Abstract
Axonal connections are widely regarded as faithful transmitters of neuronal signals with fixed delays. The reasoning behind this is that extracellular 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.
Highlights
Signal processing and transmission in neuronal systems involves currents flowing across neuronal cell membranes
When synchronous spike volleys travel through such fibre bundles, the extracellular potential within the bundles is perturbed
Since most spikes within a spike volley are positioned in an area where the extracellular potential is negative, the resulting depolarisation of the axonal membranes accelerates the spike volley on average
Summary
Signal processing and transmission in neuronal systems involves currents flowing across neuronal cell membranes. Due to the resistance of the extracellular medium, such transmembrane currents generate extracellular potentials (EPs), called local field potentials (LFPs). Neurons can interact with their neighbours by changing the electric potential of the extracellular medium (and the membrane potential of their neighbours) without forming synapses. Such interaction is termed ephaptic interaction or ephaptic coupling [2,3,4]. Since EPs generated in the cortex are generally of the order of 100μV [5] and small in comparison to neuronal threshold potentials, the influence of EPs on neural computation is often regarded as negligible. EPs can be measured with intracranial electrodes and are used as a proxy for the underlying neuronal activity [6,7,8,9]
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