Australian and New Zealand Journal of Ophthalmology 1987; 15: 135-138

Council Lecture LOOKING, MOVING AND SEEING

B. A. CRAWFORD Royal Melbourne Hospital

Abstract Why are there eye movements7 To shift images across the retina There is a system for fast centring of an image on the retina, a system for tracking a slowly moving image. and a vestibular system for main taming the same field of view How is the perception of the visual world rendered stable in the face of all these eye movements and yet the movement of particular objects within the environment is accurately seen?

Key words Eye movements, perception of movement, vestibulo-ocular reflex, flight simulation

The object of this lecture is to make sense of the following paradox. Our bodies, heads and eyes are continually on the move, yet we have an overall impression of a stable visual environment. How do we filter out the movement of retinal images induced by the movement of our own eyes and body?

The simplest movement we see is a small object moving on a stationary background, say a pen writing across a page. When another target of interest appears, it forms a peripheral retinal image. A rapid eye movement flicks this image on the fovea. There is a slight programming delay of one-fifth of a second before this saccade gets under way, but once it does it can reach a maximum velocity of a thousand degrees a second (three times round the clock face). If the saccade is small it generally hits the new target. If the saccade is large it tends to undershoot, and a second smaller but accurate shot follows. Most

of our eye movements are saccadic and most are small, only a fraction of a degree.

The intervals between fast eye movements are the fixation periods during which seeing occurs, like photo snapshots. A single day’s visual activity may total a quarter of a million visual fixations, alternating with the same number of saccades. When reading print, the duration of fixation ranges from a short tenth of a second up to three seconds. About three-quarters of all words are individually looked at, so the eyes are still about 90% of the time during reading, and for the rest of the time are flitting about through a small range.

There are several other remarkable features of saccadic eye movements. One is the accuracy of the centring of the image on the fovea. The ocular motor system needs access to a naviga- tional map of the retina: that is to say, whereabouts on the peripheral retina is the image

Council Lecture delivered 29 September 1986 at the 18th Annual Scientific Conference of the Royal Australian College of Ophthalmologists.

Reprinr requests: Dr B. A. Crawford, 200 Drummond Street, Carlton, Victoria 3053, Australia.

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of the target, from which the direction and amplitude of the saccade is computed. The geographic point-to-point ‘relationship between the retina and cerebral visual cortex is well- known, but similar geographic relations exist also for the superior colliculus, the pontine nuclei and the cerebellum. The input for these areas comes from the proportion of optic nerve axons leaving the visual pathway from the optic tract to enter the brainstem. These provide the navigational information for reflex eye movements.

Another remarkable feature is the absence of a perception of movement during a saccade. The evidence is not unanimous either for a retinal or a central origin for visual suppression during saccades. However, in an experiment when the environment was made to move so as to keep up with the saccade, visibility was clear and normal without suppression. It may be that, during a saccade, image movement across the retina exceeds the processing time of the retina for image formation. This is the obverse of the retinal characteristic used for the generation of moving pictures in cinema and video projection so as to lose the appreciation of the blank interval. After all, saccadic duration is very brief in contrast to eyelid blinking, which lasts a relatively long interval of one-third of a second and does allow a detectable sensation of visual interruption, although we generally ignore it.

If the target of interest is more than 10 or 15 degrees off the fovea there is a simultaneous eye and head movement in that direction. In actual sequence a fast saccade flicks the target image on to the fovea. A moment later the head turns towards the target to face it. The saccade is so fast that the image is centred well before the head faces the target. As the head continues to turn, the image is held on the fovea by the eyes turning back in the opposite direction, until the head turn is finished. This movement of the eyes in reverse direction from the head turn is caused by rotary force detectors in the inner ear. This brings me to the maze of canals in the inner ear of the labyrinth.

The original labyrinth of Greek legend in Crete housed the Minotaur beneath the palace of King Minos. The Minotaur had the head of a bull on

a man’s body. Theseus had the role of disposing of the monster. The daughter of Minos was Ariadne and fortunately she and Theseus got on well together. She gave him a ball of string and a sword with which he slew the Minotaur and found his way back out of the labyrinth. But this audience will not escape from the labyrinth so easily.

There are three connecting semicircular canals at right angles to each other. Directional-sensitive hairs of the cupula of a canal are excited by endolymph movement towards them induced by rotation. The otolith organ comprises the saccule and utricle whose directional-sensitive hairs are embedded in a chalky jelly which responds to the linear force of gravity in the upright and recumbent body positions. This linear sensitivity includes not only gravity but also accelerations and decelerations of walking, running, car- driving and any vibrations. As well as maintaining erect posture by spinal reflex muscle action, the otoliths give rise somehow to a sensation or perception of correct vertical uprightness, or “which way is down”, which is the sense of balance or equilibrium.

Rotation of the body or head excites a semicir- cular canal whose input to the vestibular nuclei produces a motor response, turning the eyes in the same plane as the canal but to the opposite side. Turning the head to the right excites the right horizontal canal causing contraction of the ipsilateral medial rectus and contralateral lateral rectus muscles, conjugate gaze to the left. The same rotation inhibits the horizontal canal on the left side. The other canals act similarly in pairs in vertical, oblique and torsional axes.

What does this vestibulo-ocular reflex do? During head rotation it stops the image moving across the retina, keeps the same field of view and gives a still perception of the world. The head can rotate to a maximum speed of 600 degrees per second, whereas the maximum angular velocity of vestibular eye movement is only half of this. The shortfall can be seen subjectively as I shake my head from side to side with gradually increasing speed. At first the surroundings stand still, but with increasing speed of the head my surroundings start to

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oscillate to and fro, as I exceed the capacity of the vestibular system to make a compensatory eye movement fast enough.

