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 neuroimaging 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. TMS 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 TMS on activity in retinotopic visual cortex led to a behavioral prediction that we confirmed psychophysically by showing that TMS 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.
Ruff
Christian C
CC
UCL Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London WC1N 3AR, United Kingdom. c.ruff@ucl.ac.uk
Blankenburg
Felix
F
Bjoertomt
Otto
O
Bestmann
Sven
S
Freeman
Elliot
E
Haynes
John-Dylan
JD
Rees
Geraint
G
Josephs
Oliver
O
Deichmann
Ralf
R
Driver
Jon
J
D000328:Adult; D001931:Brain Mapping / Q000379:methods*; D005625:Frontal Lobe / Q000502:physiology* / Q000648:ultrastructure; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D011601:Psychophysics; D050781:Transcranial Magnetic Stimulation; D014793:Visual Cortex / Q000502:physiology* / Q000648:ultrastructure; D014796:Visual Perception / Q000502:physiology*