The cortical eye proprioceptive signal modulates neural activity in higher-order visual cortex as predicted by the variation in visual sensitivity

Whereas the links between eye movements and the shifts in visual attention are well established, less is known about how eye position affects the prioritization of visual space. It was recently observed that visual sensitivity varies with the direction of gaze and the level of excitability in the eye proprioceptive representation in human left somatosensory cortex (S1(EYE)), so that after 1Hz repetitive transcranial magnetic stimulation (rTMS) over S1(EYE), targets presented nearer the center of the orbit are detected more accurately. Here we used whole-brain functional magnetic resonance imaging to map areas where S1(EYE)-rTMS affects the neural response evoked by retinally identical stimuli depending on the direction of rotation of the right eye. After S1(EYE)-rTMS, a single area in the left cuneus outside Brodmann Areas 17/18 showed an increased neuronal response to a right hemifield target when the right eye was rotated leftwards as compared with when it was rotated rightwards. This effect was larger after S1(EYE)-rTMS than after rTMS of a control area in the motor cortex. The neural response to retinally identical stimuli in this area could be predicted from the changes in visual detectability observed previously, but not from the location of the visual targets relative to the body. These results strongly argue for a modulatory connection from the eye proprioceptive area in the somatosensory cortex to the higher-order visual cortex. This connection may contribute to flexibly allocate priorities for visual perception depending on the proprioceptively signaled direction of gaze.