Continuous updating of visuospatial memory in superior colliculus during slow eye movements

Primates can remember and spatially update the visual direction of previously viewed objects during various types of self-motion. It is known that the brain "remaps" visual memory traces relative to gaze just before and after, but not during, discrete gaze shifts called saccades. However, it is not known how visual memory is updated during slow, continuous motion of the eyes.

Here, we recorded the midbrain superior colliculus (SC) of two rhesus monkeys that were trained to spatially update the location of a saccade target across an intervening smooth pursuit (SP) eye movement. Saccade target location was varied across trials so that it passed through the neuron's receptive field at different points of the SP trajectory. Nearly all (99% of) visual responsive neurons, but no motor neurons, showed a transient memory response that continuously updated the saccade goal during SP. These responses were gaze centered (i.e., shifting across the SC's retinotopic map in opposition to gaze). Furthermore, this response was strongly enhanced by attention and/or saccade target selection.

This is the first demonstration of continuous updating of visual memory responses during eye motion. We expect that this would generalize to other visuomotor structures when gaze shifts in a continuous, unpredictable fashion.