Acid‐sensing ion channels in neurones of the rat suprachiasmatic nucleus

Chen, Chun‐Hao; Kuo, Yi-Hsuan; Chen, Chih‐Cheng; Huang, Rong-Chi

doi:10.1113/jphysiol.2008.166918

Cited by 36 publications

(32 citation statements)

References 56 publications

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“…4D). These data are consistent with our studies of cultured neurons and earlier studies in brain slices from other brain regions (Chen et al, 2009; Pidoplichko and Dani, 2006; Zha et al, 2006). …”

Section: Resultssupporting

confidence: 94%

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

Ziemann

Allen

Dahdaleh

et al. 2009

Cell

375

455

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SUMMARY The amygdala processes and directs inputs and outputs that are key to fear behavior. However, whether it directly senses fear-evoking stimuli is unknown. Because the amygdala expresses acid sensing ion channel-1a (ASIC1a), and ASIC1a is required for normal fear responses, we hypothesized that the amygdala might detect a reduced pH. We found that inhaled CO2 reduced brain pH and evoked fear behavior in mice. Eliminating or inhibiting ASIC1a markedly impaired this activity, and localized ASIC1a expression in the amygdala rescued the CO2- induced fear deficit of ASIC1a-null animals. Buffering pH attenuated fear behavior, whereas directly reducing pH with amygdala microinjections reproduced the effect of CO2. These data identify the amygdala as an important chemosensor that detects hypercarbia and acidosis and initiates behavioral responses. They also give a molecular explanation for how rising CO2 concentrations elicit intense fear and provide a foundation for dissecting the bases of anxiety and panic disorders.

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Section: Resultssupporting

confidence: 94%

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

Ziemann

Allen

Dahdaleh

et al. 2009

Cell

375

455

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“…This slight hyperpolarization observed in SLO3 mutant sperm from going from pH 7 to 8 may be due to a slight decrease in sodium ion permeability after capacitation. A small decline in P Na after alkalization might be expected since amiloride-sensitive Na + channels have been reported to be sensitive to external pH [29]. This result shows the primacy of SLO3 K + channels in pH-dependent hyperpolarization at an elevated pH.…”

Section: Resultsmentioning

confidence: 71%

Ion Permeabilities in Mouse Sperm Reveal an External Trigger for SLO3-Dependent Hyperpolarization

et al. 2013

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Unlike most cells of the body which function in an ionic environment controlled within narrow limits, spermatozoa must function in a less controlled external environment. In order to better understand how sperm control their membrane potential in different ionic conditions, we measured mouse sperm membrane potentials under a variety of conditions and at different external K+ concentrations, both before and after capacitation. Experiments were undertaken using both wild-type, and mutant mouse sperm from the knock-out strain of the sperm-specific, pH-sensitive, SLO3 K+ channel. Membrane voltage data were fit to the Goldman-Hodgkin-Katz equation. Our study revealed a significant membrane permeability to both K+ and Cl− before capacitation, as well as Na+. The permeability to both K+ and Cl− has the effect of preventing large changes in membrane potential when the extracellular concentration of either ion is changed. Such a mechanism may protect against undesired shifts in membrane potential in changing ionic environments. We found that a significant portion of resting membrane potassium permeability in wild-type sperm was contributed by SLO3 K+ channels. We also found that further activation of SLO3 channels was the essential mechanism producing membrane hyperpolarization under two separate conditions, 1) elevation of external pH prior to capacitation and 2) capacitating conditions. Both conditions produced a significant membrane hyperpolarization in wild-type which was absent in SLO3 mutant sperm. Hyperpolarization in both conditions may result from activation of SLO3 channels by raising intracellular pH; however, demonstrating that SLO3-dependent hyperpolarization is achieved by an alkaline environment alone shows that SLO3 channel activation might occur independently of other events associated with capacitation. For example sperm may undergo stages of membrane hyperpolarization when reaching alkaline regions of the female genital tract. Significantly, other events associated with sperm capacitation, occur in SLO3 mutant sperm and thus proceed independently of hyperpolarization.

