Synchronization without active chemical synapses during hippocampal afterdischarges.

Abstract

Afterdischarges elicited by antidromic stimulation were studied in the CA1 region of transverse slices of rat hippocampus. The slices were incubated in a static bathing medium containing Mn2+ with lowered Ca2+ concentration, which blocked chemical synaptic transmission. Extracellular voltage recordings from micropipettes revealed afterdischarges of population spikes, which represent synchronized action potentials. Afterdischarge duration became longer with incubation time, occasionally lasting up to 9 s. Simultaneous recordings from three extracellular micropipettes indicated propagation of individual population spikes along the CA1 cell body layer during an afterdischarge. Intracellular recordings from pyramidal cells showed that action potentials were synchronized with population spikes. When initial action potentials of an afterdischarge were blocked by hyperpolarizing the impaled cell, subsequent action potentials remained synchronized with population spikes, indicating a synchronizing interaction between neurons. Intrasomatic neuronal recordings sometimes revealed partial action potentials that were also synchronized with population spikes. During afterdischarges, relatively weak (10 mV) hyperpolarization blocked both full and partial action potentials. These observations suggest that synchronized action potentials and partial spikes were initiated near the soma. Intracellular voltage recordings were referenced to a local extracellular microelectrode in order to determine more accurately the transmembrane potential in the presence of large population spikes .54). Such neuronal recordings revealed brief transmembrane depolarizations that occurred synchronously with population spikes. Large injected hyperpolarizing currents did not affect the brief transmembrane depolarizations. Similar differential voltage recordings across glial cell membranes did not show measurable brief transmembrane depolarizations during population spikes. However, slow glial depolarizations during afterdischarges indicated prolonged K+ accumulation and clearance in the extracellular space, which probably contributed to the hyperexcitability of pyramidal cells. During an afterdischarge, extracellular potentials were recorded simultaneously from six micropipettes arranged perpendicularly to the stratum pyramidale. Current source-density analysis indicated a sink in the cell body layer during population spikes and a corresponding source in distal dendrites. It is concluded that an electrical field effect depolarizes and thus synchronizes neurons during these afterdischarges.(ABSTRACT TRUNCATED AT 400 WORDS)