Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex.

1. Electrical stimulation of the infraorbital nerve was used to examine the coupling between neuronal activity and cerebral blood flow (CBF) in rat somatosensory cortex by laser Doppler flowmetry and extracellular recordings of field potentials. 2. The relationship between field potential (FP) and CBF amplitudes was examined as a function of the stimulus intensity (0--2.0 mA) at fixed frequency (3 Hz). FP amplitudes up to 2.0-2.5 mV were unaccompanied by increases of CBF. Above this threshold, CBF and FP amplitudes increased proportionally. 3. At fixed stimulus intensity of 1.5 mA, CBF increases were highly correlated to FP amplitudes at low frequencies of stimulation (< 2 Hz), but uncoupling was observed at stimulation frequencies of 2--5 Hz. The evoked responses were independent of stimulus duration (8--32 s). 4. The first rise in CBF occurred within the first 0.2 s after onset of stimulation in the upper 0--250 microm of the cortex. Latencies were longer (1.0--1.2 s) in lower cortical layers in which CBF and FP amplitudes were larger. 5. Local AMPA receptor blockade attenuated CBF and FP amplitudes proportionally. 6. This study showed that activity-dependent increases in neuronal activity and CBF were linearly coupled under defined conditions, but neuronal activity was well developed before CBF started to increase. Consequently, the absence of a rise in CBF does not exclude the presence of significant neuronal activity. The CBF increase in upper cortical layers preceded the rise in lower layers suggesting that vessels close to or at the brain surface are the first to react to neuronal activity. The activity-dependent rise in CBF was explained by postsynaptic activity in glutamatergic neurons.