Echolocating bats rely on audiovocal feedback to adapt sonar signal design

Significance Echolocating animals are well known for their capability to extract rich information about the environment from echo returns. However, past research has not determined whether audiovocal feedback contributes to sonar call design. Audiovocal feedback is the process whereby an animal listens to the sounds it is producing and is used by both nonecholocating animals and humans to control their ongoing vocalizations. Here, we show that echolocating bats rely on audiovocal feedback, instead of echo feedback, to adapt their sonar call design in response to acoustic jamming signals. Our findings demonstrate that bats, like birds and humans, not only use audiovocal feedback to fine-tune the features of their calls, but also do so on a rapid timescale. Many species of bat emit acoustic signals and use information carried by echoes reflecting from nearby objects to navigate and forage. It is widely documented that echolocating bats adjust the features of sonar calls in response to echo feedback; however, it remains unknown whether audiovocal feedback contributes to sonar call design. Audiovocal feedback refers to the monitoring of one’s own vocalizations during call production and has been intensively studied in nonecholocating animals. Audiovocal feedback not only is a necessary component of vocal learning but also guides the control of the spectro-temporal structure of vocalizations. Here, we show that audiovocal feedback is directly involved in the echolocating bat’s control of sonar call features. As big brown bats tracked targets from a stationary position, we played acoustic jamming signals, simulating calls of another bat, timed to selectively perturb audiovocal feedback or echo feedback. We found that the bats exhibited the largest call-frequency adjustments when the jamming signals occurred during vocal production. By contrast, bats did not show sonar call-frequency adjustments when the jamming signals coincided with the arrival of target echoes. Furthermore, bats rapidly adapted sonar call design in the first vocalization following the jamming signal, revealing a response latency in the range of 66 to 94 ms. Thus, bats, like songbirds and humans, rely on audiovocal feedback to structure sonar signal design.

[1]  Jinhong Luo,et al.  Sensorimotor integration on a rapid time scale , 2017, Proceedings of the National Academy of Sciences.

[2]  Uwe Firzlaff,et al.  The Lombard effect emerges early in young bats: implications for the development of audio-vocal integration , 2017, Journal of Experimental Biology.

[3]  Melville J. Wohlgemuth,et al.  Three-dimensional auditory localization in the echolocating bat , 2016, Current Opinion in Neurobiology.

[4]  Hans-Ulrich Schnitzler,et al.  No evidence for spectral jamming avoidance in echolocation behavior of foraging pipistrelle bats , 2016, Scientific Reports.

[5]  I. Matsuo,et al.  Echolocating Big Brown Bats, Eptesicus fuscus, Modulate Pulse Intervals to Overcome Range Ambiguity in Cluttered Surroundings , 2016, Front. Behav. Neurosci..

[6]  Henrik Brumm,et al.  Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise , 2015, Scientific Reports.

[7]  Lutz Wiegrebe,et al.  Fast sensory–motor reactions in echolocating bats to sudden changes during the final buzz and prey intercept , 2015, Proceedings of the National Academy of Sciences.

[8]  Arjan Boonman,et al.  On-board recordings reveal no jamming avoidance in wild bats , 2015, Proceedings of the Royal Society B: Biological Sciences.

[9]  Hiroshi Riquimaroux,et al.  Adaptive changes in echolocation sounds by Pipistrellus abramus in response to artificial jamming sounds , 2014, Journal of Experimental Biology.

[10]  B. Siemers,et al.  Global warming alters sound transmission: differential impact on the prey detection ability of echolocating bats , 2014, Journal of The Royal Society Interface.

[11]  Michael Smotherman,et al.  Groups of bats improve sonar efficiency through mutual suppression of pulse emissions , 2013, Front. Physiol..

[12]  Jiang Feng,et al.  Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats , 2013, Proceedings of the National Academy of Sciences.

