Saccadic eye movements direct the high-resolution foveae of our retinas toward objects of interest. With each saccade, the image jumps on the retina, causing a discontinuity in visual input. Our visual perception, however, remains stable. Philosophers and scientists over centuries have proposed that visual stability depends upon an internal neuronal signal that is a copy of the neuronal signal driving the eye movement, now referred to as a corollary discharge (CD) or efference copy. In the old world monkey, such a CD circuit for saccades has been identified extending from superior colliculus through MD thalamus to frontal cortex, but there is little evidence that this circuit actually contributes to visual perception. We tested the influence of this CD circuit on visual perception by first training macaque monkeys to report their perceived eye direction, and then reversibly inactivating the CD as it passes through the thalamus. We found that the monkey's perception changed; during CD inactivation, there was a difference between where the monkey perceived its eyes to be directed and where they were actually directed. Perception and saccade were decoupled. We established that the perceived eye direction at the end of the saccade was not derived from proprioceptive input from eye muscles, and was not altered by contextual visual information. We conclude that the CD provides internal information contributing to the brain's creation of perceived visual stability. More specifically, the CD might provide the internal saccade vector used to unite separate retinal images into a stable visual scene.

Significance statement

Visual stability is one of the most remarkable aspects of human vision. The eyes move rapidly several times per second, displacing the retinal image each time. The brain compensates for this disruption, keeping our visual perception stable. A major hypothesis explaining this stability invokes a signal within the brain, a corollary discharge, that informs visual regions of the brain when and where the eyes are about to move. Such a corollary discharge circuit for eye movements has been identified in macaque monkey. We now show that selectively inactivating this brain circuit alters the monkey's visual perception. We conclude that this corollary discharge provides a critical signal that can be used to unite jumping retinal images into a consistent visual scene.

Before each saccade, neurons in frontal eye field anticipate the impending eye movement by showing sensitivity to stimuli appearing where the neuron's receptive field will be at the end of the saccade, referred to as the future field (FF) of the neuron. We explored the time course of this anticipatory activity in monkeys by briefly flashing stimuli in the FF at different times before saccades. Different neurons showed substantial variation in FF time course, but two salient observations emerged. First, when we compared the time span of stimulus probes before the saccade to the time span of FF activity, we found a striking temporal compression of FF activity, similar to compression seen for perisaccadic stimuli in human psychophysics. Second, neurons with distinct FF activity also showed suppression at the time of the saccade. The increase in FF activity and the decrease with suppression were temporally independent, making the patterns of activity difficult to separate. We resolved this by constructing a simple model with values for the start, peak, and duration of FF activity and suppression for each neuron. The model revealed the different time courses of FF sensitivity and suppression, suggesting that information about the impending saccade triggering suppression reaches the frontal eye field through a different pathway, or a different mechanism, than that triggering FF activity. Recognition of the variations in the time course of anticipatory FF activity provides critical information on its function and its relation to human visual perception at the time of the saccade.

When light falls within a neuronal visual receptive field (RF) the resulting activity is referred to as the visual response. Recent work suggests this activity is in response to both the visual stimulation and the abrupt appearance, or salience, of the presentation. Here we present a novel method for distinguishing the two, based on the timing of random and nonrandom presentations. We examined these contributions in frontal eye field (FEF; N = 51) and as a comparison, an early stage in the primary visual cortex (V1; N = 15) of male monkeys (Macaca mulatta). An array of identical stimuli was presented within and outside the neuronal RF while we manipulated salience by varying the time between stimulus presentations. We hypothesized that the rapid presentation would reduce salience (the sudden appearance within the visual field) of a stimulus at any one location, and thus decrease responses driven by salience in the RF. We found that when the interstimulus interval decreased from 500 to 16 ms there was an approximate 79% reduction in the FEF response compared with an estimated 17% decrease in V1. This reduction in FEF response for rapid presentation was evident even when the random sequence preceding a stimulus did not stimulate the RF for 500 ms. The time course of these response changes in FEF suggest that salience is represented much earlier (<100 ms following stimulus onset) than previously estimated. Our results suggest that the contribution of salience dominates at higher levels of the visual system.SIGNIFICANCE STATEMENT The neuronal responses in early visual processing [e.g., primary visual cortex (V1)] reflect primarily the retinal stimulus. Processing in higher visual areas is modulated by a combination of the visual stimulation and contextual factors, such as salience, but identifying these components separately has been difficult. Here we quantified these contributions at a late stage of visual processing [frontal eye field (FEF)] and as a comparison, an early stage in V1. Our results suggest that as visual information continues through higher levels of processing the neural responses are no longer driven primarily by the visual stimulus in the receptive field, but by the broader context that stimulus defines-very different from current views about visual signals in FEF.