Dissociable roles of human frontal eye fields and early visual cortex in presaccadic attention – evidence from TMS

Abstract

AbstractShortly before each saccadic eye movement, presaccadic attention improves visual sensitivity at the saccade target1–5at the expense of lowered sensitivity at non-target locations6–11. Some behavioral and neural correlates of presaccadic attention and covert attention –which likewise enhances sensitivity, but during fixation12–are similar13. This resemblance has led to the debatable13–18notion that presaccadic and covert attention are functionally equivalent and rely on the same neural circuitry19–21. At a broad scale, oculomotor brain structures (e.g., FEF) are also modulated during covert attention22–24– yet by distinct neuronal subpopulations25–28. Perceptual benefits of presaccadic attention rely on feedback from oculomotor structures to visual cortices29,30(Fig. 1a); micro-stimulation of FEF in non-human primates affects activity in visual cortex31–34and enhances visual sensitivity at the movement field of the stimulated neurons35–37. Similar feedback projections seem to exist in humans: FEF+ activation precedes occipital activation during saccade preparation38,39and FEF TMS modulates activity in visual cortex40–42and enhances perceived contrast in the contralateral hemifield40. We investigated presaccadic feedback in humans by applying TMS to frontal or visual areas during saccade preparation. By simultaneously measuring perceptual performance, we show the causal and differential roles of these brain regions in contralateral presaccadic benefits at the saccade target and costs at non-targets: Whereas rFEF+ stimulation reduced presaccadic costs throughout saccade preparation, V1/V2 stimulation reduced benefits only shortly before saccade onset. These effects provide causal evidence that presaccadic attention modulates perception through cortico-cortical feedback and further dissociate presaccadic and covert attention.