FM echolocating bats shift frequencies to avoid broadcast–echo ambiguity in clutter

Sonar broadcasts are followed by echoes at different delays from objects at different distances. When broadcasts are emitted rapidly in cluttered surroundings, echo streams from successive broadcasts overlap and cause ambiguity in matching echoes to corresponding broadcasts. To identify reactions to ambiguity in clutter, echolocating bats that emit multiple-harmonic FM sounds were trained to fly into a dense, extended array of obstacles (multiple rows of vertically hanging chains) while the sonar sounds the bat emitted were recorded with a miniature radio microphone carried by the bat. Flight paths were reconstructed from thermal-infrared video recordings. Successive rows of chains extended more than 6 m in depth, so each broadcast was followed by a series of echoes from multiple rows of chains that lasted up to 40 ms. Bats emitted sounds in pairs (“strobe groups”) at short (20–40 ms) interpulse intervals (IPIs) alternating with longer IPIs (>50 ms). For many short IPIs, the stream of echoes from the first broadcast was still arriving when the second broadcast was emitted. This overlap caused ambiguity about matching echoes with broadcasts. Bats shifted frequencies of the first sound in each strobe group upward and the second sound downward by 3–6 kHz. When overlap and ambiguity ceased, frequency shifts ceased also. Frequency differences were small compared with the total broadcast band, which was 75–80 kHz wide, but the harmonic structure of echoes enhances the differences in spectrograms. Bats could use time–frequency comparisons of echoes with broadcasts to assign echoes to the corresponding broadcasts and thus avoid ambiguity.

[1]  James A Simmons,et al.  Target representation of naturalistic echolocation sequences in single unit responses from the inferior colliculus of big brown bats. , 2005, The Journal of the Acoustical Society of America.

[2]  James A. Simmons,et al.  A possible neuronal basis for representation of acoustic scenes in auditory cortex of the big brown bat , 1993, Nature.

[3]  N. Suga,et al.  Encoding of target range and its representation in the auditory cortex of the mustached bat , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Nobuo Suga,et al.  Neural mechanisms of ranging are different in two species of bats , 1989, Hearing Research.

[5]  Donald Wong,et al.  The influence of stimulus duration on the delay tuning of cortical neurons in the FM bat, Myotis lucifugus , 1992, Journal of Comparative Physiology A.

[6]  R. Lindsay,et al.  Listening in the Dark , 1958 .

[7]  C. Moss,et al.  Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. , 2000, The Journal of the Acoustical Society of America.

[8]  D. Griffin,et al.  TARGET DISCRIMINATION BY THE ECHOLOCATION OF BATS. , 1965, The Journal of experimental zoology.

[9]  J. Ostwald,et al.  Discrimination of two-wavefront echoes by the big brown bat, Eptesicus fuscus: behavioral experiments and receiver simulations , 1993, Journal of Comparative Physiology A.

[10]  C. Schreiner,et al.  Time course of forward masking tuning curves in cat primary auditory cortex. , 1997, Journal of neurophysiology.

[11]  W G Paschal,et al.  Frequency organization of delay-sensitive neurons in the auditory cortex of the FM bat, Myotis lucifugus. , 1994, Journal of neurophysiology.

[12]  Cynthia F. Moss,et al.  Behavioral Studies of Auditory Information Processing , 1995 .

[13]  J A Simmons,et al.  Neural responses to overlapping FM sounds in the inferior colliculus of echolocating bats. , 2000, Journal of neurophysiology.

[14]  J. Simmons,et al.  Interpulse interval modulation by echolocating big brown bats (Eptesicus fuscus) in different densities of obstacle clutter , 2009, Journal of Comparative Physiology A.

[15]  P. Jen,et al.  Analysis of orientation signals emitted by the CF-FM bat,Pteronotus p. parnellii and the FM bat,Eptesicus fuscus during avoidance of moving and stationary obstacles , 1982, Journal of comparative physiology.

[16]  E Covey,et al.  A neuroethological theory of the operation of the inferior colliculus. , 1996, Brain, behavior and evolution.

[17]  Cynthia F. Moss,et al.  Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus , 1990, Journal of Comparative Physiology A.

[18]  T. Imig,et al.  Cortical synthesis of azimuth-sensitive single-unit responses with nonmonotonic level tuning: a thalamocortical comparison in the cat. , 1996, Journal of neurophysiology.

[19]  James A. Simmons,et al.  Auditory Dimensions of Acoustic Images in Echolocation , 1995 .

[20]  H. Riquimaroux,et al.  Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. , 2007, The Journal of the Acoustical Society of America.

[21]  H Peremans,et al.  The spectrogram correlation and transformation receiver, revisited. , 1998, The Journal of the Acoustical Society of America.

[22]  Hiroshi Riquimaroux,et al.  On-board telemetry of emitted sounds from free-flying bats: compensation for velocity and distance stabilizes echo frequency and amplitude , 2008, Journal of Comparative Physiology A.

[23]  J. Simmons,et al.  Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. , 1982, The Journal of the Acoustical Society of America.

[24]  George D. Pollak,et al.  Characteristics of phasic on neurons in inferior colliculus of unanesthetized bats with observations relating to mechanisms for echo ranging , 1977 .

[25]  S. Stevenson,et al.  Clutter interference and the integration time of echoes in the echolocating bat, Eptesicus fuscus. , 1989, The Journal of the Acoustical Society of America.

[26]  Lee A. Miller,et al.  The acoustic behavior of four species of vespertilionid bats studied in the field , 1981, Journal of comparative physiology.

