The analysis of image motion by the rabbit retina

1. Micro-electrode recordings were made from rabbit retinal ganglion cells or their axons. Of particular interest were direction-selective units; the common on-off type represented 20.6% of the total sample (762 units), and the on-type comprised 5% of the total.2. From the large sample of direction-selective units, it was found that on-off units were maximally sensitive to only four directions of movement; these directions, in the visual field, were, roughly, anterior, superior, posterior and inferior. The on-type units were maximally sensitive to only three directions: anterior, superior and inferior.3. The direction-selective unit's responses vary with stimulus velocity; both unit types are more sensitive to velocity change than to absolute speed. On-off units respond to movement at speeds from 6'/sec to 10 degrees /sec; the on-type units responded as slowly as 30''/sec up to about 2 degrees /sec. On-type units are clearly slow-movement detectors.4. The distribution of direction-selective units depends on the retinal locality. On-off units are more common outside the ;visual streak' (area centralis) than within it, while the reverse is true for the on-type units.5. A stimulus configuration was found which would elicit responses from on-type units when the stimulus was moved in the null direction. This ;paradoxical response' was shown to be associated with the silent receptive field surround.6. The four preferred directions of the on-off units were shown to correspond to the directions of retinal image motion produced by contractions of the four rectus eye muscles. This fact, combined with data on velocity sensitivity and retinal distribution of on-off units, suggests that the on-off units are involved in control of reflex eye movements.7. The on-off direction-selective units may provide error signals to a visual servo system which minimizes retinal image motion. This hypothesis agrees with the known characteristics of the rabbit's visual following reflexes, specifically, the slow phase of optokinetic nystagmus.