  Central neurons initiate action potentials (APs) in the axon initial segment
(AIS), a compartment characterized by a high concentration of voltage-dependent
ion channels and specialized cytoskeletal anchoring proteins arranged in a
regular nanoscale pattern. Although the AIS was a key evolutionary innovation
in neurons, the functional benefits it confers are not clear. Using a mutation
of the AIS cytoskeletal protein \beta IV-spectrin, we here establish an in
vitro model of neurons with a perturbed AIS architecture that retains nanoscale
order but loses the ability to maintain a high NaV density. Combining
experiments and simulations we show that a high NaV density in the AIS is not
required for axonal AP initiation; it is however crucial for a high bandwidth
of information encoding and AP timing precision. Our results provide the first
experimental demonstration of axonal AP initiation without high axonal channel
density and suggest that increasing the bandwidth of the neuronal code and
hence the computational efficiency of network function was a major benefit of
the evolution of the AIS.
