Backpropagation of Physiological Spike Trains in Neocortical Pyramidal Neurons: Implications for Temporal Coding in Dendrites

Abstract

In vivo neocortical neurons fire apparently random trains of action potentials 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 potential trains recorded in vivo to explore the dendritic consequences of physiological patterns of action potential firing in neocortical pyramidal neurons in vitro. We find that action potentials evoked by physiological patterns of firing backpropagate threefold to fourfold more effectively into the distal apical dendrites (>600 microm from the soma) than action potential trains 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 hyperpolarization. Consistent with this voltage dependence, dendritic depolarization amplified single action potentials by fourfold to sevenfold, with a spatial profile strikingly similar to the amplification of physiological spike trains. Local blockade of distal dendritic sodium channels substantially reduced amplification of physiological spike trains, but did not significantly alter action potential trains reflecting their mean firing rate. Dendritic electrogenesis during physiological spike trains was also reduced by the blockade of calcium channels. We conclude that amplification of backpropagating action potentials during physiological spike trains is mediated by frequency-dependent supralinear temporal summation, generated by the recruitment of distal dendritic sodium and calcium channels. Together these data indicate that the temporal nature of physiological patterns of action potential firing contains a signal that is transmitted effectively throughout the dendritic tree.