Asynchronous Broadband Signals Are the Principal Source of the BOLD Response in Human Visual Cortex

Background: Activity in the living human brain can be studied using multiple methods, spanning a wide range of spatial and temporal resolutions. We investigated the relationship between electric field potentials measured with electrocorticography (ECoG) and the blood oxygen level-dependent (BOLD) response measured with functional magnetic resonance imaging (fMRI). We set out to explain the full set of measurements by modeling the underlying neural circuits. Results: ECoG responses in visual cortex can be separated into two visually driven components. One component is a specific temporal response that follows each stimulus contrast reversal (stimulus locked); the other component is an increase in the response variance (asynchronous). For electrodes in visual cortex (V1, V2, V3), the two measures respond to stimuli in the same region of visual space, but they have different spatial summation properties. The stimulus-locked ECoG component sums contrast approximately linearly across space; spatial summation in the asynchronous ECoG component is subadditive. Spatial summation measured using BOLD closely matches the asynchronous component. We created a neural simulation that accurately captures the main features of the ECoG time series; in the simulation, the stimulus-locked and asynchronous components arise from different neural circuits. Conclusions: These observations suggest that the two ECoG components arise from different neural sources within the same cortical region. The spatial summation measurements and simulations suggest that the BOLD response arises primarily from neural sources that generate the asynchronous broadband ECoG component.