title: Ionic mechanisms of microsecond-scale spike timing in single cells.
abstract: Electric fish image their environments and communicate by generating electric organ discharges through the simultaneous action potentials (APs) of electric organ cells (electrocytes) in the periphery. Steatogenys elegans generates a biphasic electrocyte discharge by the precisely regulated timing and waveform of APs generated from two excitable membranes present in each electrocyte. Current-clamp recordings of electrocyte APs reveal that the posterior membrane fires first, followed ∼30 μs later by an AP on the anterior membrane. This delay was maintained even as the onset of the first AP was advanced >5 ms by increasing stimulus intensity and across multiple spikes during bursts of APs elicited by prolonged stimulation. Simultaneous cell-attached loose-patch recordings of Na(+) currents on each membrane revealed that activation voltage for Na(+) channels on the posterior membrane was 10 mV hyperpolarized compared with Na(+) channels on the anterior membrane, with no differences in activation or inactivation kinetics. Computational simulations of electrocyte APs demonstrated that this difference in Na(+) current activation voltage was sufficient to maintain the proper firing order and the interspike delay. A similar difference in activation threshold has been reported for the Na(+) currents of the axon initial segment compared with somatic Na(+) channels of pyramidal neurons, suggesting convergent evolution of spike initiation and timing mechanisms across different systems of excitable cells.
authors.affiliation: Department of Biology, The University of Oklahoma, Norman, Oklahoma 73019, and Section of Neurobiology and Institute for Neuroscience, The University of Texas at Austin, Austin, Texas 78712.
authors.forename: Michael R
authors.initials: MR
authors.lastname: Markham
authors.forename: Harold H
authors.initials: HH
authors.lastname: Zakon
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000465:Algorithms; D000818:Animals; D001369:Axons / Q000502:physiology; D002462:Cell Membrane / Q000502:physiology; D003198:Computer Simulation; D004555:Electric Fish / Q000502:physiology*; D004557:Electric Organ / Q000166:cytology* / Q000502:physiology*; D055724:Electrophysiological Phenomena / Q000502:physiology*; D005260:Female; D066298:In Vitro Techniques; D007700:Kinetics; D008297:Male; D008566:Membranes / Q000502:physiology; D008959:Models, Neurological; D018408:Patch-Clamp Techniques; D026902:Potassium Channel Blockers / Q000494:pharmacology; D015221:Potassium Channels / Q000187:drug effects / Q000502:physiology; D026941:Sodium Channel Blockers / Q000494:pharmacology; D015222:Sodium Channels / Q000502:physiology; D013779:Tetrodotoxin / Q000494:pharmacology
chemical_list: D026902:Potassium Channel Blockers; D015221:Potassium Channels; D026941:Sodium Channel Blockers; D015222:Sodium Channels; D013779:Tetrodotoxin
keywords: action potential; electric organ; ion channels