Volume current coupling—remote direct neural coupling across the extracellular space

Abstract

Although electrical devices should not be submerged, the brain, despite its electrical implementation, is submerged in an electrolyte solution and has indeed leakage currents as demonstrated by electroencephalograms (EEGs). Ephaptic coupling is a direct electrical neural coupling mediated by leakage currents between adjacent neurons on a microscale, and it affects spike timing. Since EEGs are detectable, meaning that tens of thousands of neurons activate synchronously, their collective leakage currents can extend the coupling over longer distances, hereafter called volume current coupling (VcC). Here, we show neural coupling (NC) = synaptic coupling (SC) + VcC and find a function of VcC. When two people, sensorily isolated but electrically connected at the heads in a skillful way to exchange their volume currents (Vcs) to avoid attenuation, were given separate left–right discrimination tasks, a significant conflict, or a task-irrelevant conditional bias, occurred in the discrimination. No SC existed between the two participants, indicating a behaviorally functional VcC. The Vc propagation path contains neurons of the person producing the Vc, and intra-person VcCs can also occur. In fact, as intra-person effects, an unconditional right-preferential bias emerged when electrically disconnected, but a task-irrelevant conditional right-preferential bias, or priming, emerged when connected. Since the skillful connection intervenes only in VcC, NC = SC + VcC is true also in individual brains and one function of VcC is to generate these biases. Since VcCs are ubiquitous in the brain as electrical crosstalk, it may be better not to study cognitive and behavioral functions in the SC alone.