Biosonar spatial resolution along the distance axis: revisiting the clutter interference zone

ABSTRACT Many echolocating bats forage close to vegetation – a chaotic arrangement of prey and foliage where multiple targets are positioned behind one another. Bats excel at determining distance: they measure the delay between the outgoing call and the returning echo. In their auditory cortex, delay-sensitive neurons form a topographic map, suggesting that bats can resolve echoes of multiple targets along the distance axis – a skill crucial for the forage-amongst-foliage scenario. We tested this hypothesis combining an auditory virtual reality with formal psychophysics: we simulated a prey item embedded in two foliage elements, one in front of and one behind the prey. The simulated spacing between ‘prey’ (target) and ‘foliage’ (maskers) was defined by the inter-masker delay (IMD). We trained Phyllostomus discolor bats to detect the target in the presence of the maskers, systematically varying both loudness and spacing of the maskers. We show that target detection is impaired when maskers are closely spaced (IMD<1 ms), but remarkably improves when the spacing is increased: the release from masking is approximately 5 dB for intermediate IMDs (1–3 ms) and increases to over 15 dB for large IMDs (≥9 ms). These results are comparable to those from earlier work on the clutter interference zone of bats (Simmons et al., 1988). They suggest that prey would enjoy considerable acoustic protection from closely spaced foliage, but also that the range resolution of bats would let them ‘peek into gaps’. Our study puts target ranging into a meaningful context and highlights the limitations of computational topographic maps. Summary: Echolocating bats perceive absolute distance to objects by measuring the time delay between call and echo. In addition, they possess spatial resolution along the distance axis.

[1]  J. H. Casseday,et al.  Timing in the auditory system of the bat. , 1999, Annual review of physiology.

[2]  C. Moss,et al.  Adaptive vocal behavior drives perception by echolocation in bats , 2011, Current Opinion in Neurobiology.

[3]  Lutz Wiegrebe,et al.  Sonar beam dynamics in leaf-nosed bats , 2016, Scientific Reports.

[4]  H. Schnitzler,et al.  Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection , 1993, Behavioral Ecology and Sociobiology.

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

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

[7]  D. Mershon,et al.  Intensity and reverberation as factors in the auditory perception of egocentric distance , 1975 .

[8]  N. Qian Binocular Disparity and the Perception of Depth , 1997, Neuron.

[9]  H. Schnitzler,et al.  Echolocation signals reflect niche differentiation in five sympatric congeneric bat species , 2004, Nature.

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

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

[12]  Herbert Peremans,et al.  Echo-acoustic flow dynamically modifies the cortical map of target range in bats , 2014, Nature Communications.

[13]  Pavel Zahorik,et al.  Loudness constancy with varying sound source distance , 2001, Nature Neuroscience.

[14]  Ian P. Howard,et al.  Binocular Vision and Stereopsis , 1996 .

[15]  E Covey,et al.  Monaural interaction of excitation and inhibition in the medial superior olive of the mustached bat: an adaptation for biosonar. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

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

[17]  Hans-Ulrich Schnitzler,et al.  Spatial unmasking in the echolocating Big Brown Bat, Eptesicus fuscus , 2009, Journal of Comparative Physiology A.

[18]  L. Carney,et al.  Near-Field Discrimination of Sound Source Distance in the Rabbit , 2015, Journal of the Association for Research in Otolaryngology.

[19]  Ralph Simon,et al.  Bats Actively Use Leaves as Specular Reflectors to Detect Acoustically Camouflaged Prey , 2019, Current Biology.

[20]  J. H. Casseday,et al.  The monaural nuclei of the lateral lemniscus in an echolocating bat: parallel pathways for analyzing temporal features of sound , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  U. Firzlaff,et al.  Representation of three-dimensional space in the auditory cortex of the echolocating bat P. discolor , 2017, PloS one.

[22]  Evolution: How Bat Biosonar Bests Prey Camouflage , 2019, Current Biology.

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

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

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

[26]  J A Simmons,et al.  Clutter interference along the target range axis in the echolocating bat, Eptesicus fuscus. , 1988, The Journal of the Acoustical Society of America.

[27]  N. Suga,et al.  Acuity in ranging based on delay-tuned combination-sensitive neurons in the auditory cortex of mustached bats , 2017, Hearing Research.

[28]  Casper J. Erkelens,et al.  A computational model of depth perception based on headcentric disparity , 1998, Vision Research.

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

[30]  Brian B. Bishop,et al.  Acoustic recordings in human ear canals to sounds at different locations , 2010, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[31]  James A Simmons,et al.  Spatial release from simultaneous echo masking in bat sonar. , 2014, The Journal of the Acoustical Society of America.

[32]  B Rogers,et al.  Motion Parallax as an Independent Cue for Depth Perception , 1979, Perception.

[33]  Gerald Westheimer The resolving power of the eye , 2005, Vision Research.

[34]  D. M. Green,et al.  Signal detection theory and psychophysics , 1966 .

[35]  Tammo Houtgast,et al.  Auditory distance perception in rooms , 1999, Nature.