Abstract
Echolocation comprises an animal sending out signals and listening for the echoes bouncing off objects in the environment. Given the ease of recording outgoing clicks and cries, more information is known about the outgoing signals than what animals hear of the echoes. Loud outgoing signals produce pronounced echoes but also create problems for hearing when the animal immediately attempts to listen for the quiet returning echoes. Recent work measuring hearing with auditory evoked potentials has allowed a new look at what animals hear while they echolocate. Hearing sensation changes due to middle ear muscle contractions during bat vocalization production protect the auditory system from overstimulation and allow better echo hearing. Whale and dolphin hearing sensation levels also change to maximize the hearing of echoes but may operate differently. A number of mechanisms come into play to maximize hearing during echolocation.
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References
Au, W. W. L. (1980). Echolocation signals in open waters. In R. G. Busnel & J. F. Fish (Eds.), Animal sonar systems (pp. 251–282). New York: Plenum Press.
Au, W. W. L. (1993). The sonar of dolphins. New York: Springer-Verlag.
Au, W. W. L., & Benoit-Bird, K. J. (2003). Automatic gain control in the echolocation system of dolphins. Nature, 423, 861–863.
Aubauer, R., Au, W. W. L., Nachtigall, P. E., Pawloski, D. A., & DeLong, C. M. (2000). Classification of an electronically generated phantom target by an Atlantic bottlenose dolphin (Tursiops truncatus). Journal of the Acoustical Society of America, 107, 2750–2754.
Behrend, O., & Schuller, G. (2000). The central acoustic tract and audio-vocal coupling in the horseshoe bat, Rhinolophus rouxi. European Journal of Neuroscience, 12, 4268–4280.
Busnel, R. G., & Fish, J. F. (1980). Animal sonar systems. New York: Plenum Press.
Chiu, C. H., Xian, W., & Moss, C. F. (2008). Flying in silence: Echolocating bats cease vocalizing to avoid sonar jamming. Proceedings of the National Academy of Sciences of the USA, 105(35), 13116–13121.
Chiu, C., Xian, W., & Moss, C. F. (2009). Adaptive echolocation behavior in bats for the analysis of auditory scenes. Journal of Experimental Biology, 212(9), 1392–1404.
Cook, M. L. H., Varcia, R. A., Goldstein, J. D., McCullock, S. D., Bossart, G. D., Finneran, J. J., Houser, D., & Mann, D. (2006). Beaked whale auditory evoked potential hearing measurements. Journal of Comparative Physiology A, 192, 489–495.
Crapse, T. B., & Sommer, M. A. (2009). Corollary discharge across the animal kingdom. Nature Reviews in Neurosciences, 9, 587–600.
Dear, S. P., & Suga, N. (1995). Delay-tuned neurons in the midbrain of the big brown bat. Neurophysiology, 73(3), 1084–1100.
Dear, S. P., Fritz, J., Haresign, T., Ferragamo, M., & Simmons, J. A. (1993). Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus. Journal of Neurophysiology, 70(5), 1988–2009.
Dolphin, W. F., Au, W. W. L., Nachtigall, P. E., & Pawloski J. L. (1995). Modulation rate transfer functions to low frequency carriers by three species of cetaceans. Journal of Comparative Physiology A, 177, 235–245.
Dubrovskiy, N. A. (1990). On the two auditory systems in dolphins. In J. Thomas & R. Kastelein (Eds.), Sensory abilities of cetaceans: Laboratory and field evidence (pp. 233–254). New York: Plenum Press.
Finneran, J. J., Schlundt, C. E., Branstetter, B., & Dear, R. L. (2007). Assessing temporary threshold shift in a bottlenose dolphin (Tursiops truncatus) using multiple simultaneous auditory evoked potentials. Journal of the Acoustical Society of America, 122, 1249–1264.
Fritz, J. B., Elhilali, M., David, S. V., & Shamma, S. A. (2007). Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in AI? Hearing Research, 229, 186–203
Gaese, B. H., & Ostwald, J. (2001). Anesthesia changes frequency tuning of neurons in the rat primary auditory cortex. Journal of Neurophysiology, 86, 1062–1066.
