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      What a Plant Sounds Like: The Statistics of Vegetation Echoes as Received by Echolocating Bats

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          Abstract

          A critical step on the way to understanding a sensory system is the analysis of the input it receives. In this work we examine the statistics of natural complex echoes, focusing on vegetation echoes. Vegetation echoes constitute a major part of the sensory world of more than 800 species of echolocating bats and play an important role in several of their daily tasks. Our statistical analysis is based on a large collection of plant echoes acquired by a biomimetic sonar system. We explore the relation between the physical world (the structure of the plant) and the characteristics of its echo. Finally, we complete the story by analyzing the effect of the sensory processing of both the echolocation and the auditory systems on the echoes and interpret them in the light of information maximization. The echoes of all different plant species we examined share a surprisingly robust pattern that was also reproduced by a simple Poisson model of the spatial reflector arrangement. The fine differences observed between the echoes of different plant species can be explained by the spatial characteristics of the plants. The bat's emitted signal enhances the most informative spatial frequency range where the species-specific information is large. The auditory system filtering affects the echoes in a similar way, thus enhancing the most informative spatial frequency range even more. These findings suggest how the bat's sensory system could have evolved to deal with complex natural echoes.

          Author Summary

          More than 800 species of bats perceive their surroundings through echolocation. They emit ultrasonic pulses and analyze the information conveyed in the echoes returning from objects in their surroundings. This enables bats to orient in space, to acquire food and to perfectly function in complete darkness. In the absence of light, echoes constitute a major part of the sensory world of bats. Understanding their characteristics can thus help to shed light on the echolocation sensory system. The goal of this work is to study the characteristics of natural plant echoes. Plant echoes are very abundant in the world of the bats and are used by them to find food sources and to navigate. We show that some of the features of the echoes can be explained from the physical properties of the plant they were sampled from (e.g., its leaf size and density). We then analyze the effects of the sensory system on the echoes and suggest that they improve the representation of the echoes in a way that enhances the information that is most reliable for the bats.

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          Modelling the power spectra of natural images: statistics and information.

          Power spectra of an extensive set of natural images were analysed. Both the total power in a spectrum (corresponding to image contrast) and its dependence on spatial frequency vary considerably between images, and also within images when considered as functions of orientation. A series of probabilistic models for power spectra enabled calculating the information obtained from prior knowledge of parameters describing spectra. Most information is gained from contrast, 1/f2 spatial frequency behaviour, and contrast as a function of orientation. Variations in spatial frequency behaviour are relatively unimportant. For oriented contrast, a bandwidth of 10-30 deg is sufficient to obtain most information.
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            Natural stimulus statistics alter the receptive field structure of v1 neurons.

            Studies of the primary visual cortex (V1) have produced models that account for neuronal responses to synthetic stimuli such as sinusoidal gratings. Little is known about how these models generalize to activity during natural vision. We recorded neural responses in area V1 of awake macaques to a stimulus with natural spatiotemporal statistics and to a dynamic grating sequence stimulus. We fit nonlinear receptive field models using each of these data sets and compared how well they predicted time-varying responses to a novel natural visual stimulus. On average, the model fit using the natural stimulus predicted natural visual responses more than twice as accurately as the model fit to the synthetic stimulus. The natural vision model produced better predictions in >75% of the neurons studied. This large difference in predictive power suggests that natural spatiotemporal stimulus statistics activate nonlinear response properties in a different manner than the grating stimulus. To characterize this modulation, we compared the temporal and spatial response properties of the model fits. During natural stimulation, temporal responses often showed a stronger late inhibitory component, indicating an effect of nonlinear temporal summation during natural vision. In addition, spatial tuning underwent complex shifts, primarily in the inhibitory, rather than excitatory, elements of the response profile. These differences in late and spatially tuned inhibition accounted fully for the difference in predictive power between the two models. Both the spatial and temporal statistics of the natural stimulus contributed to the modulatory effects.
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              The sonar beam pattern of a flying bat as it tracks tethered insects.

              This paper describes measurements of the sonar beam pattern of flying echolocating bats, Eptesicus fuscus, performing various insect capture tasks in a large laboratory flight room. The beam pattern is deduced using the signal intensity across a linear array of microphones. The positions of the bat and insect prey are obtained by stereoscopic reconstruction from two camera views. Results are reported in the form of beam-pattern plots and estimated direction of the beam axis. The bat centers its beam axis on the selected target with a standard deviation (sigma) of 3 degrees. The experimental error is +/- 1.4 degrees. Trials conducted with two targets show that the bat consistently tracks one of the targets with its beam. These findings suggest that the axis of the bat sonar beam is a good index of selective tracking of targets, and in this respect is analogous to gaze in predominantly visual animals.
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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
                July 2009
                July 2009
                3 July 2009
                : 5
                : 7
                : e1000429
                Affiliations
                [1 ]Animal Physiology Department, University of Tuebingen, Tuebingen, Germany
                [2 ]University of Applied Sciences, Konstanz, Germany
                [3 ]INCM-CNRS UMR, Marseille, France
                University College London, United Kingdom
                Author notes

                Conceived and designed the experiments: YY PS MOF HUS. Performed the experiments: YY PS. Analyzed the data: YY. Contributed reagents/materials/analysis tools: YY PS MOF AB. Wrote the paper: YY.

                Article
                08-PLCB-RA-1185R3
                10.1371/journal.pcbi.1000429
                2699101
                19578430
                19eb65c5-cc4e-4ce0-be6a-8a4e47c3197d
                Yovel 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.
                History
                : 29 December 2008
                : 2 June 2009
                Page count
                Pages: 13
                Categories
                Research Article
                Neuroscience/Sensory Systems

                Quantitative & Systems biology
                Quantitative & Systems biology

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