Role of glia in K+ and pH homeostasis in the neonatal rat spinal cord

Stimulation‐evoked transient changes in extracellular potassium ([K+]e) and pH (pHe) were studied in the neonatal rat spinal cords isolated from 3–13‐day‐old pups. In unstimulated pups the [K+]e baseline was elevated and pHe was more acid than that in Ringer's solution (3.5 mM K+, pH 7.3–7.35). The [K+]e and pHe in 3–6‐day‐old pups was 3.91 ± 0.12 mM and pHe 7.19 ± 0.01, respectively, while in 10–13‐day‐old pups it was 4.35 ± 0.15 mM and 7.11 ± 0.01, respectively. The [K+]e changes evoked in the dorsal horn by a single electrical stimulus were as large as 1.5–2.5 mM. Such changes in [K+]e are evoked in the adult rat spinal cord with stimulation at a frequency of 10–30 Hz. The maximal changes of 2.1–6.5 mM were found at a stimulation frequency of 10 Hz in 3–6‐day‐old animals. In older animals the [K+]e changes progressively decreased. The poststimulation K+‐undershoot was found after a single stimulus as well as after repetitive stimulation. In 3–8‐day‐old pups, the stimulation evoked an alkaline shift, which was followed by a smaller poststimulation acid shift when the stimulation was discontinued. In pups 3–4‐days‐old the stimulation evoked the greatest alkaline shifts, i.e., by as much as 0.05 pH units after a single pulse and by about 0.1 pH units during stimulation at a frequency of 10 Hz. In 5–8‐day‐old pups, the alkaline shift became smaller and the poststimulation acid shift increased. Stimulation in 10–13‐day‐old pups produced an acid shift of 0.03–0.07 pH units, which was preceded by a scarcely discernible alkaline shift. MgCl2 (20 mM) reversibly reduced the alkaline but not the acid shifts by 50–60%. Bath application of the carbonic anhydrase inhibitor acetazolamide had no effect on the alkaline shift, while the acid shift decreased by 70–80%. The superfusion of the cord with 10 mM KCl resulted in acid shifts of 0.10–0.14 pH units. We conclude that the [K+]e ceiling level and the character of pHe transients in the spinal cord are closely related to gliogenesis. Our results suggest that glial cells buffer the activity‐related [K+]e increase and alkaline pHe shifts in the extracellular space.