Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology

Apical dendrites and somata of layer V pyramidal neurons were recorded with tight-seal patch electrodes in a slice preparation of rat somatosensory cortex. Recording sites were confirmed by measurements of the electrode location and by staining with biocytin. Dendritic recordings were made along the main trunk of the apical dendrite, usually within layer IV, at distances from 100 to 500 microns from the soma. Most cells recorded through the dendrite had a distinct enlargement of the apical trunk around the presumed recording site. The electrical properties of apical dendrites were readily distinguishable from those of somata. Dendrites generated two types of response when injected with depolarizing current. Group I responses were relatively small and broad Na(+)-dependent action potentials whose amplitude and rate-of-rise were negatively correlated with recording distance from the soma. Group II responses were complex, clustered firing patterns of Na(+)-dependent spikes together with higher-threshold slow spikes or plateaus; in these dendrites spike parameters were not correlated with distance from the soma. These two response groups were correlated with dendritic morphology: group I had significantly fewer oblique branches on the apical dendrite (5.5 vs 12.0) and a thinner apical trunk (2.0 vs 2.5 microns) than group II. TTX (1-2 microM) selectively blocked fast dendritic spikes, but not slow spikes and plateaus. Blocking Ca2+ currents reduced complex firing patterns and suppressed high-threshold slow spikes. Physiological and pharmacological studies imply that slow spikes and plateau potentials were primarily generated by high-threshold Ca2+ channels in the apical dendrite. Stimulating axons of layer I elicited EPSPs on distal apical dendrites of layer V cells. Recordings from both groups of apical dendrites revealed that EPSPs triggered a variety of distally generated, all-or-nothing depolarizations. The results show that voltage-dependent Na+ and Ca2+ currents are present in distal apical dendrites, in variable densities. These currents significantly modify distal synaptic events. The prevalence and character of active dendritic spiking (and presumably of Na+ and Ca2+ channel densities) correlate with the morphology of the apical dendritic tree.