The origin of eye movements ‘. . .lies in the need to keep an image fixed on the retina, not in the need to scan the surroundings’1. Scanning our environment, by using exploratory saccades, is a later development, and likely corresponds to the development of a fovea. Note that the retinal fovea is a specialization of the visual system that is widespread among vertebrates, but among mammals is restricted to one of two primate suborders, which includes tarsiers, monkeys and apes.
It is not surprising that the rotational VOR represents a phylogenetically ancient reflex. Many invertebrates and all vertebrate species, from amphibians, reptiles, and birds, to nonhuman primates, have the ability to reflexively rotate their eyes opposite to the direction of head rotation, keeping the visual world stable on the retina. By the Ordovician period, at least 450 million years ago, the first fishes already had a vestibulo-ocular reflex in which rotations of the head during swimming evoked compensatory movements of the eyes2. Synchronously, a second reflex evolved, the optokinetic reflex (OKR) which responded to retinal motion signals via the optic tectum, the purpose of which was also to keep visual images steady.
With the advent of modern fish (about 100 million years ago), the vestibular labyrinth reached its peak of development, and there has been relatively little change in its structure since then: the three semi-circular canals, the utricle, and the saccule are similar in all higher vertebrates3.
With respect to the development of saccades, as a fish swims and turns, the eyes would potentially become pushed to one side by the VOR: a mechanism is required to return them to a central point in the orbit1. Hence, there are recentring movements to return the eyes to the middle of the orbit; these recentring movements are the precursors to saccades, and share characteristics of saccades in that they are fast. When saccades are associated with targeting and fixating on an object, they are always associated with the development of a fovea. In goldfish, toads and rabbits, all of which lack a fovea, novel objects do not elicit a saccadic eye movement. Humans have evolved to have a "saccade and fixate" strategy, illustrating that with foveation, we have evolved from primarily having eye movements devoted to image stabilisation to eye movements concerned with identifying novel environmental stimuli in our visual fields.
With respect to the connections of the vestibular system to the vestibular nuclei:
- In invertebrates and early vertebrates, secondary connections of the vestibular nuclei are primarily vestibulospinal, in keeping with their major role in maintaining body orientation.
- In primates, vestibulospinal connections are less prominent. The lateral vestibular nucleus (Deiter’s) is small, and, by contrast, the superior vestibular nucleus is prominent in humans, where it is the major source of vestibulo-ocular fibers, and gives rise to the medial longitudinal fasciculus. In addition, vestibulocerebellar connections become progressively more prominent in higher vertebrates.
Across different species, the radii of curvature of the semicircular canals are, in general, related to the size of the animal, larger animals have larger canals. The functional significance is that large diameter canals are more sensitive than small canals because the longer tube of fluid exerts more pressure on the hair cells. Larger, more ponderous animals thereby preserve the rotational sensitivity of their semicircular canals despite their slower movements3.
Within the primates, and even the family Hominidae, there is an interesting deviation: the anterior and posterior canals of the human vestibular organs are enlarged in size relative to the horizontal canal, whereas in other species the three canals are relatively equal in size . The significance of this is that the anterior and posterior canals are orientated to sense rotation in the vertical planes, the movements that are important for controlling upright balance. Fossil skulls of early primates believed to have been obligatorily bipedal, such as Homo erectus, show the semicircular canal pattern of modern Homo sapiens, whereas those of nonobligatory bipedal species, such as Australopithecus africanus, show canals that resemble more those of non-human primates. Thus, the evolution of large vertical canals appears to have accompanied the evolution of bipedalism, suggesting that the anterior and posterior canals are important for bipedal balance4.
This comparison reveals several features: The alligator posterior (PC) and anterior semicircular canals (AC) are at distinct angles relative to each other (∼45–55 degrees), producing a triangular shape which is similar to the Allosaurus. By contrast, the homologous semicircular canals in birds and mammals are more at right angles to one another.
Also in alligators and crocodiles, there is a sharp turn of the horizontal canal (HC) near the ventral end of the posterior canal, where it begins to continue into the anterior canal. This is similar to the horizontal canal morphology seen in Allosaurus, but distinct from the more gradual bend or arc of the horizontal canal in birds5.
Redrawn from: Rogers SW. Allosaurus, crocodiles, and birds: evolutionary clues from spiral computed tomography of an endocast. Anat Rec. 1999;257(5):162?173. doi:10.1002/(SICI)1097-0185(19991015)257:5<162::AID-AR5>3.0.CO;2-W
Lateral eyed species, like the rabbit, that lack a fovea and a smooth pursuit system, do not generate eye movements that compensate for the visual consequences of translation during self-motion, in part since there is no particular value in stabilising images in the absence of a fovea.
