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Specific rearrangements of the brain bioelectric potential field and the structures where the components (waves) of the main EEG rhythms interact, as well as the stereotactic location and power of the equivalent electrical dipole sources (EEDSs), were studied at various stages of acute experimental hypoxia (breathing for 15–30 min a hypoxic gas mixture containing 8% oxygen in nitrogen). The disrupted intercentral relationships that ensure the formation of the dynamic “morphological equivalent” to support the integrative brain activity, rearrangements of this activity, and the adaptive functions of the whole brain proved to account for partial or complete disintegration of systemic brain activity during acute hypoxia. EEDS tomography showed that EEDSs responsible for the generation of the basic brain rhythmic pattern are normally located in the thalamic structures. At the initial stages of hypoxia, the distribution of the EEDS foci is changed so that the density of EEDSs is increased on the sections that include the hypothalamic region structures, basal nuclei of the forebrain, and the limbic system; the basal, frontal, and medial regions of the temporal lobes of both hemispheres are also involved. With increasing hypoxia, EEDSs appeared in the basal and medial regions of the frontal lobes. At this time, both the surface and deep regions of the frontal lobes of the brain hemispheres are the major targets of the hypoxic effect. At the stages of severe hypoxia, pronounced functional changes in the CNS are observed, including the phenomenon of movement of multiple EEDS foci primarily through the basal and mediobasal regions of the frontal and temporal lobes and in the limbic system structures. Thus, despite the generalized high-amplitude paroxysmal activity that is observed in EEG, a functional disintegration (disruption) of interactions between individual brain regions appears and leads to disturbed regulation of the brain and systemic brain activity. Spatiotemporal EEG markers have been identified that make it possible to assess the individual sensitivity and resistance to hypoxia, as well as the degree of disintegration of his systemic brain activity at different stages of hypoxia.