Cited by 272Neurobiology and Insect Physiology ResearchNeural dynamics and brain functionVisual perception and processing mechanisms

Fly photoreceptors demonstrate energy-information trade-offs in neural coding

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Niven, Jeremy E, Anderson, John C, Laughlin, Simon B·2007·PLoS Biology

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, 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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  1. Land MF, Nilsson D-E (2001) Animal eyes. Oxford: Oxford University Press. 234 p.
  2. Walcott B (1975) Anatomical changes during light-adaptation in insect compound eyes. In: Horridge GA, editor. The compound eye and vision of insects. Oxford: Clarendon Press. pp. 20-33.

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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
Published
2007-03-20
Volume
5
Issue
4
Pages
e116
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
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
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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