 1044-54.
Eggers SD, Zee DS (2003) Evaluating the dizzy patient: bedside examination and laboratory assessment of the vestibular system. Semin Neurol 23: 47-58. doi: 10.1055/s-2003-40751
Furmen JM, Durrant JD (1998) Head-only rotational testing in the elderly. J Vestib Res 8: 355-61.
Goebel JA, Isipradit P, Hanson JM (2000) Manual rotational testing of the vestibulo-ocular reflex. Laryngoscope 110: 517-35. doi: 10.1097/00005537-200004000-00004
Hain TC, Cherchi M (2021) Vestibular Testing. CONTINUUM: Lifelong Learning in Neurology 27: 330-347. doi: 10.1212/CON.0000000000000978
Kheradmand A, Zee DS (2012) The bedside examination of the vestibulo-ocular reflex (VOR): an update. Rev Neurol (Paris) 168: 710-9. doi: 10.1016/j.neurol.2012.07.011
Mahfuz MM, Schubert MC, Figtree WVC, Migliaccio AA (2020) Retinal Image Slip Must Pass the Threshold for Human Vestibulo-Ocular Reflex Adaptation. J Assoc Res Otolaryngol 21: 277-285. doi: 10.1007/s10162-020-00751-6
Rinaudo CN, Schubert MC, Figtree WVC, Todd CJ, Migliaccio AA (2019) Human vestibulo-ocular reflex adaptation is frequency selective. J Neurophysiol 122: 984-993. doi: 10.1152/jn.00162.2019
Watanabe S, Hattori K, Koizuka I (2003) Flexibility of vestibulo-ocular reflex adaptation to modified visual input in human. Auris Nasus Larynx 30 Suppl: S29-34. doi: 10.1016/s0385-8146(02)00134-7
