Visual space is compressed in prefrontal cortex before eye movements

TLDR: During saccade preparation, rather than remap, RFs of neurons in a prefrontal gaze control area massively converge towards the saccadic target, resulting in a threefold increase in the proportion of RFs responding to stimuli near the target region.

Abstract: Saccadic eye movements cause substantial shifts in the retinal image as we take in visual scenes, but our perception is stable and continuous; here, visual receptive fields are shown to shift dramatically towards the saccadic goal, running counter to the long-standing hypothesis of receptive field remapping as the basis of perceived stability. As we take in a visual scene we make rapid eye movements — called saccades — that bring different parts of the scene to the fovea, the region of the retina with highest acuity. These eye movements cause substantial shifts in the retinal image, but our perception of the visual world is stable and continuous. Tirin Moore and colleagues find a possible mechanism for this stability in prefrontal neurons. They show that during preparation for eye movement, neurons shift their visual receptive fields (those regions of space that neurons are most responsive to) in order to massively over-represent behaviourally relevant areas, consistent with human visual perception. These findings run counter to a long-standing hypothesis — that receptive fields predictively remap, shifting the representation of visual space by neurons in the brain in anticipation of the outcome of each eye movement. We experience the visual world through a series of saccadic eye movements, each one shifting our gaze to bring objects of interest to the fovea for further processing. Although such movements lead to frequent and substantial displacements of the retinal image, these displacements go unnoticed. It is widely assumed that a primary mechanism underlying this apparent stability is an anticipatory shifting of visual receptive fields (RFs) from their presaccadic to their postsaccadic locations before movement onset1. Evidence of this predictive ‘remapping’ of RFs has been particularly apparent within brain structures involved in gaze control2,3,4. However, critically absent among that evidence are detailed measurements of visual RFs before movement onset. Here we show that during saccade preparation, rather than remap, RFs of neurons in a prefrontal gaze control area massively converge towards the saccadic target. We mapped the visual RFs of prefrontal neurons during stable fixation and immediately before the onset of eye movements, using multi-electrode recordings in monkeys. Following movements from an initial fixation point to a target, RFs remained stationary in retinocentric space. However, in the period immediately before movement onset, RFs shifted by as much as 18 degrees of visual angle, and converged towards the target location. This convergence resulted in a threefold increase in the proportion of RFs responding to stimuli near the target region. In addition, like in human observers5,6, the population of prefrontal neurons grossly mislocalized presaccadic stimuli as being closer to the target. Our results show that RF shifts do not predict the retinal displacements due to saccades, but instead reflect the overriding perception of target space during eye movements.