[27]  R. Kuc,et al.  Foliage echoes: a probe into the ecological acoustics of bat echolocation. , 2000, The Journal of the Acoustical Society of America.

[28]  James A Simmons,et al.  Biosonar signals impinging on the target during interception by big brown bats, Eptesicus fuscus. , 2007, The Journal of the Acoustical Society of America.

[29]  James A Simmons,et al.  Jamming avoidance response of big brown bats in target detection , 2008, Journal of Experimental Biology.

[30]  James A. Simmons,et al.  Big brown bats and June beetles: Multiple pursuit strategies in a seasonal acoustic predator–prey system , 2005 .

[31]  Hiroshi Riquimaroux,et al.  Doppler-shift compensation in the Taiwanese leaf-nosed bat (Hipposideros terasensis) recorded with a telemetry microphone system during flight. , 2005, The Journal of the Acoustical Society of America.

[32]  Joan F. Lorden,et al.  An easily constructed carbon fiber recording and microiontophoresis assembly , 1996, Journal of Neuroscience Methods.

[33]  Nobuo Suga,et al.  Corticofugal modulation of the paradoxical latency shifts of inferior collicular neurons. , 2008, Journal of neurophysiology.

[34]  A. Feng,et al.  Echo detection and target-ranging neurons in the auditory system of the bat Eptesicus fuscus. , 1978, Science.

[35]  S. Shamma,et al.  Organization of response areas in ferret primary auditory cortex. , 1993, Journal of neurophysiology.

[36]  M Yano,et al.  A model of echolocation of multiple targets in 3D space from a single emission. , 2001, The Journal of the Acoustical Society of America.

[37]  James A Simmons,et al.  Selectivity for echo spectral interference and delay in the auditory cortex of the big brown bat Eptesicus fuscus. , 2002, Journal of neurophysiology.

[38]  C F Moss,et al.  Auditory scene analysis by echolocation in bats. , 2001, The Journal of the Acoustical Society of America.

[39]  C. Moss,et al.  Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus , 2009, Journal of Experimental Biology.

[40]  N Suga,et al.  Delay-tuned neurons in the midbrain of the big brown bat. , 1995, Journal of neurophysiology.

[41]  J A Simmons,et al.  A computational model of echo processing and acoustic imaging in frequency-modulated echolocating bats: the spectrogram correlation and transformation receiver. , 1993, The Journal of the Acoustical Society of America.

[42]  Matthias O. Franz,et al.  Plant Classification from Bat-Like Echolocation Signals , 2008, PLoS Comput. Biol..

[43]  John H. Casseday,et al.  Mechanisms for Analysis of Auditory Temporal Patterns in the Brainstem of Echolocating Bats , 1995 .

[44]  C. Moss,et al.  The sonar beam pattern of a flying bat as it tracks tethered insects. , 2003, The Journal of the Acoustical Society of America.

[45]  J. Habersetzer,et al.  Discrimination of surface-structured targets by the echolocating batMyotis myotis during flight , 1983, Journal of comparative physiology.

[46]  G D Pollak,et al.  Characteristics of phasic on neurons in inferior colliculus of unanesthetized bats with observations relating to mechanisms for echo ranging. , 1976, Journal of neurophysiology.

[47]  H. Schnitzler,et al.  From spatial orientation to food acquisition in echolocating bats , 2003 .

[48]  W. A. Lavender,et al.  Target Structure and Echo Spectral Discrimination by Echolocating Bats , 1974, Science.

[49]  D. Hartley,et al.  The sound emission pattern of the echolocating bat, Eptesicus fuscus , 1989 .

[50]  S Schmidt,et al.  Perception of structured phantom targets in the echolocating bat, Megaderma lyra. , 1992, The Journal of the Acoustical Society of America.

[51]  C F Moss,et al.  Echo-delay resolution in sonar images of the big brown bat, Eptesicus fuscus. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[52]  N. Suga,et al.  Facilitatory and inhibitory frequency tuning of combination-sensitive neurons in the primary auditory cortex of mustached bats. , 1999, Journal of neurophysiology.

[53]  N Suga,et al.  Specialized subsystems for processing biologically important complex sounds: cross-correlation analysis for ranging in the bat's brain. , 1990, Cold Spring Harbor symposia on quantitative biology.

[54]  J. A. Simmons,et al.  Frequency tuning, latencies, and responses to frequency-modulated sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus , 1997, Journal of Comparative Physiology A.

[55]  James A. Simmons,et al.  Role of broadcast harmonics in echo delay perception by big brown bats , 2008, Journal of Comparative Physiology A.

[56]  Henry E. Heffner,et al.  Audiogram of the big brown bat (Eptesicus fuscus) , 1997, Hearing Research.

[57]  C. Schreiner,et al.  Sequence sensitivity of neurons in cat primary auditory cortex. , 2000, Cerebral cortex.

[58]  N. Ulanovsky,et al.  Dynamics of jamming avoidance in echolocating bats , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[59]  J. Simmons,et al.  Spatially dependent acoustic cues generated by the external ear of the big brown bat, Eptesicus fuscus. , 1995, The Journal of the Acoustical Society of America.

[60]  George D. Pollak,et al.  Time and frequency domain processing in the inferior colliculus of echolocating bats , 1981, Hearing Research.

[61]  Nachum Ulanovsky,et al.  Rapid jamming avoidance in biosonar , 2007, Proceedings of the Royal Society B: Biological Sciences.

[62]  Ellen Covey,et al.  The biology of bats , 2000 .

[63]  James A. Simmons,et al.  Versatility of biosonar in the big brown bat, Eptesicus fuscus , 2001 .