A new category of eye movements in a small fish

One of the main functions of the oculomotor system in vertebrates and most invertebrates is to keep the image of the world relatively still on the retina [1,2]. Eye re-locations are often rapid gaze shifts or ‘saccades’ which move the eyes with high velocity in order to minimise the period during which the image is destabilised [2]. Here, we describe unusual drifting eye movements in a small teleost fish, the sandlance (Limnichthyes fasciatus). This animal breaks the universal rule of image stabilisation by showing large postsaccadic drifts as part of its normal oculomotor repertoire. When observing its environment, the sandlance shows spontaneous monocular saccades to eccentric eye positions in order to locate prey items in the water column above it (Figure 1a); the two eyes are very rarely synchronous. Its oculomotor range is large, covering almost 180 degrees horizontally (rostral to caudal) and 90 degrees vertically (lateral to dorsal) (Figure 1c,d). Between 20% and 40% of the spontaneous saccades are followed by postsaccadic drifts, especially when the saccades are to very eccentric eye positions (Figure 2a–c). The drifts can cover up to 35 degrees of angular distance and their average speed is between 2 and 3 degrees per second (Figure 2c), slower than that of saccades by two orders of magnitude (Figure 2b,c). Drifting leads the eye from an eccentric position back to a more relaxed ‘home position’, which is defined by the most relaxed state of the eye muscles. This indicates that the drift is not visually driven but results from a passive relaxation of the eye muscles after a saccade. Sandlance eye drifts occur after apparently spontaneous as well as visually evoked saccades. During eye movements elicited by rotation of the environment (optokinesis), drifts can be recorded at slow stimulus speeds (our unpublished observations). Sandlances can, however, maintain stable fixation when confronted with prey items in the water column; this alternate oculomotor strategy could perhaps indicate a higher motivational state. Other fish that also feed on small planktonic prey, such as the pipefish (Corythoichthys intestinalis), maintain stable fixation after saccades in all circumstances, and this is so for all other vertebrates whose eye movements have been studied (Figure 1c; [1]). Stabilisation is mediated by a very strong optokinetic mechanism that uses input of the world ‘panorama’ over a large input visual field in order to stabilise the eye. The eye drift in the sandlance shows that this fish can suppress the onset of this powerful reflex, an ability unique among vertebrates, although it is known to occur, for other reasons, in a few invertebrates [1]. Sandlances have a deep pit fovea with the highest ganglion-cell density that has been reported in a R272 Current Biology, Vol 9 No 8