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First published online May 19, 2008
Journal of Experimental Biology 211, 1792-1804 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.017574

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

Jeremy E. Niven^1,2,* and Simon B. Laughlin¹

¹ Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
² Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Panamá, República de Panamá

View larger version (7K): [in this window] [in a new window]   Fig. 1. The absence of a correlation between brain size and basal metabolic rate (BMR) in mammals. A plot of the percentage deviation from predicted brain size versus percentage deviation from predicted BMR in mammals reveals no correlation. This suggests that investment in the brain may be traded for other energetically cost tissues. Adapted from Striedter (Striedter, 2005); data from McNab and Eisenberg (McNab and Eisenberg, 1989).

View larger version (11K): [in this window] [in a new window]   Fig. 2. Changes in the blood flow to major organs, the brain and retina in Weddell seals during diving. The normal blood flow (pale blue) and the blood flow during diving (dark blue) to the pancreas and liver, heart, lungs, retina, cerebellum and cortex. There is a substantial reduction in blood flow to the pancreas, liver and heart but not to the lungs, retina, cerebellum and cortex. Adapted from Schmidt-Nielsen (Schmidt-Nielsen, 1998); data from Zapol et al. (Zapol et al., 1979).

View larger version (26K): [in this window] [in a new window]   Fig. 3. Tracheoles supply oxygen to neural tissue in insects. A schematic of the right optic lobe of the desert locust (Schistocerca gregaria) viewed from the posterior surface showing the posterior trachea. This shows the dense ramifications of tracheoles necessary for oxygen supply within insect brains. Adapted from Burrows (Burrows, 1980).

View larger version (22K): [in this window] [in a new window]   Fig. 4. A schematic diagram of a glutamatergic synapse showing many of the major sources of energy consumption. Movements of ions across the neuronal cell membrane account for a large proportion of the energy consumed. During transmission of the action potential along the axon, Na+ and K+ ions move through voltage-gated ion channels due to concentration gradients and potential differences across the membrane. When the action potential reaches a synapse, voltage-gated Ca2+ channels open, to admit Ca2+ ions and trigger the release of vesicles containing glutamate molecules. These glutamate molecules then bind to ligand-gated ion channels, which open admitting Na+ molecules that depolarize the post-synaptic neuron. Glutamate in the synaptic cleft is transported into the presynaptic neuron or nearby glial cells by a glutamate co-transporter. Within the pre-synaptic neuron, glutamate molecules are transported into the synaptic vesicles by a glutamate/H+ anti-porter. Almost all of these processes require the activity of two pumps, the 3Na+/2K+ pump and the H+ V-ATPase.

View larger version (8K): [in this window] [in a new window]   Fig. 5. Resting and maximum energy consumption of photoreceptors scales with their performance. Comparison of four homologous fly R1–6 photoreceptors from (smallest to largest): Drosophila melanogaster, D. virilis, Calliphora vicina and Sarcophaga carnaria. The largest photoreceptors are capable of transmitting more information but expend more energy at rest (squares; solid line) and whilst signalling (circles; broken line) than the smaller photoreceptors. This shows that neural performance is related to energy consumption at rest and whilst signalling. Adapted from Niven et al. (Niven et al., 2007).

View larger version (28K): [in this window] [in a new window]   Fig. 6. Energy budgets break down the energetic costs of neural processing into its constituent components. (A) The energy consumption of the various neuronal components that contribute to the energy consumption of a single action potential (AP) and the events at a glutamateric synapse triggered by it in rat cortex. The AP itself consumes more than 50% of the total energy consumed. Other processes that also consume energy include the activation of NMDA, non-NMDA and metabotropic glutamate post-synaptic receptors, the recycling of glutamate and the entry of presynaptic Ca2+ ions that trigger vesicle release. Many of these processes can be linked to the activity of the sodium–potassium exchanger. (B) The energy consumption of various neural components within a rat olfactory glomerulus with one sniff per second as a function of odour concentration. The contributions of different components change with increasing odour concentration. The resting potential is the dominant cost at low odour concentrations but axonal action potentials, the activation of post-synaptic receptors and dendritic back-propagating action potentials consume substantial amounts of energy at higher concentrations. Adapted from Attwell and Laughlin (Attwell and Laughlin, 2001) and Nawroth et al. (Nawroth et al., 2007).

View larger version (8K): [in this window] [in a new window]   Fig. 7. A trade-off between energy efficiency and information coding in insect photoreceptors. The information rates (bits s–1) versus the energy efficiency of information transmission (ATP molecules bit–1x106) of photoreceptors from four fly species (smallest to largest): Drosophila melanogaster, D. virilis, Calliphora vicina and Sarcophaga carnaria. Larger photoreceptors can transmit higher rates of information but are less energy efficient. Adapted from Niven et al. (Niven et al., 2007).

View larger version (4K): [in this window] [in a new window]   Fig. 8. Ion channels alter the relationship between energy consumption and information coding. Drosophila melanogaster photoreceptors from Shaker mutant flies, which lack functional Shaker K+ channels (red), have an increased energetic cost at rest and whilst signalling when compared to wild-type photoreceptors (black). Adapted from Niven et al. (Niven et al., 2003a).

View larger version (7K): [in this window] [in a new window]   Fig. 9. Reducing energy consumption with distributed coding in spiking neurons. The energy requirements for encoding 1 of 100 conditions initially decrease but subsequently increase as the number of active neurons increases (for cells signalling with spike rates below 60 Hz). As the spike rate increases the region of the parameter space in which distributed coding is advantageous becomes smaller. Adapted from Attwell and Laughlin (Attwell and Laughlin, 2001).

View larger version (39K): [in this window] [in a new window]   Fig. 10. A reduction in the size of visual cortical regions and an expansion in cortical regions associated with mechanosensory processing are associated with subterranean living. (A) The African hedgehog Atelerix albiventris lives above ground and has well developed visual (V) and auditory processing. (B) The star-nosed mole Condylura cristata is subterranean and has reduced visual (V) representation and an enlarged somatosensory representation. Adapted from Catania (Catania, 2005). See text for details.

View larger version (5K): [in this window] [in a new window]   Fig. 11. The relative size of brains and brain regions is not a direct indicator of energy consumption. (A) The average brain mass of elasmobranch fishes (E, blue) weighing between 175 and 1250 g and teleost fishes (T, red) weighing between 222 and 1170 g. (B) The specific activity of the Na+/K+ ATPase (µmol min–1 g–1). (C) The total brain Na+/K+ ATPase activity (µmol min–1). Data from Nilsson et al. (Nilsson et al., 2000).

View larger version (52K): [in this window] [in a new window]   Fig. 12. Reduction of the retina and central regions of the visual system in cave fish. (A) Eye loss in cave populations of Astyanax mexicanus that have been isolated for approximately 1 million years. The photograph shows one eyeless cave fish (foreground) and two fish from closely related surface-dwelling populations. (B) Reduction in the relative size of the brain regions associated with visual processing in fish species living permanently in caves. (i) Amblyopsis spelaea, a fish species living exclusively in caves. (ii) Chologaster agassizi, a fish species occasionally found in caves but also in surface environments. Adapted from Poulson and White (Poulson and White, 1969). Photograph by R. Borowsky, reproduced with permission.

View larger version (7K): [in this window] [in a new window]   Fig. 13. Length of time in culture causes a reduction in eye size in Drosophila melanogaster. Changes in absolute eye size with the number of years in culture. Blue indicates measurements from male flies and red indicates measurements from female flies. Error bars indicate one standard deviation. Adapted from Tan et al. (Tan et al., 2005).