Gillam, E. H., Ulanovsky, N., & McCracken, G. F. (2007). Rapid jamming avoidance in biosonar. Proceedings of the Royal Society B: Biological Sciences, 274, 651–660.
Gregg, J. D., Dudzinski, K. M., & Smith H. V. (2007). Do dolphins eavesdrop on the echolocation signals of conspecifics? International Journal of Comparative Psychology, 20, 65–88.
Griffin, D. R. (1958). Listening in the dark. New Haven CT: Yale University Press.
Henson, O. W. (1965). The activity and function of the middle ear muscles in echolocating bats. Journal of Physiology, 180, 871–887.
Henson, O. W., Pollak, G. D., Kobler, J. B., Henson, M. M., & Goldman, L. J. (1982). Cochlear microphonic potentials elicited by biosonar signals in flying bats, Pteronotus p parnellii. Hearing Research, 7, 127–147.
Herbert, H., Aschoff, A., & Ostwald, J. (1991). Topography of projections from the auditory cortex to the inferior colliculus in the rat. Journal of Comparative Neurology, 304(1), 103–122.
Hoffmann, S., & Firzlaff, U. (2009). Vocalization influences neural processing of acoustic echoes. In 5th Animal Sonar Symposium, September 14 –18, 2009 Doshisha University, Kyoto, Japan.
Houser, D. S., & Finneran, J. J. (2006a). A comparison of underwater hearing sensitivity in bottlenose dolphins (Tursiops truncatus) determined by electrophysiological and behavioral methods. Journal of the Acoustical Society of America, 120, 1713–1722.
Houser, D. S., & Finneran, J. J. (2006b). Variation in the hearing sensitivity of a dolphin population determined through the use of evoked potential audiometry. Journal of the Acoustical Society of America, 120, 4090–4099.
Huffman, R. F., & Henson, O. W., Jr. (1990). The descending auditory pathway and acousticomotor systems: Connections with the inferior colliculus. Brain Research Review, 15(3), 295–323.
Kamminga, C., & Wiersma, H. (1981). Investigations on cetacean sonar II. Acoustical Similarities and differences in odontocete sonar signals. Aquatic Mammals, 8, 41–62.
Kawasaki, M., Margoliash, D., & Suga, N. (1988). Delay-tuned combination-sensitive neurons in the auditory cortex of the vocalizing mustached bat. Journal of Neurophysiology, 59, 623–635.
Ketten, D. R. (2000). Cetacean ears. In W. W. L. Au, A. N. Popper, & R. R. Fay (Eds), Hearing by whales and dolphins (pp. 43–108). New York: Springer-Verlag.
Kick, S. A., & Simmons, J. A. (1984). Automatic gain control in the bat’s sonar receiver and the neuroethology of echolocation. Journal of Neuroscience, 4(11), 2725–2737.
Li, S., Nachtigall, P. E., & Breese, M. (2011). Dolphin echolocation: Evoked potential responses in an Atlantic bottlenose dolphin (Tursiops truncatus). The Journal of Experimental Biology, 214, 2027–2035.
Li, S., Nachtigall, P. E., & Breese, M. (2012). Auditory brain stem responses associated with echolocation in an Atlantic bottlenose dolphin (Tursiops truncatus) In A. N. Popper & A. Hawkins (Eds.), The effects of noise on aquatic life (pp. 45–47). New York: Springer Science+Business Media.
Linnenschmidt, M., Beedholm, K., Wahlberg, M., Hojer-Kristensen, J., & Nachtigall, P. E. (2012). Keeping returns optimal: Gain control exerted through sensitivity adjustments in the harbour porpoise auditory system. Proceedings of the Royal Society of London B: Biological Sciences, 279, 2237–2245.
Ma, X., & Suga, N. (2009). Specific and nonspecific plasticity of the primary auditory cortex elicited by thalamic auditory neurons. Journal of Neuroscience, 29(15), 4888–4896.
