Stimulus history reliably shapes action potential waveforms of cortical neurons

Action potentials have been shown to shunt synaptic charge to a degree that depends on their waveform. In this way, they participate in synaptic integration, and thus in the probability of generating succeeding action potentials, in a shape-dependent way. Here we test whether the different action potential waveforms produced during dynamical stimulation in a single cortical neuron carry information about the conductance stimulus history. When pyramidal neurons in rat visual cortex were driven by a conductance stimulus that resembles natural synaptic input, somatic action potential waveforms showed a large variability that reliably signaled the history of the input for up to 50 ms before the spike. The correlation between stimulus history and action potential waveforms had low noise, resulting in information rates that were three to four times larger than for the instantaneous spike rate. The reliable correlation between stimulus history and spike waveforms then acts as a local encoding at the single-cell level. It also directly affects neuronal communication as different waveforms influence the production of succeeding spikes via differential shunting of synaptic charge. Modeling was used to show that slow conductances can implement memory of the stimulus history in cortical neurons, encoding this information in the spike shape.