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“…The SCN neurons of the reduced preparation could be identified visually with an inverted microscope (IX70; Olympus, Tokyo, Japan). The preparation thus obtained allows rapid application of drugs (Chen et al 2009) and has been used to demonstrate diurnal rhythms in both spontaneous firing and Na/K pump activity (Wang and Huang 2004).…”

Section: Animalsmentioning

confidence: 99%

Intracellular Na⁺and metabolic modulation of Na/K pump and excitability in the rat suprachiasmatic nucleus neurons

Wang

Yang

Huang

2012

Journal of Neurophysiology

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Na/K pump activity and metabolic rate are both higher during the day in the suprachiasmatic nucleus (SCN) that houses the circadian clock. Here we investigated the role of intracellular Na(+) and energy metabolism in regulating Na/K pump activity and neuronal excitability. Removal of extracellular K(+) to block the Na/K pump excited SCN neurons to fire at higher rates and return to normal K(+) to reactivate the pump produced rebound hyperpolarization to inhibit firing. In the presence of tetrodotoxin to block the action potentials, both zero K(+)-induced depolarization and rebound hyperpolarization were blocked by the cardiac glycoside strophanthidin. Ratiometric Na(+) imaging with a Na(+)-sensitive fluorescent dye indicated saturating accumulation of intracellular Na(+) in response to pump blockade with zero K(+). The Na(+) ionophore monensin also induced Na(+) loading and hyperpolarized the membrane potential, with the hyperpolarizing effect of monensin abolished in zero Na(+) or by pump blockade. Conversely, Na(+) depletion with Na(+)-free pipette solution depolarized membrane potential but retained residual Na/K pump activity. Cyanide inhibition of oxidative phosphorylation blocked the Na/K pump to depolarize resting potential and increase spontaneous firing in most cells, and to raise intracellular Na(+) levels in all cells. Nonetheless, the Na/K pump was incompletely blocked by cyanide but completely blocked by iodoacetate to inhibit glycolysis, indicating the involvement of both oxidative phosphorylation and glycolysis in fueling the Na/K pump. Together, the results indicate the importance of intracellular Na(+) and energy metabolism in regulating Na/K pump activity as well as neuronal excitability in the SCN neurons.

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Acid‐sensing ion channels in neurones of the rat suprachiasmatic nucleus

Abstract: We used reduced slice reparations to study ASIC-like currents in the rat central clock suprachiasmatic nucleus (SCN). In reduced SCN preparations, a drop of extracellular pH evoked a desensitizing inward current to excite SCN neurones to fire at higher rates.

Cited by 36 publications

References 56 publications

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

Ion Permeabilities in Mouse Sperm Reveal an External Trigger for SLO3-Dependent Hyperpolarization

Intracellular Na⁺and metabolic modulation of Na/K pump and excitability in the rat suprachiasmatic nucleus neurons

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Acid‐sensing ion channels in neurones of the rat suprachiasmatic nucleus

Abstract: We used reduced slice reparations to study ASIC-like currents in the rat central clock suprachiasmatic nucleus (SCN). In reduced SCN preparations, a drop of extracellular pH evoked a desensitizing inward current to excite SCN neurones to fire at higher rates.

Cited by 36 publications

References 56 publications

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

The Amygdala Is a Chemosensor that Detects Carbon Dioxide and Acidosis to Elicit Fear Behavior

Ion Permeabilities in Mouse Sperm Reveal an External Trigger for SLO3-Dependent Hyperpolarization

Intracellular Na+and metabolic modulation of Na/K pump and excitability in the rat suprachiasmatic nucleus neurons

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Intracellular Na⁺and metabolic modulation of Na/K pump and excitability in the rat suprachiasmatic nucleus neurons