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

Abstract

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.