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CO2 chemosensitivity in Helix aspersa: three potassium currents mediate pH-sensitive neuronal spike timing
Jerod S Denton1, F V McCann, J C Leiter
1Department of Physiology, Dartmouth Medical School, Lebanon, NH 03756, USA.
American Journal of Physiology. Cell Physiology
|August 25, 2006
Summary
Elevated carbon dioxide (CO(2)) triggers lung ventilation in snails by affecting pH-sensitive potassium channels in specific neurons. This study reveals multiple potassium channels are inhibited by acidosis, enhancing neuronal activity.
Area of Science:
- Neuroscience
- Respiratory Physiology
- Cellular Biology
Background:
- Elevated carbon dioxide (CO(2)) levels stimulate lung ventilation in the snail Helix aspersa.
- This hypercapnic response is mediated by CO(2)-sensitive neurons located in the dorsal subesophageal ganglia.
- The precise molecular mechanisms underlying this chemosensory response remain incompletely understood.
Purpose of the Study:
- To investigate the hypothesis that pH-dependent inhibition of potassium channels in the dorsal subesophageal ganglia neurons mediates the CO(2) chemosensory response.
- To identify the specific types of potassium channels involved and their sensitivity to pH changes.
- To elucidate the role of these channels in neuronal excitability during hypercapnia.
Main Methods:
- Isolation and electrophysiological characterization of neurons from the dorsal subesophageal ganglia.
- Application of acid challenges to assess CO(2) chemosensitivity and changes in membrane properties.
- Voltage-clamp analysis to identify and study the properties of voltage-dependent potassium channels (I(KA) and I(KDR)).
- Investigation of pH-sensitive calcium-activated potassium channels (I(KCa)) in neurons in situ.
- Pharmacological manipulation using potassium channel inhibitors to mimic acidification effects.
Main Results:
- Isolated neurons exhibited CO(2) chemosensitivity, with membrane depolarization and increased input resistance during acid challenges.
- Two main potassium conductances, I(KA) and I(KDR), were identified in isolated neurons, both inhibited by hypercapnia.
- I(KA) activity was sensitive to both extracellular and intracellular pH, while I(KDR) was modulated by extracellular pH only.
- Evidence for a pH-sensitive calcium-activated potassium channel (I(KCa) was found in situ.
- Inhibitors of I(KA) and I(KDR) mimicked the effects of acidification on isolated cells and in situ neurons.
Conclusions:
- The study supports the hypothesis that pH-dependent inhibition of potassium channels mediates the CO(2) chemosensory response in Helix aspersa.
- I(KA) appears to initiate the chemosensory response, while I(KDR) and I(KCa) contribute to prolonging neuronal activation.
- Multiple potassium channels are inhibited by acidosis, collectively enhancing neuronal excitability and mediating the respiratory response to CO(2).
- The identified chemosensitive channels are not unique, suggesting the underlying molecular machinery for CO(2) chemosensitivity is widespread among neurons.
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