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Can the respiratory rhythm be a global signal promoting long-range communication in the brain?

Abstract : The brain is the site of intense rhythmic activity, each area of the brain expressing one or more rhythms. A central question in neuroscience is to understand how these rhythmic activities can coordinate across very distant areas of the brain to solve functions as complex as environmental perception, adapted motor responses or memory formation. One possibility is that the system uses a common time reference, a sort of central clock, from which the different neural networks involved in a function could coordinate. Today, the existence and nature of this clock are still debated. We hypothesize that the respiratory rate could be one of these central clocks, constituting a reference signal for the coordination of different areas of the brain. As a central clock, breathing has major advantages: reliability (because it is a vital function), flexibility (because it adapts to the needs of the organism), low cost (because it is a rhythm which is not not created specifically for this function). In the olfactory system, the link between respiratory rate and neuronal activity is undeniable. Respiration causes slow oscillations in the respiratory rate, bursts of rapid oscillations (gamma and beta) and the discharge of neurons. Recent literature, in which my team participates, has shown that this respiratory influence of neuronal activity is not restricted to the olfactory system, but on the contrary extends to the entire brain (neocortex, amygdala, hippocampus, thalamus). In most of the non-olfactory areas recorded the respiratory rate also modulates the discharge of neurons and rapid oscillations. The slow oscillations associated with breathing therefore seem to affect the overall dynamics of the brain. My thesis project is made up of two parts. First, in order to confirm an influence of the respiratory rate on neurons, I made intracellular recordings in four non-odor areas in anesthetized rats. The targeted structures were the median prefrontal cortex, the primary somatic cortex, the primary visual cortex and finally the hippocampus. I was able to observe respiration modulation in most of these neurons. The quantification of these data shows that the respiratory modulation events are short but observed in a significant number of neurons. These data also provide evidence that the respiratory modulation of various brain areas is not solely due to volume conduction. In a second step, in order to study the coordination of cerebral areas by the respiratory rhythm, I analyzed recordings of multisite local field potentials (LFP) in the vigilant rat. The recordings contain seven areas of the brain (olfactory bulb, anterior piriformis cortex, primary visual cortex, median prefrontal cortex, primary somatic cortex, CA1, dentate gyrus) and respiration. I was able to observe slow oscillations related to respiration in all brain states. But it is during calm awakening that respiratory modulation is greatest and appears in all recorded areas. In parallel, these slow oscillations are coupled with several types of fast oscillations. Finally, I wanted to know if, during the calm state of wakefulness, where LFPs of a large brain network are synchronized with respiration, unit activities can also synchronize with the respiratory signal. To do this, I set up an electrophysiological recording station in constrained vigilant rats allowing the recording of numerous neurons in pairs of cerebral structures with "silicon probes". The station is now functional and I was able to register 6 animals. These last data will not be fully processed when I am defending my thesis. I will present preliminary results which already allow us to show that respiration can synchronize the unit activities of many cells in even spatially distant regions of the brain.
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Submitted on : Tuesday, September 27, 2022 - 3:29:50 PM
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  • HAL Id : tel-03789626, version 1

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Maxime Juventin. Can the respiratory rhythm be a global signal promoting long-range communication in the brain?. Neuroscience. Université de Lyon, 2021. English. ⟨NNT : 2021LYSE1334⟩. ⟨tel-03789626⟩

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