Multimodal characterization of population responses evoked by applied electric field in vitro: extracellular potential, magnetic evoked field, transmembrane potential, and current-source density analysis.

An external electric field applied parallel to longitudinal axis of neurons selectively depolarizes either end and thereby activates voltage-sensitive conductance changes in a large population of neurons. Here, we characterized such population responses in the in vitro turtle cerebellum. The responses were recorded and analyzed using a multimodal approach: the magnetic evoked field was measured using a Superconducting Quantum Interference Device (SQUID) magnetometer, and concurrently the electric field potentials were recorded. Laminar profile and current-source density analysis were used to uncover the pattern of activation due to the applied electric field. Intracellular recording provided further information for identifying the elements producing the observed responses. Finally, pharmacological manipulations confirmed the nature of the conductance changes. Our results show that it is possible to activate a defined cell population of the cerebellum by an applied field and obtain a magnetic response of the order of 0.5-2 pT. A field applied from the dorsal to the ventral side of cerebellum produced tetrodotoxin-sensitive population spikes. This component was followed by a kynurenic acid (KYNA)-sensitive postsynaptic response, most likely comprised of Ca(2+)-mediated action potentials occurring at the proximal pole of the Purkinje cell dendrites and evoked by climbing fiber inputs. The applied electric field directed from the ventral to the dorsal side of cerebellum gave rise to a complex of responses that was made up of a KYNA-sensitive component (presumably synaptically activated) and an Mn(2+)-sensitive but KYNA-insensitive component (probably due to a directly activated calcium conductance change). This study provides insights into the effects of electric and magnetic fields applied to the nervous tissue of experimental animal and human studies.