Neurons in the external globus pallidus (GPe) are autonomous pacemakers, but their spontaneous firing is continually perturbed by synaptic input. Because GPe neurons fire rhythmically in slices, spontaneous inhibitory synaptic currents (IPSCs) should be evident there. We identified periodic series of IPSCs in slices, each corresponding to unitary synaptic currents from one presynaptic cell. Optogenetic stimulation of the striatal indirect pathway axons caused a pause and temporal resetting of the periodic input, confirming that it arose from local neurons subject to striatal inhibition. We determined the firing statistics of the presynaptic neurons from the unitary IPSC statistics and estimated their frequencies, peak amplitudes, and reliabilities. To determine what types of GPe neurons received the spontaneous inhibition, we recorded from genetically labeled parvalbumin (PV) and Npas1-expressing neurons. Both cell types received periodic spontaneous IPSCs with similar frequencies. Optogenetic inhibition of PV neurons reduced the spontaneous IPSC rate in almost all neurons with active unitary inputs, whereas inhibition of Npas1 neurons rarely affected the spontaneous IPSC rate in any neurons. These results suggest that PV neurons provided most of the active unitary inputs to both cell types. Optogenetic pulse stimulation of PV neurons at light levels that can activate cut axons yielded an estimate of connectivity in the fully connected network. The local network is a powerful source of inhibition to both PV and Npas1 neurons, which contributes to irregular firing and may influence the responses to external synaptic inputs.NEW & NOTEWORTHY Brain circuits are often quiet in slices. In the globus pallidus, network activity continues because of the neurons' rhythmic autonomous firing. In this study, synaptic currents generated by the network barrage were measured in single neurons. Unitary synaptic currents arising from single presynaptic neurons were identified by their unique periodicity. Periodic synaptic currents were large and reliable, even at the cell's natural firing rates, but arose from a small number of other globus pallidus neurons.
Keywords: autonomous firing; axon collaterals; globus pallidus; network activity; unitary synaptic currents.