Animal Eye Movements

The brain receives visual information about the environment through photoreceptors in the retina, which convert light into electrochemical signals and ultimately into neural activity. This entry describes various experiments on animal eye movements. The spatial orientation of the retina with respect to objects in the world determines what kind of visual information is perceived. Therefore, in all mobile animals the position of the retina with respect to visual objects of interest must be controlled, to ensure that they are aligned and that the retina is stationary with respect to such objects long enough for visual inspection.

An interesting exception are heteropod mol-lusks, which have eyes that are shaped as a long narrow stripe only three to six receptors wide and several hundred receptors long. Their visual field of view is only a few degrees high and 80 to 180 degrees long. At any given time, therefore, most of the surroundings are not seen by the animal. To solve this problem, the heteropods systematically scan the environment with smooth rotating eye movements. It seems likely that the function of these movements is to enable the carnivorous mol-lusks to detect stationary objects in the surrounding water. In contrast, the eye movements of insects, higher crustaceans, cephalopods, and vertebrates have possibly evolved to detect motion, either self-generated as in locomotion, or caused by prey or predators, and that the reason for the maintenance of eye stability is the need to avoid confusion between eye movement and image movement.

The alignment of retina and visual object is controlled by neural mechanisms that either stabilize or shift gaze. Normally, this is achieved by moving the entire eye relative to the body; in some animals, however, only part of the eye is moved. Jumping spiders have excellent vision, with among the highest acuities in invertebrates. Two of their eight eyes, the anterior median eyes (AME), provide high visual acuity but small field of view, and the remaining six eyes provide lower resolution but broad field of view. The AME are long and tubular, which helps their resolution (longer focal length, more magnification) but which means they have a narrow field of view. The AME's have a narrow field of view, so the spider needs to point them in different directions to see objects at different locations. However, the spider cannot move the whole ocular mechanism because the lenses of the eyes are actually built into the carapace. Instead, a special set of muscles moves the retina around, and the lens stays fixed.

Gaze stabilization is also important for animals that cannot move their eyes in their heads at all. For example, insects need to stabilize their gaze during flight. They achieve this by performing very fast (2000 degrees/second) turns of their thorax in mid-flight. These thorax movements start first, and [Page 53]are followed by head movements that are later and more rapid to minimize the time of gaze shift and to maximize the time available for analyzing the surroundings.

Vertebrates use two mechanisms to stabilize the position of the retina with respect to visual objects: the vestibulo-ocular reflex and the optokinetic nystagmus. The vestibulo-ocular reflex (VOR) compensates for movements of the head and relies on vestibular input from the labyrinthine semicircular canals that respond to acceleration of the head. This information is carried by neurons within the vestibular ganglion and relayed to neurons in the vestibular nucleus. These neurons integrate the vestibular input and generate an appropriate compensatory motor response by innervating oculomotor neurons. The vestibular information is much faster than visual information. Thus, the compensatory eye movements generated by the VOR have a latency of 15 milliseconds (ms), whereas eye movements that rely on visual information typically have latencies of more than 70 ms. However, because the VOR relies on information about acceleration, it becomes increasingly unreliable during sustained head rotations with constant velocity and slow acceleration. In this situation, gaze stabilization relies on visual input, using the optokinetic nystagmus (OKN). The compensatory movements generated by this system are slow, but include the full range of motion of the eyes in the head. Long, sustained head movements can lead to large shifts of the eyes. When the eyes reach the outer corners of the oculomotor range, a corrective rapid eye movement moves the eyes in the same direction as the head rotation, which enables inspection of the oncoming visual scene. These rapid eye movements are generated by the same brainstem neurons that are responsible for saccades, and this system is likely the evolutionary precursor of the saccadic gaze-shifting system.

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