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Deletion of aquaporin-4 increases extracellular K(+) concentration during synaptic stimulation in mouse hippocampus.

Haj-Yasein NN, Bugge CE, Jensen V, Østby I, Ottersen OP, Hvalby Ø, Nagelhus EA - Brain Struct Funct (2014)

Bottom Line: We show that Aqp4 deletion has a layer-specific effect on [K(+)]o that precisely mirrors the known effect on extracellular volume dynamics.In stratum pyramidale and corpus callosum, neither peak [K(+)]o nor post-stimulus [K(+)]o recovery was affected by Aqp4 deletion.Our data suggest that AQP4 modulates [K(+)]o during synaptic stimulation through its effect on extracellular space volume.

View Article: PubMed Central - PubMed

Affiliation: Letten Centre, Institute of Basic Medical Sciences, University of Oslo, 0317, Oslo, Norway.

ABSTRACT
The coupling between the water channel aquaporin-4 (AQP4) and K(+) transport has attracted much interest. In this study, we assessed the effect of Aqp4 deletion on activity-induced [K(+)]o changes in acute slices from hippocampus and corpus callosum of adult mice. We show that Aqp4 deletion has a layer-specific effect on [K(+)]o that precisely mirrors the known effect on extracellular volume dynamics. In CA1, the peak [K(+)]o in stratum radiatum during 20 Hz stimulation of Schaffer collateral/commissural fibers was significantly higher in Aqp4 (-/-) mice than in wild types, whereas no differences were observed throughout the [K(+)]o recovery phase. In stratum pyramidale and corpus callosum, neither peak [K(+)]o nor post-stimulus [K(+)]o recovery was affected by Aqp4 deletion. Our data suggest that AQP4 modulates [K(+)]o during synaptic stimulation through its effect on extracellular space volume.

No MeSH data available.


Impact of Aqp4 deletion on extracellular K+ dynamics during synaptic stimulation. a Potassium responses during and after 10 s stimulation at 20 Hz (black horizontal bar along the abscissa) from hippocampal synaptic stratum radiatum layer CA1 of wild type (blue circles, n = 60) and Aqp4−/− mice (red circles, n = 57). Vertical bars indicate SEM. Bracket indicates period of statistical significant difference (p < 0.05) between genotypes. Insets a schematic drawing of the hippocampal formation with recording and stimulating electrodes; electrode calibration graph for the K+-sensitive electrodes showing the relationship between voltage and [K+]o (bars indicate SD); histogram of the K+-decay constants, measured during the post-stimulation phase (bars indicate SEM). b As in a, but the recordings are from the stratum pyramidale (n = 21 for wild type mice, n = 25 for Aqp4−/− mice). c As in a, but during blockade of ionotropic glutamate receptors (50 μM AP5 and 20 μM DNQX) thus isolating the changes in [K+]o mediated by axonal activity. The figure shows that [K+]o during and after high-frequency stimulation was similar in the two genotypes (n = 20 for wild type mice, n = 22 for Aqp4−/− mice). d As in a, but experiments were performed on myelinated fibers of the corpus callosum. Inset a schematic drawing of the corpus callosum with recording and stimulating electrodes (n = 21 for wild type mice, n = 23 for Aqp4−/− mice)
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Fig2: Impact of Aqp4 deletion on extracellular K+ dynamics during synaptic stimulation. a Potassium responses during and after 10 s stimulation at 20 Hz (black horizontal bar along the abscissa) from hippocampal synaptic stratum radiatum layer CA1 of wild type (blue circles, n = 60) and Aqp4−/− mice (red circles, n = 57). Vertical bars indicate SEM. Bracket indicates period of statistical significant difference (p < 0.05) between genotypes. Insets a schematic drawing of the hippocampal formation with recording and stimulating electrodes; electrode calibration graph for the K+-sensitive electrodes showing the relationship between voltage and [K+]o (bars indicate SD); histogram of the K+-decay constants, measured during the post-stimulation phase (bars indicate SEM). b As in a, but the recordings are from the stratum pyramidale (n = 21 for wild type mice, n = 25 for Aqp4−/− mice). c As in a, but during blockade of ionotropic glutamate receptors (50 μM AP5 and 20 μM DNQX) thus isolating the changes in [K+]o mediated by axonal activity. The figure shows that [K+]o during and after high-frequency stimulation was similar in the two genotypes (n = 20 for wild type mice, n = 22 for Aqp4−/− mice). d As in a, but experiments were performed on myelinated fibers of the corpus callosum. Inset a schematic drawing of the corpus callosum with recording and stimulating electrodes (n = 21 for wild type mice, n = 23 for Aqp4−/− mice)

Mentions: In the hippocampus, orthodromic synaptic stimuli (50 μs, <300 μA, 0.1 Hz) were delivered through a tungsten electrode situated in stratum radiatum of the CA1 region. The extracellular synaptic responses were monitored by a reference glass electrode (filled with ACSF) placed close to the ion-sensitive electrode in stratum radiatum or stratum pyramidale at a fixed distance (400 µm) from the stimulation electrode (Fig. 2a, inset). The reference electrode was coupled to the ion-sensitive microelectrode (custom-built differential amplifier, 2 Hz low-pass filter). Thus, the monitored changes in direct current (DC) level reflected the changes in [K+]o.