The rabbit visual system is completely different to that of primates, since it is designed to quickly and effectively detect approaching predators from almost any direction. The eyes are placed high and to the sides of the skull, allowing the rabbit to see nearly 360 degrees, as well as far above the head. Rabbits have a retina with a horizontal area of high photoreceptor density, the visual streak, which allows the rabbit to concentrate on all points of the horizon at one time, enabling it to be aware of a predator coming from any direction. They are also farsighted, which explains why they may be frightened by an airplane flying overhead, since they would tend to misinterpet the plane as a bird of prey.
From: Hughes A. Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc Ophthalmol. 1971;30:33-159.
Information Gathering
In humans, all other vertebrates, and in invertebrates with good eyesight, there is one pattern of eye movements that is almost universal: the pairing of fast gaze-shifting movements, saccades, with periods of stable gaze (fixations)2. To understand their origin, it is necessary to return to return to vestibular reflexes: when a fish makes a turn, the eyes will become trapped at the limit of their range, and a mechanism is needed to return them to a central point in the orbit. These movements need to be fast, since vision will not be possible or desirable during the reset, and this seems to be where the need for saccades originated, that is, saccades evolved initially as movements to recentre eye direction when an animal turned. In animals with good eyesight in all major phyla, this ‘saccade and fixate’ system has been adapted for a second use, which is for targeting particular objects in the surroundings for improved resolution. This is always associated with a region of high resolution on the retina, either an area of elevated retinal ganglion cell density, as in a cat, or a smaller distinct fovea, as in a pipefish, chameleon, hawk or primate. These targeting movements do not occur in vertebrates without a fovea, such as goldfish, toads and rabbits (see above), and in these species, the appearance of a novel object does not provoke a saccade.
Saccades are critical to bring novel objects of interest onto the fovea, but they also require an additional system: that of ocular stabilisation, in order that the relatively slow visual system is able to extract details of a novel object. Naturally, many objects are not still, and therefore a mechanism for ocular tracking of an object needed to evolve. The very accurate gaze holding and fixating mechanisms are the VOR and OKN, but there must also be mechanisms which allow for precise pursuit of a target of interest. Pursuit requires the cancellation of the VOR and OKN, which keep the image stationary. Pursuit eye movements therefore allow the eye to move with the target and for the background to drift. This is easily demonstrated as one tracks one's moving finger, noting that the finger remains in focus, being kept in central vision, whilst the background blurs. Pursuit appears to be confined to primates, and to a very limited degree in cats.
With binocular vision, objects may be tracked at any distance, so long as the foveas can converge on the target. This is as opposed to the situation in rabbits where objects are tracked with the head and not the eyes.
Evolution of the Ocular Tilt Reaction (OTR)
The OTR has been attributed to the emergence of a phylogenetically old response, best appreciated in lateral-eyed animals, since in humans it has been largely superseded by mechanisms that are optimized for binocular, foveate, and frontal-eyed vision. In the case of a rabbit which undergoes a lateral roll tilt, with one ear down and the other up. If the rabbit’s eyes are roughly centered in the orbit one eye should go up and the other down to keep the horizontal meridians of the retinas of the rabbit aligned along the horizon.
The hypothesis is that in the face of a lesion resulting in an utricular-ocular imbalance in humans, the phylogenetically older response emerges, and this manifests as a skew deviation in frontal-eyed animals7. The relative preponderance of the individual components of head tilt, ocular torsion, and vertical eye movements, is dependent upon species differences in the range of head movement and the orientation of the optic axes8. Under normal physiological conditions in humans, the voluntary or involuntary tilting of the head is the major component, and only a relatively small ocular counterroll is necessary since the head movement compensates so well. This is clearly seen in skiers and motorcyclists: as the body tilts, the head realigns correctly with gravitational vertical.
In pathological conditions, all three components of the OTR are present.
- Torsional eye movement (known as ocular counter roll) is most prominent in frontal-eyed animals such as cat and humans.
- Skew eye movement is most prominent in animals with mobile, laterally placed eyes, but no head movement in roll, such as fish and rabbits; in these lateral-eyed animals, a body tilt around the long axis produces a rotation of the eyes that is purely vertical. Body tilt in these animals leads to relatively marked compensatory skew: if the rabbit or fish turns their bodies to the right, the lower right eye will rotate upwards, and the left eye will rotate downwards8. By contrast, in humans there is minimal skew deviation under physiological conditions, and it is likely that frontal eyed animals have evolved to inhibit the reflex in order to maintain single binocular vision.
From: https://en.wikipedia.org/wiki/Allosaurus#/media/File:Allosaurus4.jpg