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      Energy-Information Trade-Offs between Movement and Sensing

      1 , 2 , 3 , * , 1 , 4

      PLoS Computational Biology

      Public Library of Science

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          While there is accumulating evidence for the importance of the metabolic cost of information in sensory systems, how these costs are traded-off with movement when sensing is closely linked to movement is poorly understood. For example, if an animal needs to search a given amount of space beyond the range of its vision system, is it better to evolve a higher acuity visual system, or evolve a body movement system that can more rapidly move the body over that space? How is this trade-off dependent upon the three-dimensional shape of the field of sensory sensitivity (hereafter, sensorium)? How is it dependent upon sensorium mobility, either through rotation of the sensorium via muscles at the base of the sense organ (e.g., eye or pinna muscles) or neck rotation, or by whole body movement through space? Here we show that in an aquatic model system, the electric fish, a choice to swim in a more inefficient manner during prey search results in a higher prey encounter rate due to better sensory performance. The increase in prey encounter rate more than counterbalances the additional energy expended in swimming inefficiently. The reduction of swimming efficiency for improved sensing arises because positioning the sensory receptor surface to scan more space per unit time results in an increase in the area of the body pushing through the fluid, increasing wasteful body drag forces. We show that the improvement in sensory performance that occurs with the costly repositioning of the body depends upon having an elongated sensorium shape. Finally, we show that if the fish was able to reorient their sensorium independent of body movement, as fish with movable eyes can, there would be significant energy savings. This provides insight into the ubiquity of sensory organ mobility in animal design. This study exposes important links between the morphology of the sensorium, sensorium mobility, and behavioral strategy for maximally extracting energy from the environment. An “infomechanical” approach to complex behavior helps to elucidate how animals distribute functions across sensory systems and movement systems with their diverse energy loads.

          Author Summary

          Animals thrive by sensing their environment and using the information they've gathered to guide their movement. But collecting better information can result in less efficient movement: Bicycling while standing up on the pedals may help you see over obstacles ahead of you, but it causes more air drag, forcing your legs to work harder. Nocturnal weakly electric fish search for prey with their body tilted. This tilting more than doubles the resistance to movement from the water, but because the fish's ability to sense prey improves when tilted, it is better to swim this way. Beyond a certain amount of tilt, the costs of movement become too great. Interestingly, the benefit of tilting is dependent on the shape of the volume around the fish where it detects prey. We also found that if the fish was able to swivel its region of prey sensitivity, like a vision-based animal can shift its gaze, it would save energy. This conclusion helps us understand why animals like us can move our eyes. A Polish folk saying succinctly captures the gist: “He who doesn't have it in the head has it in the legs” (Ten kto nie ma w głowie ma w nogach).

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          Most cited references 15

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

          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.
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            A Devonian tetrapod-like fish and the evolution of the tetrapod body plan.

            The relationship of limbed vertebrates (tetrapods) to lobe-finned fish (sarcopterygians) is well established, but the origin of major tetrapod features has remained obscure for lack of fossils that document the sequence of evolutionary changes. Here we report the discovery of a well-preserved species of fossil sarcopterygian fish from the Late Devonian of Arctic Canada that represents an intermediate between fish with fins and tetrapods with limbs, and provides unique insights into how and in what order important tetrapod characters arose. Although the body scales, fin rays, lower jaw and palate are comparable to those in more primitive sarcopterygians, the new species also has a shortened skull roof, a modified ear region, a mobile neck, a functional wrist joint, and other features that presage tetrapod conditions. The morphological features and geological setting of this new animal are suggestive of life in shallow-water, marginal and subaerial habitats.
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              Motion and vision: why animals move their eyes.

              Nearly all animals with good vision have a repertoire of eye movements. The majority show a pattern of stable fixations with fast saccades that shift the direction of gaze. These movements may be made by the eyes themselves, or the head, or in some insects the whole body. The main reason for keeping gaze still during fixations is the need to avoid the blur that results from the long response time of the photoreceptors. Blur begins to degrade the image at a retinal velocity of about 1 receptor acceptance angle per response time. Some insects (e.g. hoverflies) stabilise their gaze much more rigidly than this rule implies, and it is suggested that the need to see the motion of small objects against a background imposes even more stringent conditions on image motion. A third reason for preventing rotational image motion is to prevent contamination of the translational flow-field, by which a moving animal can judge its heading and the distances of objects. Some animals do let their eyes rotate smoothly, and these include some heteropod molluscs, mantis shrimps and jumping spiders, all of which have narrow linear retinae which scan across the surroundings. Hymenopteran insects also rotate during orientation flights at speeds of 100-200 degrees s-1. This is just consistent with a blur-free image, as are the scanning speeds of the animals with linear retinae.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                May 2010
                May 2010
                6 May 2010
                : 6
                : 5
                Affiliations
                [1 ]Department of Mechanical Engineering, Northwestern University, Evanston, Illinois, United States of America
                [2 ]Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois, United States of America
                [3 ]Department of Biomedical Engineering, Northwestern University, Evanston, Illinois, United States of America
                [4 ]Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America
                University College London, United Kingdom
                Author notes

                Conceived and designed the experiments: MAM. Performed the experiments: MAM AAS. Analyzed the data: MAM NAP AAS. Contributed reagents/materials/analysis tools: NAP AAS. Wrote the paper: MAM.

                Article
                10-PLCB-RA-1695R3
                10.1371/journal.pcbi.1000769
                2865506
                20463870
                MacIver et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 12
                Categories
                Research Article
                Computational Biology/Computational Neuroscience
                Evolutionary Biology/Animal Behavior
                Neuroscience/Behavioral Neuroscience
                Neuroscience/Motor Systems
                Neuroscience/Sensory Systems

                Quantitative & Systems biology

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