Translational movements include standing up from a seated position (a vertical translation) or accelerating in a car (a horizontal translation). Changes relative to gravity include lying down in bed from an upright position and tilting the head forward to look at one’s feet. Further examples would include keeping your eyes on a telephone pole when one is traveling on a train, or watching a musician while swaying to their music.
The VOR associated with translations of the head is referred to as the translational VOR (tVOR), and the utricle and the saccule use similar mechanisms to the semicircular canals in order to signal that the head is translating or changing its position relative to gravity.
When one is translating forward or backward and looking at a target to the right or left, a horizontal eye movement is called for; if looking up or down, a vertical eye movement is called for, and if looking straight ahead, a convergence or divergence eye movement is called for1.
(vv)Head Shaking Heave.mp4(tt)
The translational VOR (tVOR) is mediated by the otolith organs, sensitive to linear head acceleration, and it produces a slow phase that compensates for head translation. For example, sideways motion to the left results in a horizontal rightward eye movement to maintain visual stability on an object of interest2.
These translational movements may be:
- Heave: Side-to-side (interaural)
- Bob: Up and down (vertical)
- Surge: Fore and aft (anterior-posterior)
The patient shows a deficit of normal translational VOR with respect to the heave plane: after a displacement in the heave plane, there is displacement of the eyes, and then a catch-up saccade (analagous to the head impulse test of which assesses horizontal semicircular canal function).
(vv)Heave.mp4(tt)
From: Halmagyi GM. Clinical Examination of the Vestibular System. J Vestib Res. Teaching Course, 29th Bárány Society Meeting, Lecture 2, June 5, 2016, Seoul, Korea. From: https://www.youtube.com/watch?v=ehR7SOlBBow
In addition to head translation, target location will also determine the appropriate tVOR response. Unlike the rVOR, a translational displacement must be compensated by both an eye rotation as well as a change in amplitude of eye movement that depends on target proximity. These movements can be very complex, since, for example, during forward motion, the retinal slip of a nearby object differs in both size and direction, depending on its location within the visual field. The goal of the tVOR is to selectively stabilize images on the fovea. Thus, the two eyes may move dysconjugately, with eye movements consisting of either purely vergence or a combination of vergence and conjugate eye movements. For example, as one fixates on an object and also moves (translates) the head forwards or backwards, the eyes will converge and diverge respectively.
The effects of translational displacement are therefore:
- Rotation: For example, during the same lateral displacement, nearby objects move larger distances on the retina, whereas farther objects move smaller distances: if a nearby object needs to be stabilized on the retina, the eyes should rotate by an amount that is larger the closer the target is to the subject. Thus, a train passenger who fixates on a nearby tree will have to generate a larger compensatory eye movement than if they were to fixate on a tree far off in the distance. Note also that since the size of the eye movement varies, depending on how close or far the object of regard may be, only one target can be stabilized on the fovea at any time.
- Amplitude: The translational VOR compensates for linear head movements by generating eye movements that are highly dependent on the subject’s viewing distance3. Since the amplitude and direction of the tVOR depend on the point of regard, the amplitude will increase for near targets and the direction may have to change when the target is eccentric. For example, when moving fore and aft, if one looks straight ahead, the correct response of the tVOR is convergence and divergence respectively, whereas if one looks to the side the tVOR will have a disconjugate horizontal component. For example, when the head translates to the right, the tVOR can rotate the eyes to the left to compensate for the relative motion of near targets on the retina.
Disynaptic and polysynaptic pathways, from the contralateral and ipsilateral utricles respectively, connect with the vestibular nuclei which generate compensatory eye movements, for example a shift of the head (head translation) to the right brings about compensatory eye movements to the left. These polysynaptic pathways likely involve a host of brainstem structures, including an extensive network of projections within the cerebellum, the nodulus and ventral uvula, as well as the fastigial nucleus, the anterior vermis, and the flocculus/ventral paraflocculus4.
Stabilizing the Visual Environment while Translating
The brain must decide whether to stabilize a particular image of a near object on the fovea OR to minimize image motion relative to the background; both are not possible at once.
Remarkably, the tVOR does not generate the necessary eye movements that would be required in order to perfectly stabilize the image of a near object on the fovea. Although the tVOR is capable of generating larger and faster eye movements than actually occur during natural viewing, the brain deliberately chooses a set-point that minimizes the relative image motion of the object of regard with respect to its background: it appears likely that the brain chooses the compromise set-point for the gain of the tVOR (the amplitude of compensatory movement for a head translation at a given viewing distance) that is optimal for overall visual performance during locomotion, taking into account retinal image slip of the target with respect to the background5.
There is an additional visual phenomenon of importance for the tVOR, which is optic flow, the pattern of apparent motion of objects, surfaces, and edges in a visual scene caused by the relative motion between an observer and the scene. The optic flow pattern of forward translation is characterized by objects in the periphery moving to a greater degree across the retina, whereas objects closer to the fixation point move less.
The tVOR and the ability to manipulate retinal flow by generating compensatory eye movements during translation, and thereby to optimize visual acuity on the central retina, is a specific feature of the primate and human visual systems. By contrast, lateral eyed species, such as the rabbit, lack both a fovea and a smooth pursuit system, and are not able to generate eye movements that compensate for the visual consequences of translation during self-motion. Unlike the rabbit, in the primate oculomotor system, image stabilization during translation is critical for foveal vision and stereovision.
From: Cornelissen, Frans & Dobbelsteen, John. (2009). Heading detection with simulated visual field defects. Visual Impairment Research. 1. 71-84. 10.1076/vimr.1.2.71.4412.