Abstract

Gamma (∼40-90 Hz) and beta (∼15-40 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 a basis to understand how fast rhythms could be controlled by the slower sensory and centrifugal modulations linked to the respiration. Visual Abstract: See Abstract.

Highlights

  • Oscillatory activity underlying neuronal assembly formation is crucial in most functions, including environment perception, adaptive motor responses, and memory formation (Engel and Singer, 2001; Tallon-Baudry et al, 2001; Varela et al, 2001)

  • mitral cells (MCs)/granule cells (GCs) dendrodendritic interactions were proven to be critically involved in gamma oscillations (Desmaisons et al, 1999; Lagier et al, 2004) and were suggested to be involved in beta oscillations (Fourcaud-Trocmé et al, 2014; Lepousez et al, 2014)

  • GCs were shown to display two different modes of dendritic activation (Egger et al, 2003, 2005), as follows: a local mode with a local dendritic depolarization due to MC excitation limited to a single branch of the GC dendritic tree; and a global mode with a full dendritic arbor depolarization caused by GC spikes

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Summary

Introduction

Oscillatory activity underlying neuronal assembly formation is crucial in most functions, including environment perception, adaptive motor responses, and memory formation (Engel and Singer, 2001; Tallon-Baudry et al, 2001; Varela et al, 2001). Those oscillatory mechanisms involve fine and broader timescales (Schroeder et al, 2010). These mechanisms proved to be difficult to disentangle In this regard, the olfactory bulb (OB) is well suited to investigate those mechanisms because of both the ability to handle separately the arrival of sensory inputs and centrifugal fibers (Ravel and Pager, 1990; Boyd et al, 2012; Markopoulos et al, 2012), and the prominence of these multiscale temporal phenomena. The occurrence pattern of those two fast alternating oscillations are intertwined with the respiratory slow rhythm (Buonviso et al, 2003; Lepousez and Lledo, 2013; Fukunaga et al, 2014), which

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