Despite the wealth of recent research on active signal propagation along the dendrites of layer V neocortical pyramidal neurons, there is still little known regarding the traffic of subthreshold synaptic signals. We present a study using three simultaneous whole cell recordings on the apical dendrites of these cells in acute rat brain slices to examine the spread and attenuation of spontaneous excitatory postsynaptic potentials (sEPSPs). Equal current injections at each of a pair of sites separated by approximately 500 microm on the apical dendrite resulted in equal voltage transients at the other site ("reciprocity"), thus disclosing linear behavior of the neuron. The mean apparent "length constants" of the apical dendrite were 273 and 446 microm for somatopetal and somatofugal sEPSPs, respectively. Trains of artificial EPSPs did not show temporal summation. Blockade of the hyperpolarization-activated cation current (I(h)) resulted in less attenuation by 17% for somatopetal and by 47% for somatofugal sEPSPs. A pronounced location-dependent temporal summation of EPSP trains was seen. The subcellular distribution and biophysical properties of I(h) were studied in cell-attached patches. Within less than approximately 400 microm of the soma, a low density of approximately 3 pA/microm(2) was found, which increased to approximately 40 pA/microm(2) in the apical distal dendrite. I(h) showed activation and deactivation kinetics with time constants faster than 40 ms and half-maximal activation at -95 mV. These findings suggest that integration of synaptic input to the apical tuft and the basal dendrites occurs spatially independently. This is due to a high I(h) channel density in the apical tuft that increases the electrotonic distance between these two compartments in comparison to a passive dendrite.