We now have two sets of movement infor- mation, one from the retina and the other from the labyrinth. A comparison takes place between these two sets. It is believed that the cerebellum is essential in this process. When the signals match there is a perception of stability of vision, of balance or equilibrium. Any mismatch will produce an erroneous sensation of movement that is disequilibrium.

Andre Du Laurens wrote in AD 1599 “Is it not a witty exploit of nature to close up in so small a hole a drum hard-laced having on the hinder part two small strings and three little bones resembling a forge, a hammer and a stirrup, three small muscles and a labyrinth containing the inward eye?”

Say strong convex spectacles are worn, giving a magnification of one point one in retinal image size. In a head rotation of 100 degrees per second the retinal image reaches 110 degrees per second and there will be an illusion of movement. A cylindrical spectacle lens distorts the movement signal in one meridian only, different from that given by the labyrinth. This disequilibrium in strong glasses always occurs on moving. This is at the heart of the acceptance by patients of the lens implant revolution which freed them from aphakic spectacles. Marked conflict between visual and labyrinthine movement signals will cause motion sickness. Sea sickness on board ship can be eased by gazing at the horizon so that the two movement signals accord better. The reflex response of eye movement from body rotation can be altered, by practice and by disease. The former accounts for skaters’ and ballet dancers’ ability to perform spins and pirouettes without vertigo, and the latter accounts for the generation of nystagmus.

Thus far I have described how our vision remains stable. How then do we see things moving when we should? The smooth pursuit system will hold a slowly moving target on the fovea, but no faster than 30 degrees per second (one clock face hour). The term “pursuit” is therefore more descriptive of its tendency to lag

LOOKING, MOVING A N D SEEING

behind faster targets rather than its speed, as tracking has to be repeatedly augmented by saccades. Let us look at the visual aspect of tracking a moving target.

If I look at my finger moving from side to side across my field of view my initial impression is that my finger is moving. Because I am looking at the finger, tracking it, the image remains on the fovea and the background field of view passes across the retina; so what I perceive initially as a moving finger can by introspection be easily reversed to a fixed finger on a moving background. Here is another example: on a night when a full moon is seen through wind-blown clouds a strong impression arises that the moon is moving, sailing rapidly through the clouds. It takes an effort to remind oneself that the moon is still.

So it is, that when only a part of the visual field moves and the rest is still a perceptual interpre- tation is made. The preference in perception is towards the smaller part of the field to be moving and the larger part to be fixed, because this fits with usual experience and expectation, but as we have just heard, it is not always the correct choice. We call the expected perception reality, and the unexpected illusion. We have moved rapidly from the physiology of vision to its psychology.

I now describe the simulation of aircraft flight. A flight simulator is the nose-end of the actual aircraft mounted on four huge hydraulic pistons which manoeuvre the simulator. On the outside of the cockpit a rack of television sets is mounted facing inwards. These project moving scenes. An enormous cable connects the simulator to a bank of computer cabinets nearby. Inside the cockpit the equipment is complete and functioning. When a programme is chosen a computer graphic construction of a twilight scene at a particular airport fills the cockpit windows to a full field.

Using the controls the engines are started, with proper sound. We let off the brakes, increase power and move along the runway. The lights approach and pass. We feel the vibration as the wheels pass over the runway joints. As we lift off, the runway recedes, and the lights of the city

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with its local landmarks are seen and the horizon drops as we climb. We bank, turn and see the horizon tilt, feel the off-centre gravity force, and an extensive new view over the city is gradually revealed.

The simulated visual movement is obtained by projection of diminishing and increasing size of images, the variation of their speed and direction and the tilting thereof, associated with concordant cockpit inclination and sounds, all coupled to the instrument controls and readings. Thereupon we experience the skill and thrill of flight manoeuvres and navigation, until landing at an airport in another country. One night recently our College President and I flew in the Airbus Simulator to Hong Kong and back. So convincing was the experience that afterwards we felt a sense of regret at having no duty-free purchase. In fact the simulator travelled no further than one metre. You should be encouraged, rather than the reverse, to know that next time you fly your Aircrew will have done virtually all its training on the ground.

In summary, we have seen that for targets moving within the field of vision, where there are sensory clues from the retina only, visual fallacies of movement easily arise. The most frequently

used line of defence against our movements causing visual confusion is the unseeing nature of the retina during saccadic movement of the eyes. The memorable description, 400 years ago, of the labyrinth as the inward eye headlines its role in identifying simulated movement of the environment caused by our moving. And this explains why spectacle lenses, by changing retinal image size, cause difficulty from erroneous sensations of movement. Fortunately, recovery from spectacle-induced disequilibrium usually follows. It depends upon the cerebellar adjustment of the vestibulo-ocular reflex eye movements. Continued practice in the new spectacles alters the eye movement induced by labyrinthine signals of body motion in order to accord with the motion signals from the retina.

References 1. Carpenter RHS. Movements of the eyes. London: PION,

1977. 2. Groner R, Menz C, Fisher DF, eta/, eds. Eye movements

and psychological functions. New Jersey: Lawrence Erlbaum, 1983.

3. Haber RN. Flight simulation. Sci. Am. 1986; 255: 90-97. 4. lgarashi M, Black FO, eds. Vestibular and visual control

on posture and locomotor equilibrium. Basel: Karger, 1985.

5. Maunton RF, ed. The vestibular system. London: Academic Press, 1975.

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