CoChat
Sign Up
Cited by 1,056Neuroscience and Neuropharmacology ResearchNeurobiology and Insect Physiology ResearchPhysiological and biochemical adaptations

Energy limitation as a selective pressure on the evolution of sensory systems

Open access
Niven, Jeremy E., Laughlin, Simon B.·2008·Journal of Experimental Biology
DOI 10.1242/jeb.017574
Open this paper in CoChat — free accountOpen PDF

Abstract

Evolution of animal morphology, physiology and behaviour is shaped by the selective pressures to which they are subject. Some selective pressures act to increase the benefits accrued whilst others act to reduce the costs incurred, affecting the cost/benefit ratio. Selective pressures therefore produce a trade-off between costs and benefits that ultimately influences the fitness of the whole organism. The nervous system has a unique position as the interface between morphology, physiology and behaviour; the final output of the nervous system is the behaviour of the animal, which is a product of both its morphology and physiology. The nervous system is under selective pressure to generate adaptive behaviour, but at the same time is subject to costs related to the amount of energy that it consumes. Characterising this trade-off between costs and benefits is essential to understanding the evolution of nervous systems, including our own. Within the nervous system, sensory systems are the most amenable to analysing costs and benefits, not only because their function can be more readily defined than that of many central brain regions and their benefits quantified in terms of their performance, but also because recent studies of sensory systems have begun to directly assess their energetic costs. Our review focuses on the visual system in particular, although the principles we discuss are equally applicable throughout the nervous system. Examples are taken from a wide range of sensory modalities in both vertebrates and invertebrates. We aim to place the studies we review into an evolutionary framework. We combine experimentally determined measures of energy consumption from whole retinas of rabbits and flies with intracellular measurements of energy consumption from single fly photoreceptors and recently constructed energy budgets for neural processing in rats to assess the contributions of various components to neuronal energy consumption. Taken together, these studies emphasize the high costs of maintaining neurons at rest and whilst signalling. A substantial proportion of neuronal energy consumption is related to the movements of ions across the neuronal cell membrane through ion channels, though other processes such as vesicle loading and transmitter recycling also consume energy. Many of the energetic costs within neurons are linked to 3Na(+)/2K(+) ATPase activity, which consumes energy to pump Na(+) and K(+) ions across the cell membrane and is essential for the maintenance of the resting potential and its restoration following signalling. Furthermore, recent studies in fly photoreceptors show that energetic costs can be related, via basic biophysical relationships, to their function. These findings emphasize that neurons are subject to a law of diminishing returns that severely penalizes excess functional capacity with increased energetic costs. The high energetic costs associated with neural tissue favour energy efficient coding and wiring schemes, which have been found in numerous sensory systems. We discuss the role of these efficient schemes in reducing the costs of information processing. Assessing evidence from a wide range of vertebrate and invertebrate examples, we show that reducing energy expenditure can account for many of the morphological features of sensory systems and has played a key role in their evolution.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1242/jeb.017574

Cites

151 of 151 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Given the extremely high costs of building and maintaining nervous systems, neutral evolutionary processes are arguably less prevalent during nervous system evolution than for example in genome evolution.

    “Given the extremely high costs of building and maintaining nervous systems [10–12], neutral evolutionary processes are arguably less prevalent during nervous system evolution than for example in genome evolution [13].”

    From Origin and early evolution of neural circuits for the control of ciliary locomotion (2011) · cites this paper as [11]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. Barlow, H. B. (1961). Possible principles underlying the transformation of sensory messages. In Sensory Communication (ed. W. A. Rosenblith), pp. 217-234. Cambridge, MA: MIT Press.
  2. G. J. Siegel, B.W. Agranoff, R. W. Albers, S. K. Fisher and M. D. Uhler), pp. 637-669. Philadelphia: Lippincott-Raven.
  3. Hölldobler, B. and Wilson, E. O. (1990). The Ants. Cambridge, MA: Harvard University Press.

Cited by

Sorted by citations

Related

Authors
Niven, J. E., & Laughlin, S. B.
Affiliations
  • Smithsonian Tropical Research Institute (PA)
  • University of Cambridge (GB)
Corresponding author
Niven, Jeremy E.
ORCID
Venue
Journal of Experimental Biology
Publisher
The Company of Biologists
Published
2008-06-01
Volume
211
Issue
11
Pages
1792-1804
ISSN
  • 0022-0949 (ISSN-L)
  • 1477-9145
DOI
10.1242/jeb.017574
OpenAlex
W1986098213
Cited by
1,056
References
151
Citations by year
2026: 54 · 2025: 72 · 2024: 74 · 2023: 63 · 2022: 74 · 2021: 78 · 2020: 83 · 2019: 79 · 2018: 54 · 2017: 62 · 2016: 63 · 2015: 57 · 2014: 52 · 2013: 59 · 2012: 46
FWCI
2.36
Type
journal article
Language
en
Open access
Locations
  • Journal of Experimental Biology (publishedVersion)
  • PubMed (publishedVersion)
  • HighWire Press Open Archive (submittedVersion)
  • Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
Funders
  • Royal Society
  • Smithsonian Tropical Research Institute
  • Biotechnology and Biological Sciences Research Council
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Keywords
sensory system evolution, cost-benefit trade-off, visual system, Na+/K+-ATPase, energy balance, nervous system evolution, vesicle recycling, information processing
MeSH terms
Animals, Brain, Diptera, Energy Metabolism, Biological Evolution, Fishes, Mammals, Photoreceptor Cells, Rabbits, Retina, Selection, Genetic, Vision, Ocular, Visual Perception

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review