Modulation of voltage-dependent K+ conductances in photoreceptors trades off investment in contrast gain for bandwidth

Modulation is essential for adjusting neurons to prevailing conditions and differing demands. Yet understanding how modulators adjust neuronal properties to alter information processing remains unclear, as is the impact of neuromodulation on energy consumption. Here we combine two computational models, one Hodgkin-Huxley type and the other analytic, to investigate the effects of neuromodulation upon Drosophila melanogaster photoreceptors. Voltage-dependent K+ conductances in these photoreceptors: (i) activate upon depolarisation to reduce membrane resistance and adjust bandwidth to functional requirements; (ii) produce negative feedback to increase bandwidth in an energy efficient way; (iii) produce shunt-peaking thereby increasing the membrane gain bandwidth product; and (iv) inactivate to amplify low frequencies. Through their effects on the voltage-dependent K+ conductances, three modulators, serotonin, calmodulin and PIP2, trade-off contrast gain against membrane bandwidth. Serotonin shifts the photoreceptor performance towards higher contrast gains and lower membrane bandwidths, whereas PIP2 and calmodulin shift performance towards lower contrast gains and higher membrane bandwidths. These neuromodulators have little effect upon the overall energy consumed by photoreceptors, instead they redistribute the energy invested in gain versus bandwidth. This demonstrates how modulators can shift neuronal information processing within the limitations of biophysics and energy consumption.Author summary: The properties of neurons and neural circuits can be adjusted by neuromodulators, molecules that alter their ability to respond to future activity. Many neuromodulators target voltage-dependent ion channels, molecular components of cell membranes that influence the electrical activity of neurons. Because of their importance, the action of neuromodulators upon voltage-dependent ion channels and the subsequent changes in neural activity has been studied extensively. However, the properties of voltage-dependent ion channels also influence the energy that neural signalling consumes. Here we assess the impact of neuromodulators upon neuronal energy consumption. We use analytical and computational models to determine the impact of different neuromodulators upon the signalling properties and energy consumption of fly photoreceptors. Our models uncover previously unknown properties of voltage-dependent ion channels in fly photoreceptors, showing how they adjust the membrane properties, gain and bandwidth, to prevailing light levels. Neuromodulators alter voltage-dependent ion channel properties, adjusting the gain and bandwidth. Although neuromodulators do not substantially alter the overall energy consumption of photoreceptors, they redistribute energy investment in gain and bandwidth. Hence, our models provide novel insights into the functions that neuromodulators play in neurons and neural circuits.