Molecular variation contributes to the evolution of adaptive phenotypes, though it is often diffi... more Molecular variation contributes to the evolution of adaptive phenotypes, though it is often difficult to understand precisely how. The adaptively significant electric organ discharge behavior of weakly electric fish is the direct result of biophysical membrane properties set by ion channels. Here, we describe a voltage-gated potassium-channel gene in African electric fishes that is under positive selection and highly expressed in the electric organ. The channel produced by this gene shortens electric organ action potentials by activating quickly and at hyperpolarized membrane potentials. The source of these properties is a derived patch of negatively charged amino acids in an extracellular loop near the voltage sensor. We demonstrate that this negative patch acts by contributing to the global surface charge rather than by local interactions with specific amino acids in the channel's extracellular face. We suggest a more widespread role for this loop in the evolutionary tuning of...
Regulating membrane potential and synaptic function contributes significantly to the energetic co... more Regulating membrane potential and synaptic function contributes significantly to the energetic costs of brain signaling, but the relative costs of action potentials (APs) and synaptic transmission during high-frequency firing are unknown. The continuous high-frequency (200-600Hz) electric organ discharge (EOD) of Eigenmannia, a weakly electric fish, underlies its electrosensing and communication. EODs reflect APs fired by the muscle-derived electrocytes of the electric organ (EO). Cholinergic synapses at the excitable posterior membranes of the elongated electrocytes control AP frequency. Based on whole-fish O2 consumption, ATP demand per EOD-linked AP increases exponentially with AP frequency. Continual EOD-AP generation implies first, that ion homeostatic processes reliably counteract any dissipation of posterior membrane ENa and EK and second that high frequency synaptic activation is reliably supported. Both of these processes require energy. To facilitate an exploration of the ...
The bioelectrical properties and resulting metabolic demands of electrogenic cells are determined... more The bioelectrical properties and resulting metabolic demands of electrogenic cells are determined by their morphology and the subcellular localization of ion channels. The electric organ cells (electrocytes) of the electric fish Eigenmannia virescens generate action potentials (APs) with Na+ currents >10 μA and repolarize the AP with Na+-activated K+ (KNa) channels. To better understand the role of morphology and ion channel localization in determining the metabolic cost of electrocyte APs, we used two-photon three-dimensional imaging to determine the fine cellular morphology and immunohistochemistry to localize the electrocytes' ion channels, ionotropic receptors, and Na+-K+-ATPases. We found that electrocytes are highly polarized cells ∼1.5 mm in anterior-posterior length and ∼0.6 mm in diameter, containing ∼30,000 nuclei along the cell periphery. The cell's innervated posterior region is deeply invaginated and vascularized with complex ultrastructural features, whereas...
Energetic demands of social communication signals can constrain signal duration, repetition, and ... more Energetic demands of social communication signals can constrain signal duration, repetition, and magnitude. The metabolic costs of communication signals are further magnified when they are coupled to active sensory systems that require constant signal generation. Under such circumstances, metabolic stress incurs additional risk because energy shortfalls could degrade sensory system performance as well as the social functions of the communication signal. The weakly electric fish Eigenmannia virescens generates electric organ discharges (EODs) that serve as both active sensory and communication signals. These EODs are maintained at steady frequencies of 200-600Hz throughout the lifespan, and thus represent a substantial metabolic investment. We investigated the effects of metabolic stress (food deprivation) on EOD amplitude (EODa) and EOD frequency (EODf) in E. virescens and found that only EODa decreases during food deprivation and recovers after restoration of feeding. Cortisol did ...
We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) ampli... more We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na+ current ( INa) with extremely rapid recovery from inactivation (τrecov = 0.3 ms) allowing complete recovery of Na+ current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K+ current and a Na...
