Visual sensitivity of frontal eye field neurons during the preparation of saccadic eye movements

Abstract

Primate vision is continuously disrupted by saccadic eye movements, and yet this disruption goes unperceived. One mechanism thought to reduce perception of this self-generated movement is saccadic suppression, a global loss of visual sensitivity just before, during, and after saccadic eye movements. The frontal eye field (FEF) is a candidate source of neural correlates of saccadic suppression previously observed in visual cortex, because it contributes to the generation of visually guided saccades and modulates visual cortical responses. However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, we recorded the visual responses of FEF neurons to brief, full-field visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (Macaca mulatta) We measured visual sensitivity during both epochs and found that it declines before saccade onset. Visual sensitivity was significantly reduced in visual but not visuomotor neurons. This reduced sensitivity was also present in visual neurons with no movement-related modulation during visually guided saccades and thus occurred independently from movement-related activity. Across the population of visual neurons, sensitivity began declining ∼80 ms before saccade onset. We also observed a similar presaccadic reduction in sensitivity to isoluminant, chromatic stimuli. Our results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation, and thus these neurons exhibit a signature of saccadic suppression.

Perceptual saccadic suppression starts in the retina

“…4e). It is very intriguing that such stimulus-stimulus retinal effects may be inherited all the way deep into the brain’s visual processing hierarchy, including cortical (frontal eye field) and subcortical (superior colliculus) areas 44 that are also implicated in saccadic suppression 15, 43, 45, 46 .…”

“…Indeed, the time courses of the neural adaptation effects in the frontal eye field and superior colliculus 44 , and related brain areas, are similar to our observed perceptual time courses in the absence of real saccades. Given that both the frontal eye field and superior colliculus have previously been implicated in suppression with real saccades 15, 43, 45, 46 , it is thus conceivable that saccadic suppression in these areas is inherited, at least partially, from the retina.…”

Perceptual saccadic suppression starts in the retina

“…Indeed, the time courses of the neural adaptation effects in the frontal eye field and superior colliculus 42 , and related brain areas, are similar to our observed perceptual time courses without real saccades. Given that both the frontal eye field and superior colliculus have previously been implicated in saccadic suppression 14,41,43,44 , it is thus conceivable that suppression in these areas is inherited, at least partially, from the retina.…”

“…4e). It is intriguing that such stimulus-stimulus retinal effects may be inherited deep into the brain's visual processing hierarchy, including cortical (frontal eye field) and subcortical (superior colliculus) areas 42 that are implicated in saccadic suppression 14,41,43,44 .…”

Functional Categories of Visuomotor Neurons in Macaque Frontal Eye Field

“…As noted above, the particular memory-guided saccade task used here is not identical to tasks used in previous studies. Factors like stimulus luminance, chromaticity, and contrast will need to be explored systematically (Krock and Moore, 2016). Moreover, FEF neurons are sensitive to reward contingency (Roesch and Olson, 2003) and other cognitive processes (Ferrera et al, 2009; Middlebrooks and Sommer, 2012; Teichert et al, 2014).…”