Deletion of aquaporin-4 increases extracellular K(+) concentration during synaptic stimulation in mouse hippocampus.

Haj-Yasein NN, Bugge CE, Jensen V, Østby I, Ottersen OP, Hvalby Ø, Nagelhus EA - Brain Struct Funct (2014)

Impact of Aqp4 deletion on extracellular K+ dynamics during synaptic stimulation. a Potassium responses during and after 10 s stimulation at 20 Hz (black horizontal bar along the abscissa) from hippocampal synaptic stratum radiatum layer CA1 of wild type (blue circles, n = 60) and Aqp4−/− mice (red circles, n = 57). Vertical bars indicate SEM. Bracket indicates period of statistical significant difference (p < 0.05) between genotypes. Insets a schematic drawing of the hippocampal formation with recording and stimulating electrodes; electrode calibration graph for the K+-sensitive electrodes showing the relationship between voltage and [K+]o (bars indicate SD); histogram of the K+-decay constants, measured during the post-stimulation phase (bars indicate SEM). b As in a, but the recordings are from the stratum pyramidale (n = 21 for wild type mice, n = 25 for Aqp4−/− mice). c As in a, but during blockade of ionotropic glutamate receptors (50 μM AP5 and 20 μM DNQX) thus isolating the changes in [K+]o mediated by axonal activity. The figure shows that [K+]o during and after high-frequency stimulation was similar in the two genotypes (n = 20 for wild type mice, n = 22 for Aqp4−/− mice). d As in a, but experiments were performed on myelinated fibers of the corpus callosum. Inset a schematic drawing of the corpus callosum with recording and stimulating electrodes (n = 21 for wild type mice, n = 23 for Aqp4−/− mice)
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Fig2: Impact of Aqp4 deletion on extracellular K+ dynamics during synaptic stimulation. a Potassium responses during and after 10 s stimulation at 20 Hz (black horizontal bar along the abscissa) from hippocampal synaptic stratum radiatum layer CA1 of wild type (blue circles, n = 60) and Aqp4−/− mice (red circles, n = 57). Vertical bars indicate SEM. Bracket indicates period of statistical significant difference (p < 0.05) between genotypes. Insets a schematic drawing of the hippocampal formation with recording and stimulating electrodes; electrode calibration graph for the K+-sensitive electrodes showing the relationship between voltage and [K+]o (bars indicate SD); histogram of the K+-decay constants, measured during the post-stimulation phase (bars indicate SEM). b As in a, but the recordings are from the stratum pyramidale (n = 21 for wild type mice, n = 25 for Aqp4−/− mice). c As in a, but during blockade of ionotropic glutamate receptors (50 μM AP5 and 20 μM DNQX) thus isolating the changes in [K+]o mediated by axonal activity. The figure shows that [K+]o during and after high-frequency stimulation was similar in the two genotypes (n = 20 for wild type mice, n = 22 for Aqp4−/− mice). d As in a, but experiments were performed on myelinated fibers of the corpus callosum. Inset a schematic drawing of the corpus callosum with recording and stimulating electrodes (n = 21 for wild type mice, n = 23 for Aqp4−/− mice)
Mentions: In the hippocampus, orthodromic synaptic stimuli (50 μs, <300 μA, 0.1 Hz) were delivered through a tungsten electrode situated in stratum radiatum of the CA1 region. The extracellular synaptic responses were monitored by a reference glass electrode (filled with ACSF) placed close to the ion-sensitive electrode in stratum radiatum or stratum pyramidale at a fixed distance (400 µm) from the stimulation electrode (Fig. 2a, inset). The reference electrode was coupled to the ion-sensitive microelectrode (custom-built differential amplifier, 2 Hz low-pass filter). Thus, the monitored changes in direct current (DC) level reflected the changes in [K+]o.

Bottom Line: We show that Aqp4 deletion has a layer-specific effect on [K(+)]o that precisely mirrors the known effect on extracellular volume dynamics.In stratum pyramidale and corpus callosum, neither peak [K(+)]o nor post-stimulus [K(+)]o recovery was affected by Aqp4 deletion.Our data suggest that AQP4 modulates [K(+)]o during synaptic stimulation through its effect on extracellular space volume.

View Article: PubMed Central - PubMed

Affiliation: Letten Centre, Institute of Basic Medical Sciences, University of Oslo, 0317, Oslo, Norway.

ABSTRACT
The coupling between the water channel aquaporin-4 (AQP4) and K(+) transport has attracted much interest. In this study, we assessed the effect of Aqp4 deletion on activity-induced [K(+)]o changes in acute slices from hippocampus and corpus callosum of adult mice. We show that Aqp4 deletion has a layer-specific effect on [K(+)]o that precisely mirrors the known effect on extracellular volume dynamics. In CA1, the peak [K(+)]o in stratum radiatum during 20 Hz stimulation of Schaffer collateral/commissural fibers was significantly higher in Aqp4 (-/-) mice than in wild types, whereas no differences were observed throughout the [K(+)]o recovery phase. In stratum pyramidale and corpus callosum, neither peak [K(+)]o nor post-stimulus [K(+)]o recovery was affected by Aqp4 deletion. Our data suggest that AQP4 modulates [K(+)]o during synaptic stimulation through its effect on extracellular space volume.

No MeSH data available.