Molecular variation contributes to the evolution of adaptive phenotypes, though it is often diffi... more Molecular variation contributes to the evolution of adaptive phenotypes, though it is often difficult to understand precisely how. The adaptively significant electric organ discharge behavior of weakly electric fish is the direct result of biophysical membrane properties set by ion channels. Here, we describe a voltage-gated potassium-channel gene in African electric fishes that is under positive selection and highly expressed in the electric organ. The channel produced by this gene shortens electric organ action potentials by activating quickly and at hyperpolarized membrane potentials. The source of these properties is a derived patch of negatively charged amino acids in an extracellular loop near the voltage sensor. We demonstrate that this negative patch acts by contributing to the global surface charge rather than by local interactions with specific amino acids in the channel's extracellular face. We suggest a more widespread role for this loop in the evolutionary tuning of...
Regulating membrane potential and synaptic function contributes significantly to the energetic co... more Regulating membrane potential and synaptic function contributes significantly to the energetic costs of brain signaling, but the relative costs of action potentials (APs) and synaptic transmission during high-frequency firing are unknown. The continuous high-frequency (200-600Hz) electric organ discharge (EOD) of Eigenmannia, a weakly electric fish, underlies its electrosensing and communication. EODs reflect APs fired by the muscle-derived electrocytes of the electric organ (EO). Cholinergic synapses at the excitable posterior membranes of the elongated electrocytes control AP frequency. Based on whole-fish O2 consumption, ATP demand per EOD-linked AP increases exponentially with AP frequency. Continual EOD-AP generation implies first, that ion homeostatic processes reliably counteract any dissipation of posterior membrane ENa and EK and second that high frequency synaptic activation is reliably supported. Both of these processes require energy. To facilitate an exploration of the ...
The bioelectrical properties and resulting metabolic demands of electrogenic cells are determined... more The bioelectrical properties and resulting metabolic demands of electrogenic cells are determined by their morphology and the subcellular localization of ion channels. The electric organ cells (electrocytes) of the electric fish Eigenmannia virescens generate action potentials (APs) with Na+ currents >10 μA and repolarize the AP with Na+-activated K+ (KNa) channels. To better understand the role of morphology and ion channel localization in determining the metabolic cost of electrocyte APs, we used two-photon three-dimensional imaging to determine the fine cellular morphology and immunohistochemistry to localize the electrocytes' ion channels, ionotropic receptors, and Na+-K+-ATPases. We found that electrocytes are highly polarized cells ∼1.5 mm in anterior-posterior length and ∼0.6 mm in diameter, containing ∼30,000 nuclei along the cell periphery. The cell's innervated posterior region is deeply invaginated and vascularized with complex ultrastructural features, whereas...
Energetic demands of social communication signals can constrain signal duration, repetition, and ... more Energetic demands of social communication signals can constrain signal duration, repetition, and magnitude. The metabolic costs of communication signals are further magnified when they are coupled to active sensory systems that require constant signal generation. Under such circumstances, metabolic stress incurs additional risk because energy shortfalls could degrade sensory system performance as well as the social functions of the communication signal. The weakly electric fish Eigenmannia virescens generates electric organ discharges (EODs) that serve as both active sensory and communication signals. These EODs are maintained at steady frequencies of 200-600Hz throughout the lifespan, and thus represent a substantial metabolic investment. We investigated the effects of metabolic stress (food deprivation) on EOD amplitude (EODa) and EOD frequency (EODf) in E. virescens and found that only EODa decreases during food deprivation and recovers after restoration of feeding. Cortisol did ...
We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) ampli... more We investigated the ionic mechanisms that allow dynamic regulation of action potential (AP) amplitude as a means of regulating energetic costs of AP signaling. Weakly electric fish generate an electric organ discharge (EOD) by summing the APs of their electric organ cells (electrocytes). Some electric fish increase AP amplitude during active periods or social interactions and decrease AP amplitude when inactive, regulated by melanocortin peptide hormones. This modulates signal amplitude and conserves energy. The gymnotiform Eigenmannia virescens generates EODs at frequencies that can exceed 500 Hz, which is energetically challenging. We examined how E. virescens meets that challenge. E. virescens electrocytes exhibit a voltage-gated Na+ current ( INa) with extremely rapid recovery from inactivation (τrecov = 0.3 ms) allowing complete recovery of Na+ current between APs even in fish with the highest EOD frequencies. Electrocytes also possess an inwardly rectifying K+ current and a Na...
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