Madsen, P. T., Wahlberg, M., & Møhl, B. (2002). Male sperm whale (Physeter macrocephalus) acoustics in a high-latitude habitat: Implications for echolocation and communication. Behavioral Ecology and Sociobiology, 53, 31–41.
Madsen, P. T., Johnson, M., Aguilar de Soto, N., Zimmer, W. M. X., & Tyack, P. (2005). Biosonar performance of foraging beaked whales (Mesoplodon densirostris). Journal of Experimental Biology, 208, 181–194.
Mittmann, D., & Wenstrup, J. J. (1995). Combination-sensitive neurons in the inferior colliculus. Hearing Research, 90(1–2), 185–191.
Møhl, B., Wahlberg, M., Madsen, P. T., Heerfordt, A., & Lund, A. (2003). The monopulsed nature of sperm whale clicks. Journal of the Acoustical Society of America, 114, 1143–1154.
Mooney, T. A., Nachtigall, P. E., Taylor, K. A., Rasmussen, M., & Miller, L. (2009). Auditory temporal resolution of a wild white-beaked dolphin (Lagenorhynchus albirostris). Journal of Comparative Physiology A, 195, 375–384.
Moore, P. W. B., Hall, R. W., Friedl, W. A., & Nachtigall, P. E.(1984). The critical interval in dolphin echolocation: What is it? Journal of the Acoustical Society of America, 76, 314–317.
Nachtigall, P. E., & Moore, P. W. B. (1988). Animal sonar: Processes and performance. New York: Plenum Press.
Nachtigall, P. E., Yuen, M. E., Mooney, T. A., & Taylor, K. A. (2005). Hearing measurements from a stranded infant Risso’s dolphin (Grampus griseus). Journal of Experimental Biology, 208, 4181–4188.
Nachtigall, P. E., Mooney, T. A., Taylor, K. A., & Yuen, M. L. (2007a). Hearing and auditory evoked potential methods applied to odontocete cetaceans. Aquatic Mammals, 33(1), 6–13.
Nachtigall, P. E., Supin, A. Y., Amundin, M., Röken, B., Møller, T., Mooney, T. A., Taylor, K. A., & Yuen, M. E. (2007b). Polar bear (Ursus maritimus) hearing measured with auditory evoked potentials. Journal of Experimental Biology, 210, 1116–1122.
Nachtigall, P.E. and Supin, A. Ya. (2013) False killer whales reduce their hearing sensitivity if a loud sound is preceded by a warning. Journal of Experimental Biology, 216, 3062–3070
Nelson, P. C., Smith, Z. M., & Young, E. D. (2009). Wide-dynamic-range forward suppression in marmoset inferior colliculus neurons is generated centrally and accounts for perceptual masking. Journal of Neuroscience, 29(8), 2553–2562.
Neumann, I., & Schuller, G. (1991). Spectral and temporal gating mechanisms enhance the clutter rejection in the echolocating bat, Rhinolophus rouxi. Journal of Comparative Physiology A, 169(1), 109–116.
Neuweiler, G., Metzner, W., Heilmann, U., Rübsamen, R., Eckrich, M., & Costa, H. H. (1987). Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Journal of Behavioral Ecology and Sociobiology, 20, 53–67.
Olsen, J. F., & Suga, N. (1991). Combination-sensitive neurons in the medial geniculate body of the mustached bat: Encoding of target range information. Journal of Neurophysiology, 65(6), 1275–1296.
O’Neill, W. E., & Suga, N. (1982). Encoding of target range and its representation in the auditory cortex of the mustached bat. Journal of Neuroscience, 2(1), 17–31.
Pacini, A. F., Nachtigall, P. E., Quintos, C., Schofield, D., Look, D. A., Levine, G., & Turner, J. (2011). Audiogram of a stranded Blainville’s beaked whale (Mesoplodon densirostris) measured using auditory evoked potentials. Journal of Experimental Biology, 214, 2409–2415.
