Competing Mechanisms of Gamma and Beta Oscillations in the Olfactory Bulb Based on Multimodal Inhibition of Mitral Cells Over a Respiratory Cycle

International audienceGamma (ϳ40-90 Hz) and beta (ϳ15-40 Hz) oscillations and their associated neuronal assemblies are key features of neuronal sensory processing. However, the mechanisms involved in either their interaction and/or the switch between these different regimes in most sensory systems remain misunderstood. Based on in vivo recordings and biophysical modeling of the mammalian olfactory bulb (OB), we propose a general scheme where OB internal dynamics can sustain two distinct dynamic states, each dominated by either a gamma or a beta regime. The occurrence of each regime depends on the excitability level of granule cells, the main OB interneurons. Using this model framework, we demonstrate how the balance between sensory and centrifugal input can control the switch between the two oscillatory dynamic states. In parallel, we experimentally observed that sensory and centrifugal inputs to the rat OB could both be modulated by the respiration of the animal (2-12 Hz) and each one phase shifted with the other. Implementing this phase shift in our model resulted in the appearance of the alternation between gamma and beta rhythms within a single respiratory cycle, as in our experimental results under urethane anesthesia. Our theoretical framework can also account for the oscillatory frequency response, depending on the odor intensity, the odor valence, and the animal sniffing strategy observed under various conditions including animal freely-moving. Importantly, the results of the present model can form Significance Statement Neuronal oscillations accompany the sensory perception at multiple timescales. Fast-paced activities (gamma, ϳ40-90 Hz; beta, ϳ15-40 Hz) facilitate discrimination and signal cognitive response. Slower processes (2-12 Hz) gate the time window for sensory and centrifugal inputs to ascend and descend, respectively, relative to sensory relays. In the olfactory bulb, which is the first relay of the olfactory system, the main local interneurons provide a major interface between ascending and descending activities. The balance between these two pathways controls the two types of inhibition released by these interneurons on the main relay cells and thereby the network oscillatory dynamics. Using minimalist computational simulations and in vivo experiments, we proposed a general scheme intimately linked to olfactory processing. Theory/New Concepts 2015, 2(6) e0018-15.2015 1-24 a basis to understand how fast rhythms could be controlled by the slower sensory and centrifugal modulations linked to the respiration