Axonal connections are widely regarded as faithful transmitters of neuronal signals with fixed delays. The reasoning behind this is that extra-cellular potentials caused by spikes travelling along axons are too small to have an effect on other axons. Here we devise a computational framework that allows us to study the effect of extracellular potentials generated by spike volleys in axonal fibre bundles on axonal transmission delays. We demonstrate that, although the extracellular potentials generated by single spikes are of the order of microvolts, the collective extracellular potential generated by spike volleys can reach several millivolts. As a consequence, the resulting depolarisation of the axonal membranes increases the velocity of spikes, and therefore reduces axonal delays between brain areas. Driving a neural mass model with such spike volleys, we further demonstrate that only ephaptic coupling can explain the reduction of stimulus latencies with increased stimulus intensities, as observed in many psychological experiments.
Author summaryAxonal fibre bundles that connect distant cortical areas contain millions of densely packed axons. When synchronous spike volleys travel through such fibre bundles, the extracellular potential within the bundles is perturbed. We use computer simulations to examine the magnitude and shape of this perturbation, and demonstrate that it is sufficiently strong to affect axonal transmission speeds. Since most spikes within a spike volley are positioned in an area where the extracellular potential is negative (relative to a distant reference), the resulting depolarisation of the axonal membranes accelerates the spike volley on average. This finding is in contrast to previous studies of ephaptic coupling effects between axons, where ephaptic coupling was found to slow down spike propagation. Our finding has consequences for information transmission and synchronisation between cortical areas. April 2, 2020 1/20 1 Signal processing and transmission in neuronal systems involves currents flowing across 2 neuronal cell membranes. Due to the resistance of the extracellular medium, such 3 transmembrane currents generate extracellular potentials (EPs), also called local field 4 potentials (LFPs). The sources of EPs are synaptic currents, action potentials, calcium 5 spikes and voltage-dependent intrinsic currents [1]. Neurons can therefore interact with 6 their neighbours by changing the electric potential of the extracellular medium (and 7 hence the membrane potential of their neighbours) without forming synapses. Such 8 interaction is termed ephaptic interaction or ephaptic coupling [2-4]. Since EPs 9 generated in the cortex are generally of the order of 100µV [5] and therefore small in 10 comparison to neuronal threshold potentials, the influence of EPs on neural 11 computation is often regarded as negligible. EPs can be measured with intracranial 12 electrodes and are used as a proxy for the underlying neuronal activity [6-9]. 13 Seminal experiments by Katz and Schmitt [10], Rosenbl...