Backpropagation of physiological spike trains in neocortical pyramidal neurons: Implications for temporal coding in dendrites

In vivo neocortical neurons fire apparently random trains of action potenti als in response to sensory stimuli. Does this randomness represent a signal or noise around a mean firing rate? Here we use the timing of action poten tial trains recorded in vivo to explore the dendritic consequences of physi ological patterns of action potential firing in neocortical pyramidal neuro ns in vitro. We find that action potentials evoked by physiological pattern s of firing backpropagate threefold to fourfold more effectively into the d istal apical dendrites (>600 mum from the soma) than action potential train s reflecting their mean firing rate. This amplification of backpropagation was maximal during high-frequency components of physiological spike trains (80-300 Hz). The disparity between backpropagation during physiological and mean firing patterns was dramatically reduced by dendritic hyperpolarizati on. Consistent with this voltage dependence, dendritic depolarization ampli fied single action potentials by fourfold to seven-fold, with a spatial pro file strikingly similar to the amplification of physiological spike trains. Local blockade of distal dendritic sodium channels substantially reduced a mplification of physiological spike trains, but did not significantly alter action potential trains reflecting their mean firing rate. Dendritic elect rogenesis during physiological spike trains was also reduced by the blockad e of calcium channels. We conclude that amplification of backpropagating ac tion potentials during physiological spike trains is mediated by frequency- dependent supralinear temporal summation, generated by the recruitment of d istal dendritic sodium and calcium channels. Together these data indicate t hat the temporal nature of physiological patterns of action potential firin g contains a signal that is transmitted effectively throughout the dendriti c tree.