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Different effects of raised [K+]o on membrane potential and contraction in mouse fast- and slow-twitch muscle
S P Cairns1, W A Hing, J R Slack
1Department of Physiology, School of Medicine, University of Auckland, New Zealand.
Abstract:
Increasing extracellular K+ concentration ([K+]o) from 4 to 7-14 mM reduced both tetanic force and resting membrane potential (Em) in isolated slow-twitch soleus and fast-twitch extensor digitorum longus (EDL) muscles of the mouse. The tetanic force-[K+]o relationships showed a greater force loss over 8-11 mM [K+]o in soleus than EDL, mainly because the Em was 2-3 mV less negative at each [K+]o in soleus. The tetanic force-resting Em relationships show that force was reduced in two phases: phase 1 (Em < -60 mV), a 20% force decline in which the relationships superimposed in soleus and EDL, and phase 2 (Em -60 to -55 mV), a marked force decline that was steeper in EDL than soleus. Additionally in phase 2, longer stimulation pulses restored tetanic force; the twitch force-stimulation strength relationship was shifted toward higher voltages; caffeine, a myoplasmic Ca2+ concentration elevator, increased maximum force; and twitch force fell abruptly. We suggest that 1) the K(+)-depressed force is due to reduced Ca2+ release resulting from an altered action potential profile (phase 1) and inexcitable fibers due to an increased action potential threshold (phase 2), and 2) K+ contributes to fatigue in both fast- and slow-twitch muscle when it causes depolarization to about -60 mV.
Insights
High extracellular potassium ([K+]o) impairs muscle force by altering action potentials and increasing excitability thresholds. This affects both slow- and fast-twitch muscles, contributing to fatigue when depolarization reaches -60 mV.
Area of Science:
- Muscle Physiology
- Neuroscience
- Biophysics
Background:
- Extracellular potassium concentration ([K+]o) plays a crucial role in regulating muscle cell membrane potential (Em).
- Changes in [K+]o can significantly impact muscle force production and excitability in both slow- and fast-twitch muscle fibers.
Purpose of the Study:
- To investigate the effects of increasing extracellular K+ concentration on tetanic force and resting membrane potential in isolated mouse soleus and EDL muscles.
- To elucidate the mechanisms underlying K+-induced force depression and identify potential differences between fast- and slow-twitch muscle fibers.
Main Methods:
- Isolated slow-twitch soleus and fast-twitch extensor digitorum longus (EDL) muscles from mice were used.
- Tetanic force and resting membrane potential (Em) were measured at varying extracellular K+ concentrations (4 to 14 mM).
- Force-Em relationships were analyzed, and interventions like altered stimulation pulses and caffeine were employed to probe underlying mechanisms.
Main Results:
- Increasing [K+]o reduced tetanic force and Em in both soleus and EDL muscles.
- Soleus muscles exhibited greater force loss at higher [K+]o (8-11 mM) compared to EDL, attributed to less negative Em.
- Force reduction occurred in two phases: a superimposed decline (Em < -60 mV) and a steeper decline in EDL (Em -60 to -55 mV), suggesting altered action potential profiles and increased thresholds.
Conclusions:
- K+-induced force depression results from reduced Ca2+ release due to altered action potential profiles (Phase 1) and fiber inexcitability from increased action potential threshold (Phase 2).
- Extracellular K+ contributes to muscle fatigue in both fast- and slow-twitch fibers when it depolarizes the membrane potential to approximately -60 mV.