The Neural Basis of Functional MRI Responses

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To study the link between fMRI and electrophysiology, one must be able to conduct both invasive recordings and fMRI scanning on the same animal subjects. The Intramural Research Program at the National Institute of Mental Health is one of the only sites in the world at which such measurements can be conducted. In the last years, we have refined our methods to allow for both sequential and simultaneous measurement of electrophysiological and fMRI signals from the same tissue in awake, behaving nonhuman primates. Much of this work has been done in direct collaboration with the Neurophysiology Imaging Facility, a shared core facility dedicated to structural and functional brain imaging and nonhuman primates. In a previous study, we showed that during perceptual suppression, where a visual stimulus is physically present but temporarily escapes perception, fMRI signals and electrophysiological signals in the primary visual cortex become uncharacteristically divergent. Specifically, the fMRI signal reflected the monkeys perceptual state, whereas the spiking of individual neurons in the same region of the brain reflected the presence of the physical stimulus, but did not change their activity according to the reported perception. This divergence was not observed during the conventional presentation of visual stimuli. More recent work from our lab has suggested that synaptic activity in the upper layers of the visual cortex, which receive feedback input from higher visual centers, show activity changes that reflect the monkeys percept. We are presently conducting experiments to understand how the such upper-layer activity might lead to fMRI changes in the primary visual cortex, but at the same time not affect the rate of action potential firing among neurons in the same region. Last year, we published a study investigating the basis of spontaneous fMRI activity, which is taken as the basis for so-called functional connectivity throughout the neuroimaging community. When the brain is not confronted with any sensory stimuli, its activity level remains high, with the origin of the observed slow, endogenous fluctuations poorly understood. Previous work has demonstrated that the spatiotemporal correlations of these fluctuations exhibit a similarity known functional networks, and this approach is presently employed by hundreds of labs to study the human brain. To study whether the spontaneous fMRI fluctuations have a clear electrophysiological basis, we performed simultaneous electrophysiological and fMRI measurements in awake monkeys. We found that the electrical activity correlated with activity changes over large swathes of the cerebral cortex, indicating that such widespread activity, which is typically discarded as hemodynamic noise, does indeed have a neurological basis. In fact, this global aspect of brain activity may be particularly important because it accounts for a high fraction of metabolic consumption. These findings have already begun to influence the human neuroimaging communitys consideration of global fMRI noise measured during rest. Finally, as an offshoot of the blindsight study mentioned in the project The Neurophysiology of Visual Perception, we have been examining the extent to which residual fMRI responses to visual stimuli presented to a blind visual field are reflected in the firing of neurons in the same cortical area. Initial findings from cortical area V4 suggest that spiking responses in this area are very weak despite the moderate fMRI responses. By contrast, the local field potential responses are strong, suggesting that, as in V1, synaptic inputs may give rise to fMRI responses in the absence of neural spiking. Together, these three projects are beginning to elucidate the link between neural and fMRI signals during both sensory stimulation and spontaneous activity during rest.