Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex

Background: Regions in human frontal cortex may have modulatory top-down influences on retinotopic visual cortex, but to date neuroirraging methods have only been able to provide indirect evidence for such functional interactions between remote but interconnected brain regions. Here we combined transcranial magnetic stimulation (TMS) with concurrent functional magnetic resonance imaging (fMRI), plus psychophysics, to show that stimulation of the right human frontal eye-field (FEF) produced a characteristic topographic pattern of activity changes in retinotopic visual areas V1-V4, with functional consequences for visual perception. Results: FEF TMS led to activity increases for retinotopic representations of the peripheral visual field, but to activity decreases for the central field, in areas V1-V4. These frontal influences on visual cortex occurred in a top-down manner, independently of visual input. TIVIS of a control site (vertex) did not elicit such visual modulations, and saccades, blinks, or pupil dilation could not account for our results. Finally, the effects of FEF TIVIS on activity in retinotopic visual cortex led to a behavioral prediction that we confirmed psychophysically by showing that TIVIS of the frontal site (again compared with vertex) enhanced perceived contrast for peripheral relative to central visual stimuli. Conclusions: Our results provide causal evidence that circuits originating in the human FEF can modulate activity in retinotopic visual cortex, in a manner that differentiates the central and peripheral visual field, with functional consequences for perception. More generally, our study illustrates how the new approach of concurrent TMS-fMRI can now reveal causal interactions between remote but interconnected areas of the human brain.