Computations in cortical circuits are mediated by synaptic interactions between excitatory
and inhibitory neurons, and yet we know little about their activity in awake animals.
Here, through single and dual whole-cell recordings combined with two-photon microscopy
in the barrel cortex of behaving mice, we directly compare the synaptically driven
membrane potential dynamics of inhibitory and excitatory layer 2/3 neurons. We find
that inhibitory neurons depolarize synchronously with excitatory neurons, but they
are much more active with differential contributions of two classes of inhibitory
neurons during different brain states. Fast-spiking GABAergic neurons dominate during
quiet wakefulness, but during active wakefulness Non-fast-spiking GABAergic neurons
depolarize, firing action potentials at increased rates. Sparse uncorrelated action
potential firing in excitatory neurons is driven by fast, large, and cell-specific
depolarization. In contrast, inhibitory neurons fire correlated action potentials
at much higher frequencies driven by slower, smaller, and broadly synchronized depolarization.