Pecka, M., Zahn, T. P., Saunier-Rebori, B., Siveke, I., Felmy, F., Wiegrebe, L., Klug, A., Pollak, G. D., & Grothe, B. (2007). Inhibiting the inhibition: A neuronal network for sound localization in reverberant environments. Journal of Neuroscience, 27(7), 1782–1790.
Peremans, H., & Hallam, J. (1998). The spectrogram correlation and transformation receiver, revisited. Journal of the Acoustical Society of America, 104(2), 1101–1110.
Pietsch, G., & Schuller, G. (1987). Auditory self-stimulation by vocalization in the CF-FM bat, Rhinolophus rouxi. Journal of Comparative Physiology A, 160, 635–644.
Popov, V. V., Supin, A. Ya., Pletenko, M. G., Tarakanov, M. B., Klishin, V. O., Bulgakavo, T. N., & Rosanova, E. I. (2007). Audiogram variability in normal bottlenose dolphins (Tursiops truncatus). Aquatic Mammals, 33, 14–24.
Prechtl, H. (1995). Senso-motorische Wechselwirkung im auditorischen Mittelhirn der Hufeisennasen-Fledermaus, Rhinolophus rouxi. Doctoral dissertation, University of Munich, Germany.
Rasmussen, M. H., Miller, L. A., & Au, W. W. L. (2002). Source levels of clicks from free-ranging white beaked dolphins (Lagenorhinchus albirostris Gray 1846) recorded in Icelandic waters. Journal of the Acoustical Society of America, 111, 1122–1125.
Ridgway, S. H., & McCormick, J. G. (1967). Anesthetization of porpoises for major surgery. Science, 158, 510–512.
Ridgway, S. H., & Carder, D. A. (2001). Assessing hearing and sound production in cetacean not available for behavior audiograms: Experiences with sperm, pygmy sperm, and gray whales. Aquatic Mammals, 27(3), 267–276.
Saillant, P. A., Simmons, J. A., Dear, S. P., & McMullen, T. A. (1993). A computational model of echo processing and acoustic imaging in frequency-modulated echolocating bats: The spectrogram correlation and transformation receiver. Journal of the Acoustical Society of America, 94(5), 2691–2712.
Schregardus, D. S., Pieneman, A. W., Ter Maat, A., Jansen, R. F., Brouwer, T. G. F., & Gahr, M. L. (2006). A lightweight telemetry system for recording neuronal activity in freely behaving small animals. Journal of Neuroscience Methods, 155(1), 62–71.
Schuller, G. (1979). Vocalization influences auditory processing in collicular neurons of the CF-FM bat, Rhinolophus ferrumequinum. Journal of Comparative Physiology A, 132, 39–46.
Schuller, G., & Pollack, G. (1979). Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats: Evidence for an acoustic fovea. Journal of Comparative Physiology A, 132(1), 47–54.
Schuller, G., & Radtke-Schuller, S. (1988). Midbrain areas as candidates for audio-vocal interface in echolocating bats. In P. E. Nachtigall & P. W. B. Moore (Eds.), Animal sonar: Processes and performance. New York: Plenum Press.
Schuller, G., & Radtke-Schuller, S. (1990). Neural control of vocalization in bats: Mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Experimental Brain Research , 79(1), 192–206.
Schuller, G., O’Neill, W. E. & Radtke-Schuller, S. (1991) Facilitation and delay sensitivity of auditory cortex neurons in CF-FM bats, Rhinolophus rouxi and Pteronotus p. parnellii. European Journal of Neuroscience, 3, 1165–1181.
Stimpert, A. K., Wiley, D. N., Au, W. W. L., Johnson, M. P., & Arsenault, R. (2007). Megaclicks: Acoustic click trains and buzzes produced during nighttime foraging of humpback whales (Megaptera novaeangliae). Biological Letters, 3, 467–470.
Suga, N. (2008). Role of corticofugal feedback in hearing. Journal of Comparative Physiology A, 194, 169–183.
