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Developmental maturation of activity‐induced K+ and pH transients and the associated extracellular space dynamics in the rat hippocampus

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The Journal of Physiology

Published online on

Abstract

--- - |2+ Key points Neuronal activity induces fluctuation in extracellular space volume, [K+]o, and pHo, the management of which influences neuronal function The neighbor astrocytes buffer the K+ and pH and swell during the process, causing shrinkage of the extracellular space Here, we report the developmental rise of the homeostatic control of the extracellular space dynamics, the regulation of which becomes tighter with maturation and is thus proposed to ensure efficient synaptic transmission in the mature animals The extracellular space dynamics of volume, [K+]o, and pHo evolve independently with developmental maturation, and while all are inextricably tied to neuronal activity, they do not couple directly Abstract Neuronal activity in the mammalian central nervous system associates with transient extracellular space (ECS) dynamics involving elevated K+ and pH and shrinkage of the ECS. These ECS properties affect membrane potentials, neurotransmitter concentrations, and protein function and are thus anticipated to be under tight regulatory control. It has remained unresolved to what extent these ECS dynamics are developmentally regulated as synaptic precision arises and whether they are directly or indirectly coupled. To resolve the development of homeostatic control of [K+]o, pH, and ECS and their interrelation, we utilized ion‐sensitive microelectrodes in electrically stimulated rat hippocampal slices from rats of different developmental stages (P3–P28). With the employed stimulation paradigm, the stimulus‐evoked peak [K+]o and pHo transients were stable across age groups, until normalized to neuronal activity (field potential amplitude), in which case K+ and pH shifted significantly more in the younger animals. The ECS dynamics, oppositely, increased with age until normalized to the field potential, and thus correlated with neuronal activity. With age, the animals not only managed the peak [K+]o better but displayed swifter post‐stimulus removal of [K+]o, in correlation with the increased expression of the α1‐3 isoforms of the Na+/K+‐ATPase, and swifter return of ECS volume. The different ECS dynamics approached a near‐identical temporal pattern in the more mature animals. In conclusion, while these phenomena are inextricably tied to neuronal activity, our data suggest that they do not couple directly. This article is protected by copyright. All rights reserved - The Journal of Physiology, Volume 0, Issue ja, -Not available-.