Oscillations of Glial Membrane Potential in a Localized Region of the Blood-Brain Barrier of an Insect

In an abdominal ganglion of the American cockroach, Periplaneta americana, electrophysiological characteristics of the perineurium, the glial layer that forms the insect blood-brain barrier, were investigated by microelectrode recording. The potential across the barrier was positive relative to the bathing medium. Its value increased when the external K concentration was raised, as to be expected from a depolarization of the perineurial cell membrane facing the saline, the basolateral membrane. A negative ‘all-or-nothing’ transient, having an amplitude of some 30mV and a half-amplitude duration of about 1.5 min, was also induced, either during the K elevation or after. Given sufficient K exposure, a series of these transients occurred, with a periodicity of 3–15 min, indicating that a cellular oscillator had been activated. The delay between application of high K and the appearance of the first transient was variable, and couldbe as long as 60 min for a threefold increase in K level. The transients could persist upon return of normal saline, for atleast 85min, with little change in amplitude. By recording transperineurial potential simultaneously with recording from superficial cells, one of which was identified as a perineurial cell by peroxidase injection, the transients were found to begenerated by a depolarization of the membrane adjacent to the underlying nerve cells, the adglial membrane. Analysis using a simple electrical model yielded values for the resting electromotive force (e.m.f.) generated by the membranes, −50mV for the basolateral, −71 mV for the adglial, and indicated that the paracellular pathway had a resistance 4.3 times larger than the transcellular resistance. These results reveal a cellular oscillator, apparently of cytosolic type, in the perineurial glia of an insect ganglion, and demonstrate physiological differences between the perineurium of the ganglion and that of other regions of the insect nervous system.