Theta waves, neural spikes and seizures can propagate by ephaptic coupling in vivo

Abstract

Electric field coupling has been shown to be responsible for non-synaptic neural activity propagation in hippocampal slices and cortical slices. Epileptiform and slow-wave sleep activity can propagate by electric field coupling without using synaptic connections at speeds of ~0.1 m/s in vitro. However, the characteristics of the events that can propagate using electric field coupling through a volume conductor in vivo have not been studied. Thus, we tested the hypothesis that various types of neural signals such as interictal spikes, theta waves and seizures could propagate in vivo across a transection in the hippocampus. We induced epileptiform activity in 4 rats under anesthesia by injecting 4-aminopyridine in the temporal region of the hippocampus, four recording electrodes were inserted along the longitudinal axis of the hippocampus. A transection was made between the electrodes to study the propagation of the neural activity. Although 54% of the interictal spikes could propagate through the cut, only those spikes with a high amplitude and short duration had a high probability to do so. 70% of seizure events could propagate through the cut but parameters distinguishing between propagating and non-propagating seizure events could not be identified. Theta activity was also observed to propagate at a mean speed of 0.16 ± 0.12 m/s in the characteristic range of propagation using electric field coupling through the transection. The electric field volume conduction mechanism was confirmed by showing that propagation was blocked by placing a dielectric layer within the cut. The speed of propagation was not affected by the transection thereby providing further evidence that various types of neural signals including activity in the theta range can propagate by electric field coupling in-vivo.