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We studied the role of cholinergic systems of the rat brain in the mechanisms of acute response of the neocortex and hippocampus to acute hypobaric hypoxia. The activity of choline acetyltransferase and Na/K-ATPase and the protein content were measured in subfractions of synaptic membranes and the synaptoplasm of “light” and “heavy” synaptosomes. The same biochemical indices were measured in fractions of light and heavy synaptosomes from the nucleus of the solitary tract of the medulla oblongata. In the neocortex, we analyzed the ultrastructure of the synaptic pool. We found active involvement of cholinergic systems in the response to acute hypoxia in all brain structures studied. The synapses of cholinergic projection neurons from the basal nuclei of the frontal cortex (light fractions of synaptosomes), neocortical interneurons (heavy fractions of synaptosomes), and, presumably, GABAergic interneurons of the hippocampus (heavy fraction) were the most sensitive to hypoxia. At the limit of resistance to hypoxia, increased metabolic activity predominated in the synapses of rats that had poorly resistance to hypoxia, while in highly resistant rats this activity was diminished. This difference is related to the different duration of their exposure to critical altitude. We found a reduction in the number of synapses and staging in the development of the functional response of synapses to acute hypoxia. We propose a mechanism for the structural and functional reorganization of synaptic links during acute hypoxia, which is general for both poorly and highly resistant rats. We also hypothesize that a reduction of synapses is one of early triggers that switches neurons to levels of interaction that are adequate for hypoxia.