Generation of low-gamma oscillations in a GABAergic network model of the striatum

Striatal oscillations in the low-gamma frequency range have been consistently recorded in a number of experimental studies. However, whether these rhythms are locally generated in the striatum circuit, which is mainly composed of GABAergic neurons, remains an open question. GABAergic medium spiny projection neurons represent the great majority of striatal neurons, but they fire at very low rates. GABAergic fast-spiking interneurons typically show firing rates that are approximately 10 times higher than those of principal neurons, but they are a very small minority of the total neuronal population. In this study, based on physiological constraints we developed a computational network model of these neurons and dissected the oscillations. Simulations showed that the population of medium spiny projection neurons, and not the GABAergic fast-spiking interneurons, determines the frequency range of the oscillations. D2-type dopamine receptor-expressing neurons dominate the generation of low-gamma rhythms. Feedforward inputs from GABAergic fast-spiking interneurons promote the oscillations by strengthening the inhibitory interactions between medium spiny projection neurons. The promotion effect is independent of the degree of synchronization in the fast-spiking interneuron population but affected by the strength of their feedforward inputs to medium spiny projection neurons. Our results provide a theoretical explanation for how firing properties and connections of the three types of GABAergic neurons, which are susceptible to on-going behaviors, experience, and dopamine disruptions, sculpt striatal oscillations.