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

Niven JE, Anderson JC, Laughlin SB - PLoS Biol. (2007)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.

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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The Scaling of Metabolic Cost with Performance in Dipteran R1–6 PhotoreceptorsThe logarithms of the total cost (open symbols) and the fixed cost (solid symbols) are plotted against the logarithm of maximum information rate. Costs are in ATP molecules hydrolysed per photoreceptor per second. Each data point represents the mean values from R1–6 photoreceptors in one of the four dipteran species used in this study. The linear fits suggest that the total cost of photoreceptor signalling (dashed line) increases as (information rate)1.7, and the fixed cost of maintaining the photoreceptor in the dark (solid line) increases as (information rate)1.47.
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pbio-0050116-g007: The Scaling of Metabolic Cost with Performance in Dipteran R1–6 PhotoreceptorsThe logarithms of the total cost (open symbols) and the fixed cost (solid symbols) are plotted against the logarithm of maximum information rate. Costs are in ATP molecules hydrolysed per photoreceptor per second. Each data point represents the mean values from R1–6 photoreceptors in one of the four dipteran species used in this study. The linear fits suggest that the total cost of photoreceptor signalling (dashed line) increases as (information rate)1.7, and the fixed cost of maintaining the photoreceptor in the dark (solid line) increases as (information rate)1.47.

Mentions: The information rates measured with our brightest stimuli are indicative of a photoreceptor's maximum performance. Comparing metabolic costs with these highest rates, we see that both the total cost and the dark cost increase supralinearly with performance. Plots of the logarithms of costs against the logarithms of highest rates (Figure 7) suggest that the total cost increases as (performance)1.7, and the dark cost increases close to (performance)1.5, but with only four species these exponents are preliminary estimates. Nonetheless, there is no doubt that both the unit cost of information (the total cost per bit) and the dark cost are directly related to a photoreceptor's ability to transmit information (Figures 5 and 6); the higher a photoreceptor's maximum bit rate, the higher the dark cost, the higher the signalling cost, and the higher the total cost per bit.


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

Niven JE, Anderson JC, Laughlin SB - PLoS Biol. (2007)

The Scaling of Metabolic Cost with Performance in Dipteran R1–6 PhotoreceptorsThe logarithms of the total cost (open symbols) and the fixed cost (solid symbols) are plotted against the logarithm of maximum information rate. Costs are in ATP molecules hydrolysed per photoreceptor per second. Each data point represents the mean values from R1–6 photoreceptors in one of the four dipteran species used in this study. The linear fits suggest that the total cost of photoreceptor signalling (dashed line) increases as (information rate)1.7, and the fixed cost of maintaining the photoreceptor in the dark (solid line) increases as (information rate)1.47.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1828148&req=5

pbio-0050116-g007: The Scaling of Metabolic Cost with Performance in Dipteran R1–6 PhotoreceptorsThe logarithms of the total cost (open symbols) and the fixed cost (solid symbols) are plotted against the logarithm of maximum information rate. Costs are in ATP molecules hydrolysed per photoreceptor per second. Each data point represents the mean values from R1–6 photoreceptors in one of the four dipteran species used in this study. The linear fits suggest that the total cost of photoreceptor signalling (dashed line) increases as (information rate)1.7, and the fixed cost of maintaining the photoreceptor in the dark (solid line) increases as (information rate)1.47.
Mentions: The information rates measured with our brightest stimuli are indicative of a photoreceptor's maximum performance. Comparing metabolic costs with these highest rates, we see that both the total cost and the dark cost increase supralinearly with performance. Plots of the logarithms of costs against the logarithms of highest rates (Figure 7) suggest that the total cost increases as (performance)1.7, and the dark cost increases close to (performance)1.5, but with only four species these exponents are preliminary estimates. Nonetheless, there is no doubt that both the unit cost of information (the total cost per bit) and the dark cost are directly related to a photoreceptor's ability to transmit information (Figures 5 and 6); the higher a photoreceptor's maximum bit rate, the higher the dark cost, the higher the signalling cost, and the higher the total cost per bit.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom.

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.

Show MeSH