Suga, N., & Schlegel, P. (1972). Neural attenuation of responses to emitted sounds in echolocating bats. Science, 177, 82–84.
Suga, N., & Shimozawa, T. (1974). Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science, 183, 1211–1212.
Suga, N., & Jen, P. H. S. (1975). Peripheral control of acoustic signals in the auditory system of echolocating bats. Journal of Experimental Biology, 62, 277–311.
Supin, A. Ya., & Popov, V. V. (1995a). Envelope-following response and modulation rate transfer function in the dolphin’s auditory system. Hearing Research, 92, 38–45.
Supin, A. Ya., & Popov, V. V. (1995b). Temporal resolution in the dolphin’s auditory system revealed by double-click evoked potential study. Journal of the Acoustical Society of America, 97, 2586–2593.
Supin, A. Ya. , Popov, V. V., & Mass, A. M. (2001). The sensory physiology of aquatic mammals. Boston: Kluwer Academic.
Supin, A. Ya., Nachtigall, P. E., & Pawloski, J. L. (2003). Evoked potential recording during echolocation in a false killer whale (Pseudorca crassidens). Journal of the Acoustical Society of America, 113(5), 2408–2411.
Supin, A. Ya., Nachtigall, P. E., Au, W. W. L., & Breese, M. (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale’s auditory system: Evoked potential study. Journal of the Acoustical Society of America, 115(6), 3218–3225.
Supin, A. Ya., Nachtigall, P. E., Au, W. W. L., & Breese, M. (2005). Invariance of echo-responses to target strength and distance in an echolocating false killer whale: Evoked potential study. Journal of the Acoustical Society of America, 117(6), 3928–3935.
Supin, A. Ya., Nachtigall, P. E., & Breese, M. (2006). Source to sensation level ratio of transmitted biosonar pulses in an echolocating false killer whale. Journal of the Acoustical Society of America, 120, 518–526.
Supin, A. Ya., Nachtigall, P. E., & Breese, M. (2007). Evoked-potential recovery during double click stimulation in a whale: A possibility of biosonar automatic gain control. Journal of the Acoustical Society of America, 121, 618–625.
Supin, A. Ya., Nachtigall, P. E., & Breese, M. (2008). Hearing sensitivity during target presence and absence while a whale echolocates. Journal of the Acoustical Society of America, 123, 534–541.
Thomas, J. A., Moss, C. F., & Vater, M. (2004). Echolocation in bats and dolphins. Chicago: University of Chicago Press.
Ulanovsky, N., & Moss, C. F. (2007). Hippocampal cellular and network activity in freely moving echolocating bats. Nature Neuroscience, 10, 224–233.
Ulanovsky, N., Fenton, M. B., Tsoar, A., & Korine, C. (2004). Dynamics of jamming avoidance in echolocating bats. Proceedings of the Royal Society of London B: Biological Sciences, 27, 1467–1475.
Wartzog, D., & Ketten, D. R. (1999). Marine mammal sensory systems. In J. E. Reynolds III & S. A. Rommel (Eds.), Biology of marine mammals. Washington, DC: Smithsonian Institution Press.
Wever, E. G., & Vernon, J. A. (1961). The protective mechanism of the bat’s ear. Annals of Otology, Rhinology and Laryngology, 70(1), 5–17.
Wiegrebe, L. (2008). An autocorrelation model of bat sonar. Biological Cybernetics, 98, 587–595.
Yuen, M. E., Nachtigall, P. E., Supin, A. Ya., & Breese, M. (2005). Behavioral and auditory evoked potential audiograms of a false killer whale (Pseudorca crassidens). Journal of the Acoustical Society of America, 118 (4), 2688–2695.
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Nachtigall, P.E., Schuller, G. (2014). Hearing During Echolocation in Whales and Bats. In: Surlykke, A., Nachtigall, P., Fay, R., Popper, A. (eds) Biosonar. Springer Handbook of Auditory Research, vol 51. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9146-0_5
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