Ultra-rapid sodium channel kinetics and a sodium-activated potassium channel maintain high action potential frequencies during rapid modulations of action potential amplitude in a weakly electric fish
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1
The University of Oklahoma, Zoology Department, United States
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2
Yale University School of Medicine, Department of Cellular and Molecular Physiology, United States
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3
The University of Texas at Austin, Section of Neurobiology, United States
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4
The Unviersity of Texas at Austin, Institute for Neuroscience, United States
Energetic demands of action potential (AP) generation are a major cost of electrical signaling by excitable cells in the central nervous system and periphery. Energy consumption by AP generation is particularly acute in the electric organ (EO) of weakly electric fish, and some species regulate AP energetic demands by dynamically regulating AP amplitude. These fish navigate and communicate by generating and sensing electric fields, known as electric organ discharges (EODs) produced by the synchronized action potentials (APs) of electrogenic cells (electrocytes) in the EO. Electrocyte ionic currents are often several microAmperes, many orders of magnitude larger than currents in central neurons, creating significant energetic costs of AP generation.
One class of South American electric fish, wave-type fish, generate sinusoidal waveforms produced by EODs emitted at highly regular rates with interpulse intervals equal to the EOD duration. Most wave-type fish generate EODs at individually-fixed frequencies throughout the lifespan, creating high energetic demands and predation risk from electroreceptive predators. We have shown previously that the wave-type fish Sternopygus macrurus (EOD frequencies 70-150 Hz) manages EOD energetic/predation costs by reducing EOD amplitude during times of inactivity and increasing EOD amplitude during active periods and social interaction. These circadian and socially-induced EOD modulations are produced by rapid changes in AP amplitude controlled by circulating melanocortin hormones that up-regulate Na+ channel trafficking into the electrocyte membrane. The increased Na+ current magnitude also broadens AP and EOD pulse width with little consequence because of the relatively long intervals (5-8 ms) between individual EODs.
Here we investigated the ionic mechanisms of EOD amplitude modulation in Eigenmannia virescens, a related gymnotiform fish that discharges at much higher frequencies (200-600 Hz) likely incurring increased energetic demands of EOD generation. EOD amplitude in this species appears to be particularly sensitive to energetic constraints, and E. virescens exhibits large day-night changes in EOD amplitude, potentially a mechanism of energetic regulation. The ionic currents of its electrocytes are not known nor have the ionic mechanisms of EOD amplitude modulation been determined. We also studied Eigenmannia because its high electrocyte AP frequencies require mechanisms for changing EOD amplitude while maintaining stable EOD pulse width. With inter-pulse intervals less than 2 ms, increases in AP width would shorten the interpulse interval, preventing recovery of Na+ channels sufficient to maintain EOD waveform.
We found that melanocortin peptides applied in vitro increased electrocyte AP amplitude but not AP width. E. virescens electrocytes exhibited a voltage-gated Na+ current with extremely rapid kinetics, an inwardly rectifying K+ current, and a Na+-activated K+ current (KNa) that has not been identified in any gymnotiform species to date. Melanocortin peptides increased the magnitude of all three currents, but increased KNa current is a direct function of enhanced Na+ influx. Numerical simulations suggest that KNa channels are necessary for maintaining stable AP width during AP amplitude modulations. Thus, E. virescens overcomes the challenges of modulating EOD amplitude in a high-frequency signal through ultra-rapid Na+ channel kinetics and a KNa channel that scales repolarizing K+ currents to the magnitude of Na+ currents.
Keywords:
action potential,
Electric organ discharge,
energetics,
Neuromodulation
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for Participant Symposium)
Topic:
Learning, Memory and Behavioral Plasticity
Citation:
Markham
MR,
Kaczmarek
LK and
Zakon
HH
(2012). Ultra-rapid sodium channel kinetics and a sodium-activated potassium channel maintain high action potential frequencies during rapid modulations of action potential amplitude in a weakly electric fish.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00331
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Received:
30 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Michael R Markham, The University of Oklahoma, Zoology Department, Norman, OK, 73019, United States, markham@ou.edu