Fly photoreceptors demonstrate energy-information trade-offs in neural coding.pdf (704.56 kB)
Fly photoreceptors demonstrate energy-information trade-offs in neural coding
journal contribution
posted on 2023-06-07, 07:19 authored by Jeremy NivenJeremy Niven, John C Anderson, Simon B LaughlinTrade-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.
History
Publication status
- Published
File Version
- Published version
Journal
PLoS BiologyISSN
1544-9173Publisher
Public Library of ScienceExternal DOI
Volume
5Page range
828-840Event location
United StatesDepartment affiliated with
- Evolution, Behaviour and Environment Publications
Full text available
- Yes
Peer reviewed?
- Yes
Legacy Posted Date
2020-06-23First Open Access (FOA) Date
2020-06-23First Compliant Deposit (FCD) Date
2020-06-23Usage metrics
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