Abstract

The dynamics and the sharp onset of action potential (AP) generation have recently been the subject of intense experimental and theoretical investigations. According to the resistive coupling theory, an electrotonic interplay between the site of AP initiation in the axon and the somato-dendritic load determines the AP waveform. This phenomenon not only alters the shape of APs recorded at the soma, but also determines the dynamics of excitability across a variety of time scales. Supporting this statement, here we generalize a previous numerical study and extend it to the quantification of the input-output gain of the neuronal dynamical response. We consider three classes of multicompartmental mathematical models, ranging from ball-and-stick simplified descriptions of neuronal excitability to 3D-reconstructed biophysical models of excitatory neurons of rodent and human cortical tissue. For each model, we demonstrate that increasing the distance between the axonal site of AP initiation and the soma markedly increases the bandwidth of neuronal response properties. We finally consider the Liquid State Machine paradigm, exploring the impact of altering the site of AP initiation at the level of a neuronal population, and demonstrate that an optimal distance exists to boost the computational performance of the network in a simple classification task.

Highlights

  • The dynamics of action potential (AP) initiation and its underlying time-scales have been themes of intense investigation in rodent and human cortical neurons, both experimentally [1,2,3,4,5,6,7,8] and theoretically [6,9,10,11,12]

  • We investigated the influence of the AP onset dynamics and response bandwidth on the computational power of a neuronal network

  • We studied the dynamics of the excitability in multicompartmental neuron models with increasing complexity

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Summary

Introduction

The dynamics of AP initiation and its underlying time-scales have been themes of intense investigation in rodent and human cortical neurons, both experimentally [1,2,3,4,5,6,7,8] and theoretically [6,9,10,11,12]. Early numerical and theoretical studies on single-compartmental models of spike-initiation [9,14] suggested a strong causal relationship between the rapidity of the AP at its onset and the dynamics of the instantaneous firing rate. The latter determine the encoding and tracking properties of neurons and networks of rapid components in their input [8]. They demonstrated in silico that increasing the AIS distance from the soma makes the AP somatic waveform sharper than for proximal AIS locations [12]

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