Typical action potentials drive muscle contraction in C. elegans
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1
Mt. Sinai Hospital, Samuel Lunenfeld Research Institute, Canada
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2
University of Toronto, Department of Molecular Genetics, Canada
Action potential is a rapid and transient change in electrical potential across the membrane to allow them to have an ON-OFF response [1]. At the mammalian neuromuscular junctions (NMJs), a single action potential by the motor neuron evokes one corresponding action potential at the muscle fiber, which triggers muscle contraction [2]. At Drosophila larval NMJs, a single motor neuron action potential evokes sub-threshold, graded response in body wall muscle, whereas adult NMJs display similar properties as in mouse [3]. C. elegans genome does not encode voltage-gated Na+ channel proteins [4]; there has also been no success in recording voltage-gated Na+ currents from any C. elegans tissues. A recent study reported the first successful recording of ‘action potential’ in a single motoneuron [5]; it was however quickly ‘corrected’ by other groups to be plateau potential [6]. Although the possibility of generating typical action potentials by the C. elegans nervous system can’t be completely ruled out, all current evidence argued against its essential or prevalent roles in dictating the precise regulation of muscle contraction or locomotion. How neurons or other excitable cells control their activities, and how the locomotory pattern is generated in C. elegans remains a puzzle.
Using optical stimulation, imaging and electrophysiology studies, here we report:
1) C. elegans body wall muscles fire typical action potentials.
2) The frequency and kinetics of spontaneous firing of action potentials depend on Na+, Ca+ and K+, mediated through the L-type VGCC and two potassium channels.
3) Presynaptic motoneurons regulate the frequency of these action potentials through neurotransmittor release. Excitatory neurotransmittor acetylcholine potentiates the burst of action potentials, whereas GABA inhibits the firing of action potentials.
4) These action potentials drive the contraction of the body wall muscles.
We propose a simple model to resolve how C. elegans regulates its locomotory system: through the ability to fire and modulate the frequency of action potentials, C. elegans body wall muscles turn the graded input from the nervous system into the ON-OFF output signals to control its locomotion. This would be the very first example of utilizing action potentials in postsynaptic cells to modulate the graded presynaptic input.
References
1. Hill, B. Ion Channels of Excitable Membranes (Sinauer, Sunderland, 2001).
2. Hall, Z.W and Sanes J.R. Synaptic Structure and development: The Neuromuscular Junction, Cell. 72, 99-121 (1993).
3. Budnik, V and Ruiz-Canada, C. The Fly Neuromuscular Junction: Structure and Function (Second Edition), Int Rev Neurobiol. 75, 1-406 (2006).
4. Bargmann, C. Neurobiology of the Caenorhabditis elegans Genome, Science.282(5396), 2028-2033 (1998).
5. Mellem, J,E. et al., Action potentials contribute to neuronal signaling in C. elegans,Nat Neurosci. 11(8), 865-7 (2008).
6. Lockery, S.R and Goodman, M.B. The quest for action potential in C. elegans neurons hits a plateau, Nat Neurosci. 12(4), 337-8 (2009).
Conference:
B.R.A.I.N. platform in Physiology poster day 2009, Toronto, ON, Canada, 16 Dec - 16 Dec, 2009.
Presentation Type:
Poster Presentation
Topic:
Poster presentations
Citation:
Gao
S and
Zhen
M
(2009). Typical action potentials drive muscle contraction in C. elegans.
Front. Neurosci.
Conference Abstract:
B.R.A.I.N. platform in Physiology poster day 2009.
doi: 10.3389/conf.neuro.03.2009.17.016
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Received:
17 Dec 2009;
Published Online:
17 Dec 2009.
*
Correspondence:
Shangbang Gao, Mt. Sinai Hospital, Samuel Lunenfeld Research Institute, Toronto, Canada, gao@lunenfeld.ca