Energetics of resting and evoked fMRI signals were related to localized ensemble firing rates () measured by electrophysiology in rats. Two different unstimulated, or baseline, states were established by anesthesia. Halothane and ␣-chloralose established baseline states of high and low energy, respectively, in which forepaw stimulation excited the contralateral primary somatosensory cortex (S1). With ␣-chloralose, forepaw stimulation induced strong and reproducible fMRI activations in the contralateral S1, where the ensemble firing was dominated by slow signaling neurons (SSN; range of 1-13 Hz). Under halothane, weaker and less reproducible fMRI activations were observed in the contralateral S1 and elsewhere in the cortex, but ensemble activity in S1 was dominated by rapid signaling neurons (RSN; range of 13-40 Hz). For both baseline states, the RSN activity (i.e., higher frequencies, including the ␥ band) did not vary upon stimulation, whereas the SSN activity (i.e., ␣ band and lower frequencies) did change. In the high energy baseline state, a large majority of total oxidative energy [cerebral metabolic rate of oxygen consumption (CMR O2)] was devoted to RSN activity, whereas in the low energy baseline state, it was roughly divided between SSN and RSN activities. We hypothesize that in the high energy baseline state, the evoked changes in fMRI activation in areas beyond S1 are supported by rich intracortical interactions represented by RSN. We discuss implications for interpreting fMRI data where stimulus-specific ⌬CMR O2 is generally small compared with baseline CMR O2.awake ͉ behavior ͉ calibrated fMRI ͉ glucose ͉ glutamate N oninvasive NMR and electrophysiological methods offer considerably different spatiotemporal results that presumably reflect the same cerebral activity. Localized energy consumption of neuronal and glial populations in MRI voxels has been evaluated (1), initially from 13 C MRS (2) and more recently from calibration of functional MRI (fMRI) (3). In vivo electrophysiological measurements of neuronal activity, from single neurons or large ensembles (4), are considered the gold standard of cerebral activity (5). Can measurements from these dissimilar techniques provide complementary insights into the working brain?A promising convergence between these apparently different results relies on a universal thermodynamic principle, the fundamental relationship between the work done and the energy expended. Cerebral energy comes almost exclusively from glucose oxidation (6). Recent results have shown that the cerebral metabolic rate of oxygen consumption (CMR O2 ) is almost completely dedicated to supporting work associated with synaptic activity (7,8). Changes in CMR O2 from calibrated fMRI (9) are linear with changes in firing rates of a representative neuronal ensemble in the same voxel (10). This basic work/ energy relationship has been extended by in vivo investigations (11, 12) that relate imaging energetics to the underlying neuronal activities.Neuroimaging methods localize changes of task-i...

Functional magnetic resonance imaging (fMRI) with blood-oxygenation level dependent (BOLD) contrast is an important tool for mapping brain activity. Interest in quantitative fMRI has renewed awareness in importance of oxidative neuroenergetics, as reflected by cerebral metabolic rate of oxygen consumption(CMRO2), for supporting brain function. Relationships between BOLD signal and the underlying neurophysiological parameters have been elucidated to allow determination of dynamic changes inCMRO2 by “calibrated fMRI,” which require multi-modal measurements of BOLD signal along with cerebral blood flow (CBF) and volume (CBV). But how doCMRO2 changes, steady-state or transient, derived from calibrated fMRI compare with neural activity recordings of local field potential (LFP) and/or multi-unit activity (MUA)? Here we discuss recent findings primarily from animal studies which allow high magnetic fields studies for superior BOLD sensitivity as well as multi-modal CBV and CBF measurements in conjunction with LFP and MUA recordings from activated sites. A key observation is that while relationships between neural activity and sensory stimulus features range from linear to non-linear, associations between hyperemic components (BOLD, CBF, CBV) and neural activity (LFP, MUA) are almost always linear. More importantly, the results demonstrate good agreement between the changes inCMRO2 and independent measures of LFP or MUA. The tight neurovascular and neurometabolic couplings, observed from steady-state conditions to events separated by <200 ms, suggest rapid oxygen equilibration between blood and tissue pools and thus calibrated fMRI at high magnetic fields can provide high spatiotemporal mapping ofCMRO2 changes.

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