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

[14]  Hanjun Liu,et al.  Time-dependent Neural Processing of Auditory Feedback during Voice Pitch Error Detection , 2011, Journal of Cognitive Neuroscience.

[15]  Feng Rong,et al.  Sensorimotor Integration in Speech Processing: Computational Basis and Neural Organization , 2011, Neuron.

[16]  Hiroshi Riquimaroux,et al.  FM echolocating bats shift frequencies to avoid broadcast–echo ambiguity in clutter , 2010, Proceedings of the National Academy of Sciences.

[17]  C. Moss,et al.  Adaptive echolocation behavior in bats for the analysis of auditory scenes , 2009, Journal of Experimental Biology.

[18]  S. Sober,et al.  Adult birdsong is actively maintained by error correction , 2009, Nature Neuroscience.

[19]  C. Moss,et al.  Flying in silence: Echolocating bats cease vocalizing to avoid sonar jamming , 2008, Proceedings of the National Academy of Sciences.

[20]  N. Ulanovsky,et al.  What the bat's voice tells the bat's brain , 2008, Proceedings of the National Academy of Sciences.

[21]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

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

[23]  F. Guenther,et al.  Neural mechanisms underlying sensory feedback control of speech , 2007 .

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

[25]  C. Larson,et al.  Voice F0 responses to pitch-shifted voice feedback during English speech. , 2007, The Journal of the Acoustical Society of America.

[26]  Shiva R. Sinha,et al.  Vocal Premotor Activity in the Superior Colliculus , 2007, The Journal of Neuroscience.

[27]  Jay J Bauer,et al.  Vocal responses to unanticipated perturbations in voice loudness feedback: an automatic mechanism for stabilizing voice amplitude. , 2006, The Journal of the Acoustical Society of America.

[28]  John F. Houde,et al.  Compensatory responses to brief perturbations of speech amplitude , 2005 .

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

[30]  Michael Smotherman,et al.  Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency. , 2002, The Journal of experimental biology.

[31]  T C Hain,et al.  Effects of delayed auditory feedback (DAF) on the pitch-shift reflex. , 2001, The Journal of the Acoustical Society of America.

[32]  Michael S. Brainard,et al.  Auditory feedback in learning and maintenance of vocal behaviour , 2000, Nature Reviews Neuroscience.

[33]  C. Larson,et al.  Voice F0 responses to manipulations in pitch feedback. , 1998, The Journal of the Acoustical Society of America.

[34]  G. Neuweiler Auditory adaptations for prey capture in echolocating bats. , 1990, Physiological reviews.

[35]  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.

[36]  J. Habersetzer,et al.  Adaptive echolocation sounds in the batRhinopoma hardwickei , 1981, Journal of comparative physiology.

[37]  W. A. Lavender,et al.  Echolocation by free-tailed bats (Tadarida) , 1978, Journal of comparative physiology.

[38]  N. Suga,et al.  Neurophysiological studies on echolocation systems in awake bats producing CF-FM orientation sounds. , 1974, The Journal of experimental biology.

[39]  H. Schnitzler,et al.  Die Ultraschall-Ortungslaute der Hufeisen-Fledermäuse (Chiroptera-Rhinolophidae) in verschiedenen Orientierungssituationen , 1968, Zeitschrift für vergleichende Physiologie.

[40]  J. J. G. McCue,et al.  The resistance of bats to jamming , 1963 .

[41]  Bernard S. Lee Effects of delayed speech feedback , 1950 .

[42]  D. Griffin ECHOLOCATION BY BLIND MEN, BATS AND RADAR. , 1944, Science.

[43]  C. Larson,et al.  Human laryngeal responses to auditory stimulation. , 1983, The Journal of the Acoustical Society of America.

[44]  H. Schnitzler,et al.  Die Ultraschallortungslaute der Hufeisen-Fledermause (Chiroptera-Rhinolophidae) in vershiedenen Orientierungssituationen , 1968 .

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