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

Shortly before each saccadic eye movement, presaccadic attention improves visual sensitivity at the saccade target ^1-5 at the expense of lowered sensitivity at non-target locations ^6-11 . Some behavioral and neural correlates of presaccadic attention and covert attention -which likewise enhances sensitivity, but during fixation ¹² -are similar ¹³ . This resemblance has led to the debatable ^13-18 notion that presaccadic and covert attention are functionally equivalent and rely on the same neural circuitry ^19-21 . At a broad scale, oculomotor brain structures (e.g., FEF) are also modulated during covert attention ^22-24 - yet by distinct neuronal subpopulations ^25-28 . Perceptual benefits of presaccadic attention rely on feedback from oculomotor structures to visual cortices ^29,30 ( Fig. 1a ); micro-stimulation of FEF in non-human primates affects activity in visual cortex ^31-34 and enhances visual sensitivity at the movement field of the stimulated neurons ^35-37 . Similar feedback projections seem to exist in humans: FEF+ activation precedes occipital activation during saccade preparation ^38,39 and FEF TMS modulates activity in visual cortex ^40-42 and enhances perceived contrast in the contralateral hemifield ⁴⁰ . 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.