Trial-by-trial relationship between neural activity, oxygen consumption, and blood flow responses

Trial-by-trial variability in local field potential (LFP), tissue partial pressure of oxygen (PO2), cerebral blood flow (CBF), and deoxyhemoglobin-weighted optical imaging of intrinsic signals (OIS) were tested in the rat somatosensory cortex while fixed electrical forepaw stimulation (1.0-ms pulses with amplitude of 1.2 mA at a frequency of 6 Hz) was repeatedly applied. The changes in the cerebral metabolic rate of oxygen (CMRO2) were also evaluated using a hypotension condition established by our group based on the administration of a vasodilator. Under normal conditions, CBF, PO2, and OIS showed positive signal changes (48%, 32%, and 0.42%, respectively) following stimulation. Over multiple trials, the CBF responses were well correlated with the integral of the LFP amplitudes (sigmaLFP) (Rmean=0.78), whereas a lower correlation was found between PO2 and sigmaLFP (Rmean=0.60) and between OIS and sigmaLFP (Rmean=0.54). Under the hypotension condition the LFP responses were preserved, but the CBF responses were suppressed and the PO2 and OIS changes were negative (-12% and -0.28%, respectively). In this condition, the trial-by-trial variations in PO2 and OIS were well correlated with the variability in sigmaLFPs (Rmean= -0.77 and -0.76, respectively), indicating a single trial coupling between CMRO2 changes and sigmaLFP. These findings show that CBF and CMRO2 signals are more directly correlated with neural activity compared to blood oxygen-sensitive methods such as OIS and BOLD fMRI.