Ultrafast population coding and axo-somatic compartmentalization

Abstract

Cortical neurons in the fluctuation driven regime can realize ultrafast population encoding. The underlying biophysical mechanisms, however, are not well understood. Reducing the sharpness of the action potential onset can impair ultrafast population encoding, but it is not clear whether a sharp action potential onset is sufficient for ultrafast population encoding. One hypothesis proposes that the sharp action potential onset is caused by the electrotonic separation of the site of action potential initiation from the soma, and that this spatial separation also results in ultrafast population encoding. Here we examined this hypothesis by studying the linear response properties of model neurons with a defined initiation site. We find that placing the initiation site at different axonal positions has only a weak impact on the linear response function of the model. It fails to generate the ultrafast response and high bandwidth that is observed in cortical neurons. Furthermore, the high frequency regime of the linear response function of this model is insensitive to correlation times of the input current contradicting empirical evidence. When we increase the voltage sensitivity of sodium channels at the initiation site, the two empirically observed phenomena can be recovered. We provide an explanation for the dissociation of sharp action potential onset and ultrafast response. By investigating varying soma sizes, we furthermore highlight the effect of neuron morphology on the linear response. Our results show that a sharp onset of action potentials is not sufficient for the ultrafast response. In the light of recent reports of activity-dependent repositioning of the axon initial segment, our study predicts that a more distal initiation site can lead to an increased sharpness of the somatic waveform but it does not affect the linear response of a population of neurons.