Electric fish strengthen their communication signals nightly and during social encounters by rapidly trafficking ion channels into cell membranes, demonstrating a direct relationship between environmental stimuli, channel trafficking, and behavior.
Electric fish generate and sense electric fields for navigation and communication. These signals can be energetically costly to produce and can attract electroreceptive predators. To minimize costs, some nocturnally active electric fish rapidly boost the power of their signals only at times of high social activity, either as night approaches or in response to social encounters. Here we show that the gymnotiform electric fish Sternopygus macrurus rapidly boosts signal amplitude by 40% at night and during social encounters. S. macrurus increases signal magnitude through the rapid and selective trafficking of voltage-gated sodium channels into the excitable membranes of its electrogenic cells, a process under the control of pituitary peptide hormones and intracellular second-messenger pathways. S. macrurus thus maintains a circadian rhythm in signal amplitude and adapts within minutes to environmental events by increasing signal amplitude through the rapid trafficking of ion channels, a process that directly modifies an ongoing behavior in real time.
Excitable cells, such as neurons and muscle cells, control behavior by generating action potentials, electrical signals that propagate along the cell membrane. Action potentials are generated when the cell allows charged molecules (ions) such as sodium and potassium to move across the membrane through specialized proteins called ion channels. By changing the number of ion channels in the plasma membrane, excitable cells can rapidly remodel their functional characteristics, potentially causing changes in behavior. To gain an understanding of how environmental events cause the remodeling of excitable cell membranes and the resulting behavioral adaptations, we studied the electric communication/navigation signals of an electric fish, Sternopygus macrurus. High amplitude signals facilitate communication and electrolocation, but are energetically costly and more detectable by those predators that can detect electrical signals. We found that Sternopygus increase signal amplitude at night, when they are active, and increase signal amplitude rapidly during social encounters. Electrocytes, the cells that produce the signal, rapidly boost the signal amplitude when they allow more sodium to cross the cell membrane, thereby generating larger action potentials. To increase sodium currents during the action potential, electrocytes rapidly insert additional sodium channels into the cell membrane in response to hormones released into circulation by the pituitary. By adding new ion channels to the electrocyte membrane only during periods of activity or social encounters and removing these channels during inactive periods, these animals can save energy and reduce predation risks associated with communication.