Oscillations are a hallmark of neural population activity in various brain regions with a spectrum covering a wide range of frequencies. Within this spectrum γ oscillations have received particular attention due to their ubiquitous nature and their correlation with higher brain functions. Recently, it has been reported that γ oscillations in the hippocampus of behaving rodents are segregated in two distinct frequency bands: slow and fast. These two γ rhythms correspond to different states of the network, but their origin has been not yet clarified.Here we show theoretically and numerically that a single inhibitory population can give rise to coexisting slow and fast γ rhythms corresponding to collective oscillations of a balanced spiking network. The slow and fast γ rhythms are generated via two different mechanisms: the fast one being driven by the coordinated tonic neural firing and the slow one by endogenous fluctuations due to irregular neural activity. We show that almost instantaneous stimulations can switch the collective γ oscillations from slow to fast and vice versa. Furthermore, to draw a connection with the experimental observations, we consider the modulation of the γ rhythms induced by a slower (θ) rhythm driving the network dynamics. In this context, depending on the strength of the forcing and the noise amplitude, we observe phase-amplitude and phase-phase coupling between the fast and slow γ oscillations and the θ forcing. Phase-phase coupling reveals on average different θ-phase preferences for the two coexisting γ rhythms joined to a wide cycle-to-cycle variability.

Theta-nested gamma oscillations have been reported in many areas of the brain and are believed to represent a fundamental mechanism to transfer information across spatial and temporal scales. In a series of recent experiments in vitro it has been possible to replicate with an optogenetic theta frequency stimulation several features of cross-frequency coupling (CFC) among theta and gamma rhythms observed in behaving animals. In order to reproduce the main findings of these experiments we have considered a new class of neural mass models able to reproduce exactly the macroscopic dynamics of spiking neural networks. In this framework, we have examined two setups able to support collective gamma oscillations: namely, the pyramidal interneuronal network gamma (PING) and the interneuronal network gamma (ING). In both setups we observe the emergence of theta-nested gamma oscillations by driving the system with a sinusoidal theta-forcing in proximity of a Hopf bifurcation. These mixed rhythms always display phase amplitude coupling. However, two different types of nested oscillations can be identified: one characterized by a perfect phase locking between theta and gamma rhythms, corresponding to an overall periodic behavior; another one where the locking is imperfect and the dynamics is quasi-periodic or even chaotic. From our analysis it emerges that the locked states are more frequent in the ING setup. In agreement with the experiments, we find theta-nested gamma oscillations for forcing frequencies in the range [1:10] Hz, whose amplitudes grow proportionally to the forcing intensity and which are clearly modulated by the theta phase. Furthermore, analogously to the experiments, the gamma power and the frequency of the gamma-power peak increase with the forcing amplitude. At variance with experimental findings, the gamma-power peak does not shift to higher frequencies by increasing the theta frequency. This effect can be obtained, in our model, only by incrementing, at the same time, also the stimulation power. An effect achieved by increasing the amplitude either of the noise or of the forcing term proportionally to the theta frequency. On the basis of our analysis both the PING and the ING mechanism give rise to theta-nested gamma oscillations with almost identical features.