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The ongoing activity of neurons generates a spatially- and time-varying fieldof extracellular voltage ($V_e$). This $V_e$ field reflects population-levelneural activity, but does it modulate neural dynamics and the function ofneural circuits? We provide a cable theory framework to study how a bundle ofmodel neurons generates $V_e$ and how this $V_e$ feeds back and influencesmembrane potential ($V_m$). We find that these "ephaptic interactions" aresmall but not negligible. The model neural population can generate $V_e$ withmillivolt-scale amplitude and this $V_e$ perturbs the $V_m$ of "nearby" cablesand effectively increases their electrotonic length. After using passive cabletheory to systematically study ephaptic coupling, we explore a test case: themedial superior olive (MSO) in the auditory brainstem. The MSO is a possiblelocus of ephaptic interactions: sounds evoke large $V_e$ in vivo in thisnucleus (millivolt-scale). The $V_e$ response is thought to be generated by MSOneurons that perform a known neuronal computation with submillisecond temporalprecision (coincidence detection to encode sound source location). Using abiophysically-based model of MSO neurons, we find millivolt-scale ephapticinteractions consistent with the passive cable theory results. These subtlemembrane potential perturbations induce changes in spike initiation threshold,spike time synchrony, and time difference sensitivity. These results suggestthat ephaptic coupling may influence MSO function.

Neuronal coupling by endogenous electric fields: Cable theory and applications to coincidence detector neurons in the auditory brainstem