Fly photoreceptors demonstrate energy-information trade-offs in neural coding
Open accessAbstract
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, approximately 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 approximately 200 bits s(-1) in D. melanogaster to approximately 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.
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In fly photoreceptors, a fivefold increase in performance requires a 25-fold increase in energy consumption.
“In fly photoreceptors, for example, a fivefold increase in performance requires a 25-fold increase in energy consumption [17].”
From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [17]
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- Authors
- Niven, J. E., Anderson, J. C., & Laughlin, S. B.
- Affiliations
- University of Cambridge (GB)
- University of Sussex (GB)
- Corresponding author
- Laughlin, Simon B
- Venue
- PLoS Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2007-03-20
- Volume
- 5
- Issue
- 4
- Pages
- e116
- ISSN
- 1544-9173 (ISSN-L)
- 1545-7885
- PMC
- PMC1828148
- OpenAlex
- W1999488699
- Cited by
- 272
- References
- 85
- Citations by year
- 2026: 10 · 2025: 9 · 2024: 16 · 2023: 9 · 2022: 7 · 2021: 10 · 2020: 11 · 2019: 13 · 2018: 9 · 2017: 24 · 2016: 20 · 2015: 14 · 2014: 20 · 2013: 23 · 2012: 14
- FWCI
- 5.97
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Sussex Research Online (University of Sussex) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
- Funders
- Directorate for Biological Sciences
- Engineering and Physical Sciences Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- neural coding, photoreceptors, Drosophila melanogaster, Drosophila virilis, Calliphora vicina, Sarcophaga carnaria, retinal neurons, information rate, energy consumption, resting membrane potential, ATP hydrolysis, diminishing returns, nervous system evolution, insect vision
- MeSH terms
- Animals, Drosophila, Energy Metabolism, Neurons, Photoreceptor Cells, Invertebrate
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