Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro

Abstract

1. In simultaneous recordings from pairs of neurones in hippocampal slices from guinea-pigs, single action potentials fired by CA3 pyramidal cells could initiate inhibitory postsynaptic potentials (IPSPs) in nearby pyramidal cells. 2. The latencies of these IPSPs could be as short as 3 ms. However, they were mediated disynaptically via chemical, excitatory synapses, since inhibitory coupling was suppressed by an excitatory amino acid antagonist. 3. The properties of excitatory synapses made onto inhibitory cells were examined to assess the basis for this strong coupling. Inhibitory cells were identified either by showing that they inhibited another cell or by their characteristic firing pattern. 4. Excitatory postsynaptic potentials (EPSPs) elicited by single pyramidal cell action potentials had a mean amplitude of 1-4 mV and a time to peak of 1.5-4 ms. In most cases they decayed with a time constant similar to that of the inhibitory cell membrane. 5. EPSP amplitude increased with hyperpolarization of the postsynaptic membrane. Membrane polarization had little effect on EPSP shape. 6. EPSPs fluctuated in amplitude and transmission sometimes failed, suggesting transmission was quantal and that few quanta were released. 7. When presynaptic cells were made to fire bursts of action potentials, EPSPs in inhibitory cells were initially potentiated. 8. EPSPs could cause inhibitory cells to fire. The interval between pre- and postsynaptic spikes could be as short as 2.5 ms and the probability of spike transmission could be as high as 0.6. Some inhibitory cells which received feedback excitation were also excited in feedforward fashion by mossy fibre stimuli. 9. One pyramidal cell could activate several disynaptic inhibitory pathways terminating on another pyramidal cell. This suggests that excitatory synapses made by pyramidal cell axon collaterals onto inhibitory cells are divergent. 10. This strong, divergent excitation of inhibitory cells ensures recurrent inhibition is sufficiently widespread, rapid and potent to control the spread of activity by recurrent excitatory connections between CA3 pyramidal cells.