Occipital activations and deactivations induced by stimulation of the right human frontal eye field

Abstract

The frontal eye fields (FEF) are traditionally thought to be involved in the preparation and execution of eye movements, but more recent evidence suggests a role in covert spatial attention also. Projections from this putative control area in frontal cortex may modulate activity in visual cortex, but direct evidence for this is lacking in humans, despite recent breakthroughs in monkey studies. Here we used a combination of fMRI and Transcranial Magnetic Stimulation (TMS) in the scanner to show that stimulation of human FEF can modulate activity in retinotopically mapped visual cortex. Right FEF stimulation activated bilaterally sectors of retinotopic visual cortex (V1–V3, and beyond) that represent the peripheral visual field; but it deactivated sectors representing the central visual field. This FEF-induced retinotopic pattern did not depend on resting activation in visual cortex, as it was equivalently present with or without concurrent visual stimulation. Nor was it due to TMS-induced eye movements, blinks, or pupil changes. These data (1) provide direct support for FEF modulation of visual cortex, (2) are consistent with recent anatomical and physiological studies in other primates, which suggest distinct FEF-occipital connections for central and peripheral visual field representations, and (3) illustrate how concurrent TMS and fMRI can now be used to study functional influences between remote but interconnected brain areas.