Ion channel regulation of the dynamical instability of the resting membrane potential in saccular hair cells of the green frog (Rana esculenta)

Aims:  We investigated the ion channel regulation of the resting membrane potential of hair cells with the aim to determine if the resting membrane potential is poised close to instability and thereby a potential cause of the spontaneous afferent spike activity. Methods:  The ionic mechanism and the...

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Published in:Acta physiologica Scandinavica 2005-12, Vol.185 (4), p.271-290
Main Authors: Jørgensen, F., Kroese, A. B. A.
Format: Article
Language:English
Subjects:
Animals
Biological and medical sciences
Calcium Channels - metabolism
Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation
Fundamental and applied biological sciences. Psychology
hair cell
Hair Cells, Auditory - metabolism
Ion Channel Gating - physiology
Ion Channels - metabolism
membrane potential
Membrane Potentials - physiology
Models, Biological
Patch-Clamp Techniques
potassium channels
Potassium Channels - metabolism
Rana esculenta
Saccule and Utricle
sacculus
Vertebrates: nervous system and sense organs
voltage fluctuation
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Summary:Aims:  We investigated the ion channel regulation of the resting membrane potential of hair cells with the aim to determine if the resting membrane potential is poised close to instability and thereby a potential cause of the spontaneous afferent spike activity. Methods:  The ionic mechanism and the dynamic properties of the resting membrane potential were examined with the whole‐cell patch clamp technique in dissociated saccular hair cells and in a mathematical model including all identified ion channels. Results:  In hair cells showing I/V curves with a low membrane conductance flanked by large inward and outward rectifying potassium conductances, the inward rectifier (KIR), the delayed outward rectifier (KV) and the large conductance, calcium‐sensitive, voltage‐gated potassium channel (BKCa) were all activated at rest. Under current clamp conditions, the outward current through these channels balanced the inward current through mechano‐electrical transduction (MET) and Ca2+ channels. In 45% (22/49) of the cells, the membrane potential fluctuated spontaneously between two voltage levels determined by the voltage extent of the low membrane conductance range. These fluctuations were not influenced by blocking the MET channels but could be reversibly stopped by increasing [K+]o or by blocking of KIR channels. Blocking the BKCa channels induced regular voltage oscillations. Conclusions:  Two intrinsic dynamical instabilities of Vm are present in hair cells. One of these is observed as spontaneous voltage fluctuations by currents through KIR, KV and h‐channels in combination with a steady current through MET channels. The other instability shows as regenerative voltage changes involving Ca2+ and KV channels. The BKCa channels prevent the spontaneous voltage fluctuations from activating the regenerative system.
ISSN:0001-6772
1365-201X
DOI:10.1111/j.1365-201X.2005.01495.x