Neurons are continually exposed to background synaptic activity in vivo. This is thought to influence neural information processing, but background levels of excitation and inhibition remain controversial. Here we show, using whole-cell recordings in anesthetized rats, that spontaneous depolarizations ("Up states") in neocortical pyramidal neurons are driven by sparse, mostly excitatory synaptic activity (less than five inputs per millisecond; approximately 10% inhibitory). The mean synaptic conductance change is small (<10 nS at the soma) and opposed by anomalous rectification, resulting in a net increase in input resistance during Up states. These conditions enhance the effectiveness of each synapse at depolarized potentials. Hence, neocortical networks are relatively quiet at rest, and the effect of synaptic background is weaker than previously thought.