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Contributions of intrinsic and synaptic activities to the generation of neuronal discharges in in vitro hippocampus

Ivan Cohen and Richard Miles

1. Extracellular and intracellular records were made from guinea-pig hippocampal slices to examine the contributions of intrinsic cellular properties and synaptic events to the generation of neuronal activity. Extracellular signals were filtered to pass action potentials, which could be detected within a distance of about 80 µm from a discharging cell.

2. Spontaneous action potentials were invariably detected in records from the stratum pyramidale of CA3 region. Blocking excitatory synaptic transmission with NBQX and APV reduced their frequency by 23 ± 35 %. Suppressing synaptic inhibition, while excitation was already blocked, increased the rate of spike discharge to 177 ± 71 % of its control value.

3. Most action potentials recorded intracellularly from CA3 pyramidal cells were initiated in the absence of a detectable synaptic event. In contrast, most action potentials generated by inhibitory cells located close to stratum pyramidale were preceded by an EPSP.

4. In 31 simultaneous recordings, intracellular pyramidal cell action potentials appeared consistently to initiate extracellular spikes with a mean latency of 2·2 ± 1·0 ms. Single inhibitory cell action potentials could initiate a reduction in the frequency of extracellular spikes of duration 10-30 ms.

5. Some identified extracellular spikes (n = 9) consistently preceded intracellularly recorded IPSPs. IPSPs were initiated monosynaptically with latencies of 0·9-1·5 ms. In reciprocal interactions, single pyramidal cell action potentials could trigger the discharge of an identified unit that in turn appeared to initiate an IPSP in the same pyramidal cell.

6. These data suggest that intrinsic cellular mechanisms underly much of the spontaneous activity of pyramidal cells of the CA3 region of the hippocampus in vitro. Both synaptic inhibition and a strong excitation of inhibitory cells by pyramidal cells act to reduce population activity.

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