Decorrelated Input Dissociates Narrow Band γ Power and BOLD in Human Visual Cortex

Abstract

Although fMRI using the BOLD contrast is widely used for noninvasively mapping hemodynamic brain activity in humans, its exact link to underlying neural processing is poorly understood. Whereas some studies have reported that BOLD signals measured in visual cortex are tightly linked to neural activity in the narrow band γ (NBG) range, others have found a weak correlation between the two. To elucidate the mechanisms behind these conflicting findings, we hypothesized that BOLD reflects the strength of synaptic inputs to cortex, whereas NBG is more dependent on how well these inputs are correlated. To test this, we measured NBG, BOLD, and cerebral blood flow responses to stimuli that either correlate or decorrelate neural activity in human visual cortex. Next, we simulated a recurrent network model of excitatory and inhibitory neurons that reproduced in detail the experimental NBG and BOLD data. Results show that the visually evoked BOLD response was solely predicted by the sum of local inputs, whereas NBG was critically dependent on how well these inputs were correlated. In summary, the NBG-BOLD relationship strongly depends on the nature of sensory input to cortex: stimuli that increase the number of correlated inputs to visual cortex will increase NBG and BOLD in a similar manner, whereas stimuli that increase the number of decorrelated inputs will dissociate the two. The NBG-BOLD relationship is therefore not fixed but is rather highly dependent on input correlations that are both stimulus- and state-dependent.

SIGNIFICANCE STATEMENT It is widely believed that γ oscillations in cortex are tightly linked to local hemodynamic activity. Here, we present experimental evidence showing how a stimulus can increase local blood flow to the brain despite suppressing γ power. Moreover, using a sophisticated model of cortical neurons, it is proposed that this occurs when synaptic input to cortex is strong yet decorrelated. Because input correlations are largely determined by the state of the brain, our results demonstrate that the relationship between γ and local hemodynamics is not fixed, but rather context dependent. This likely explains why certain neurodevelopmental disorders are characterized by weak γ activity despite showing normal blood flow.