Comparison of spontaneous and evoked activity of CA1 pyramidal cells and dentate gyrus granule cells of the hippocampus at an increased extracellular potassium concentration

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We studied the effect of changing extracellular potassium concentration ([K+]o) on spontaneous and evoked burst activity of glutamatergic neurons in the mouse hippocampus using whole-cell patch clamp. We show that increasing [K+]o from 3 to 8.5 mM (potassium load) induced spontaneous tonic (1) and pacemaker burst (2) activity of CA1 pyramidal cells (20% and 10% of the total number of cells, respectively). In contrast to CA1, potassium loading did not lead to the appearance of pacemaker granule cells in the dentate gyrus (DG). Similarly, potassium load increased the evoked burst activity of CA1 pyramidal cells and, paradoxically, suppressed the burst activity of DG granule cells over the entire range of current steps from 10 to 200 pA. Potassium load shifted the current-voltage characteristics to the right and substantially increased inward currents in CA1 and DG cells. Inward and outward currents of DG neurons were 4–4.5 times as high as those of CA1 cells. The possible involvement of potassium-activated potassium-conducting channels is discussed in the bimodal effect of potassium load on the excitability of CA1 and DG glutamatergic neurons. Our results suggest that CA1 pyramidal cells may be more sensitive to potassium load than DG granule cells, which may play a role in hyperexcitation of neural networks during epileptogenesis.

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A. Galashin

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Email: dynnik@rambler.ru
俄罗斯联邦, Pushchino, 142290

M. Konakov

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

Email: dynnik@rambler.ru
俄罗斯联邦, Pushchino, 142290

V. Dynnik

Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences

编辑信件的主要联系方式.
Email: dynnik@rambler.ru
俄罗斯联邦, Pushchino, 142290

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2. Fig. 1. Electrophysiological characteristics of pyramidal neurons of field CA1 at 3 mM and 8.5 mM KCl in extracellular solution. a, b, c – Effect of increased concentration of potassium ions on the resting potential (a), membrane resistance (b) and threshold current (c). d, d – Spontaneous (in the absence of stimulation) bursting (d) and tonic (d) activity at 8.5 mM KCl. e – Current-voltage characteristics of pyramidal neurons of field CA1 at 3 mM and 8.5 mM KCl. Stimulation from –100 to +20 mV for 500 ms from the initial potential of –70 mV. g – Response of pyramidal cells to stimulation with a current of +200 pA for 500 ms relative to the resting potential at 3 mM and 8.5 mM KCl. h – Curves of the dependence of the number of action potentials on the intensity of current stimulation (from 0 to +200 pA for 500 ms relative to the resting potential). * p < 0.05, ns – insignificant; a, b, c – paired t-test; f, h – two-way ANOVA with repeated measures (p < 0.0001) and post hoc Šidák test (p < 0.05). Data are presented as mean ± SEM.

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3. Fig. 2. Electrophysiological characteristics of granule neurons of the dentate gyrus at 3 mM and 8.5 mM KCl in the extracellular solution. a, b, c – Effect of increased concentration of potassium ions on the resting potential (a), membrane resistance (b) and threshold current (c). d – Response of granule cells to stimulation with a current of +200 pA for 500 ms relative to the resting potential at 3 mM and 8.5 mM KCl. g – Curves of the dependence of the number of action potentials on the strength of current stimulation (from 0 to +200 pA for 500 ms relative to the resting potential). e – Absence of spontaneous (in the absence of stimulation) activity in DG cells at 3 mM and 8.5 mM KCl. g – Current-voltage characteristics of granule neurons of the dentate gyrus at 3 mM and 8.5 mM KCl. Stimulation from –100 to +20 mV for 500 ms from the initial potential of –70 mV. * p < 0.05, ns – not significant; a, b, c – paired t-test; d, g – two-way ANOVA with repeated measures (p < 0.0001) and post hoc Šidák test (p < 0.05). Data are presented as mean ± SEM.

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