The Stochastic Nature of Action Potential Backpropagation in Apical Tuft Dendrites

In cortical pyramidal neurons, backpropagating action potentials (bAPs) supply Ca²⁺ to synaptic contacts on dendrites. To determine whether the efficacy of AP backpropagation into apical tuft dendrites is stable over time, we performed dendritic Ca²⁺ and voltage imaging in rat brain slices. We found that the amplitude of bAP-Ca²⁺ in apical tuft branches was unstable, as it varied from trial to trial (termed "bAP-Ca²⁺ flickering"). Small perturbations in dendritic physiology, such as spontaneous synaptic inputs, channel inactivation, or temperature-induced changes in channel kinetics, can cause bAP flickering. In the tuft branches, the density of Na⁺ and K⁺ channels was sufficient to support local initiation of fast spikelets by glutamate iontophoresis. We quantified the time delay between the somatic AP burst and the peak of dendritic Ca²⁺ transient in the apical tuft, because this delay is important for induction of spike-timing dependent plasticity (STDP). Depending on the frequency of the somatic AP triplets, Ca²⁺ signals peaked in the apical tuft 20 - 50 ms after the first AP in the soma. Interestingly, at low frequency (<20 Hz), the Ca²⁺ peaked sooner than at high frequency, because only the 1st AP invaded tuft. Activation of dendritic VGCCs is sensitive to the duration of the dendritic voltage transient. In apical-tuft branches, small changes in the duration of bAP voltage waveforms cause disproportionately large increases in dendritic Ca²⁺ influx (bAP-Ca²⁺ flickering). The stochastic nature of bAP-Ca²⁺ adds a new perspective on the mechanisms by which pyramidal neurons combine inputs arriving at different cortical layers.

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