Fly Photoreceptors Demonstrate Energy-Information Trade-Offs in Neural Coding

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Abstract
Trade-offs between energy consumption and neuronal performance must shape the design and evolution of nervous systems, but we lack empirical data showing how neuronal energy costs vary according to performance. Using intracellular recordings from the intact retinas of four flies, Drosophila melanogaster, D. virilis, Calliphora vicina, and Sarcophaga carnaria, we measured the rates at which homologous R1–6 photoreceptors of these species transmit information from the same stimuli and estimated the energy they consumed. In all species, both information rate and energy consumption increase with light intensity. Energy consumption rises from a baseline, the energy required to maintain the dark resting potential. This substantial fixed cost, ∼20% of a photoreceptor's maximum consumption, causes the unit cost of information (ATP molecules hydrolysed per bit) to fall as information rate increases. The highest information rates, achieved at bright daylight levels, differed according to species, from ∼200 bits s−1 in D. melanogaster to ∼1,000 bits s−1 in S. carnaria. Comparing species, the fixed cost, the total cost of signalling, and the unit cost (cost per bit) all increase with a photoreceptor's highest information rate to make information more expensive in higher performance cells. This law of diminishing returns promotes the evolution of economical structures by severely penalising overcapacity. Similar relationships could influence the function and design of many neurons because they are subject to similar biophysical constraints on information throughput. Many animals show striking reductions or enlargements of sense organs or brain regions according to their lifestyle and habitat. For example, cave dwelling or subterranean animals often have reduced eyes and brain regions involved in visual processing. These differences suggest that although there are benefits to possessing a particular sense organ or brain region, there are also significant costs that shape the evolution of the nervous system, but little is known about this trade-off, particularly at the level of single neurons. We measured the trade-off between performance and energetic costs by recording electrical signals from single photoreceptors in different fly species. We discovered that photoreceptors in the blowfly transmit five times more information than the smaller photoreceptors of the diminutive fruit fly Drosophila. The blowfly pays a high price for better performance; its photoreceptor uses ten times more energy to code the same quantity of information. We conclude that, for basic biophysical reasons, neuronal energy consumption increases much more steeply than performance, and this intensifies the evolutionary pressure to reduce performance to the minimum required for adequate function. Thus the biophysical properties of sensory neurons help to explain why the sense organs and brains of different species vary in size and performance.