Echo-Imaging Exploits an Environmental High-Pass Filter to Access Spatial Information with a Non-Spatial Sensor

Summary Echo-imaging evolved as the main remote sense under lightless conditions. It is most precise in the third dimension (depth) rather than in the visually dominating dimensions of azimuth and elevation. We asked how the auditory system accesses spatial information in the dimensions of azimuth and elevation with a sensory apparatus that is fundamentally different from vision. We quantified echo-acoustic parameters of surface-wave patterns with impulse-response recordings and quantified bats' perceptual sensitivity to such patterns with formal psychophysics. We demonstrate that the spectro-temporal auditory representation of a wave pattern implicitly encodes its spatial frequency. We further show that bats are much more sensitive to wave patterns of high spatial frequencies than of low spatial frequencies. We conclude that echo-imaging accesses spatial information by exploiting an inherent environmental high-pass filter for spatial frequency. The functional similarities yet mechanistic differences between visual and auditory system signify convergent evolution of spatial-information processing.

[1]  J. Simmons Echolocation in Bats: Signal Processing of Echoes for Target Range , 1971, Science.

[2]  L. Rayleigh,et al.  XII. On our perception of sound direction , 1907 .

[3]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[4]  N Suga,et al.  Target range-sensitive neurons in the auditory cortex of the mustache bat. , 1979, Science.

[5]  Manfred Kössl,et al.  Chronotopically organized target-distance map in the auditory cortex of the short-tailed fruit bat. , 2010, Journal of neurophysiology.

[6]  E. Kalko,et al.  Perception of silent and motionless prey on vegetation by echolocation in the gleaning bat Micronycteris microtis , 2013, Proceedings of the Royal Society B: Biological Sciences.

[7]  J. Altringham,et al.  The distribution of Daubenton's bats (Myotis daubentonii) and pipistrelle bats (Pipistrellus pipistrellus) (Vespertilionidae) in relation to small-scale variation in riverine habitat , 2000 .

[8]  R. Barclay,et al.  Bat activity over calm and turbulent water , 1987 .

[9]  Louis W. Gellermann Chance Orders of Alternating Stimuli in Visual Discrimination Experiments , 1933 .

[10]  S. Zeki Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[11]  S. Radtke-Schuller,et al.  The auditory cortex of the bat Phyllostomus discolor: Localization and organization of basic response properties , 2008, BMC Neuroscience.

[12]  H. Peremans,et al.  What Noseleaves Do for FM Bats Depends on Their Degree of Sensorial Specialization , 2010, PloS one.

[13]  L. Miller,et al.  Echolocation constraints of Daubenton’s Bat foraging over water , 1999 .

[14]  R. Nowak Walker's bats of the world , 1994 .

[15]  Uwe Firzlaff,et al.  The Sonar Aperture and Its Neural Representation in Bats , 2011, The Journal of Neuroscience.

[16]  L. Wiegrebe,et al.  Flutter sensitivity in FM bats. Part II: amplitude modulation , 2018, Journal of Comparative Physiology A.

[17]  H. Bleckmann,et al.  Sensory ecology of a semi-aquatic spider (Dolomedes triton) , 1984, Behavioral Ecology and Sociobiology.

[18]  R. Barclay,et al.  The infl1uence of physical clutter and noise on the activity of bats over water , 1989 .

[19]  A. Grinnell,et al.  Echolocation and foraging behavior of the lesser bulldog bat, Noctilio albiventris : preadaptations for piscivory? , 1998, Behavioral Ecology and Sociobiology.

[20]  M. Ruedi,et al.  Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. , 2001, Molecular phylogenetics and evolution.

[21]  H. Schnitzler,et al.  The acoustic advantage of hunting at low heights above water: behavioural experiments on the European 'trawling' bats Myotis capaccinii, M. dasycneme and M. daubentonii. , 2001, The Journal of experimental biology.

[22]  M. Bar Visual objects in context , 2004, Nature Reviews Neuroscience.

[23]  M. Murakami,et al.  Effect of emergent aquatic insects on bat foraging in a riparian forest. , 2006, The Journal of animal ecology.

[24]  E. Kalko,et al.  Activity Pattern of the Trawling Phyllostomid Bat, Macrophyllum macrophyllum, in Panamá 1 , 2005 .

[25]  Hans-Ulrich Schnitzler,et al.  Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats , 2013, Front. Physiol..

[26]  R. Patterson,et al.  Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform. , 1995, The Journal of the Acoustical Society of America.

[27]  L. Wiegrebe,et al.  Flutter sensitivity in FM bats. Part I: delay modulation , 2018, Journal of Comparative Physiology A.

[28]  J. Simmons The resolution of target range by echolocating bats. , 1973, The Journal of the Acoustical Society of America.

[29]  Victor Klymenko,et al.  Spatial frequency differences can determine figure-ground organization. , 1986, Journal of experimental psychology. Human perception and performance.

[30]  F. Bretschneider,et al.  Prey detection in trawling insectivorous bats: duckweed affects hunting behaviour in Daubenton's bat, Myotis daubentonii , 1998, Behavioral Ecology and Sociobiology.

[31]  B. Siemers,et al.  Trawling bats exploit an echo-acoustic ground effect , 2013, Front. Physiol..

[32]  H. Schnitzler,et al.  The echolocation and hunting behavior of Daubenton's bat, Myotis daubentoni , 1989, Behavioral Ecology and Sociobiology.

[33]  H. Bleckmann Perception of water surface waves: how surface waves are used for prey identification, prey localization, and intraspecific communication , 1985 .

[34]  Lutz Wiegrebe,et al.  An autocorrelation model of bat sonar , 2008, Biological Cybernetics.

[35]  D. Griffin Listening in the dark: The acoustic orientation of bats and men. , 1958 .

[36]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[37]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.