Neuronal and network resonance in the external globus pallidus

The external globus pallidus (GPe) is a connectional hub in the basal ganglia, receiving from and transmitting synaptic signals to all the other structures. The GPe is composed of a set of interconnected GABAergic projection neurons that fire spontaneously and respond to synaptic inputs by small changes in the timing of the next action potential. This style of synaptic integration produces spiking resonance, a preferential entrainment of spiking to input frequency components close to the cell's own firing rate. GPe neurons differ widely in firing rate, and also differ widely in frequency tuning. If the neurons were not interconnected, the GPe composite output would transmit a broad spectrum of input signals, with each cell transmitting signal components in its preferred frequency range. However, we have found that the sparse mutual inhibition among GPe neurons produces a collective resonance in the local network, not present in the response of any single neuron. Using a computer simulation of a 1,000-neuron subset of the GPe with connectivity based on experimental studies, we describe the emergence of a network resonance depending on the transmission delays in the local network. Our findings show that the resonant network response of the GPe does not require changes in the firing rates of individual neurons. Network resonance arises from coherence among neurons at a specific frequency determined by the delay caused by axonal conduction time and synaptic delay for monosynaptic interactions. Network resonance amplifies the collective response to input frequency components at and near this frequency.NEW & NOTEWORTHY Spiking resonance causes spontaneously firing neurons to preferentially encode information about frequency components of their input that are close to the cell's own rate. In the globus pallidus, transmission delays in the local collateral connections can produce an additional resonance in the collective output of neurons sharing a common input.