Total neuroenergetics support localized brain activity: Implications for the interpretation of fMRI

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Abstract
In α-chloralose-anesthetized rats, changes in the blood oxygenation level-dependent (BOLD) functional MRI (fMRI) signal (ΔS/S), and the relative spiking frequency of a neuronal ensemble (Δν/ν) were measured in the somatosensory cortex during forepaw stimulation from two different baselines. Changes in cerebral oxygen consumption (ΔCMRO2/CMRO2) were derived from the BOLD signal (at 7T) by independent determinations in cerebral blood flow (ΔCBF/CBF) and volume (ΔCBV/CBV). The spiking frequency was measured by extracellular recordings in layer 4. Changes in all three parameters (CMRO2, ν, and S) were greater from the lower baseline (i.e., deeper anesthesia). For both baselines, ΔCMRO2/CMRO2 and Δν/ν were approximately one order of magnitude larger than ΔS/S. The final values of CMRO2 and ν reached during stimulation were approximately the same from both baselines. If only increments were required to support functions then their magnitudes should be independent of the baseline. In contrast, if particular magnitudes of activity were required, then sizes of increments should inversely correlate with the baseline (being larger from a lower baseline). The results show that particular magnitudes of activity support neural function. The disregard of baseline activity in fMRI experiments by differencing removes a large and necessary component of the total activity. Implications of these results for understanding brain function and fMRI experiments are discussed.