Gamma oscillations in basal ganglia stem from the interplay between local inhibition and beta synchronization
Basal ganglia activity fluctuations have primarily been studied in the context of beta (12-30 Hz) oscillations, a well-established neural marker for Parkinson's Disease (PD). Recent studies have also identified gamma (30-100 Hz) oscillations within the basal ganglia, suggesting it could serve as an alternative marker, but the underlying circuit mechanisms remain poorly understood. Here, through a spiking network model of the basal ganglia, we identified two distinct gamma oscillations: a high-frequency gamma rhythm within the globus pallidus (GPe-TI) and a slower gamma rhythm within D2 medium spiny neurons (MSNs), both stemming from self-inhibition. When we simulated dopamine depletion to mimic the effects of PD, the intensity of gamma oscillations in the GPe-TI was not affected, but their peak frequency increased due to phase-amplitude coupling with pathological beta oscillations. This suggests that the GPe-TI loop, while robust to dopamine depletion, becomes more synchronized with beta activity in the context of PD, leading to faster gamma rhythms. In contrast, gamma oscillations in D2 MSNs were not present in simulated healthy condition and only emerged under dopamine-depleted pathological conditions. Moreover, both their intensity and peak frequency were strongly modulated by pathological beta activity. Together, these findings highlight the complementary roles of self-inhibition and beta oscillations in shaping gamma activity within basal ganglia circuits. The GPe-TI loop primarily sustains high-frequency gamma rhythms, while low frequency gamma rhythms in D2 MSNs are strongly dependent on dopamine-depletion-related beta modulation. These results underscore the importance of network-wide interactions in PD, where pathological beta oscillations influence gamma activity. This study offers insights into the mechanisms of gamma oscillations in PD and highlights the potential of gamma activity, in both the prototypical and striatal loops, as a marker for disease progression and monitoring pathological dysfunction in PD.