Passive sound-localization acuity and the ability to use binaural time and intensity cues were determined for the common vampire bat (Desmodus rotundus). The bats were tested using a conditioned suppression/avoidance procedure in which they drank defibrinated blood from a spout in the presence of sounds from their right, but stopped drinking (i.e., broke contact with the spout) whenever a sound came from their left, thereby avoiding a mild shock. The mean minimum audible angle for three bats for a 100-ms noise burst was 13.1°—within the range of thresholds for other bats and near the mean for mammals. Common vampire bats readily localized pure tones of 20 kHz and higher, indicating they could use interaural intensity-differences. They could also localize pure tones of 5 kHz and lower, thereby demonstrating the use of interaural time-differences, despite their very small maximum interaural distance of 60 μs. A comparison of the use of locus cues among mammals suggests several implications for the evolution of sound localization and its underlying anatomical and physiological mechanisms.
References
1.
Barber
, J. R.
, Razak
, K. A.
, and Fuzessery
, Z. M.
(2003
). “Can two streams of auditory information be processed simultaneously? Evidence from the gleaning bat Antrozous pallidus
,” J. Comp. Physiol. A
189
, 843
–855
.2.
Barnard
, S. M.
(1995
). Bats in Captivity
(Wild Ones Animal Books
, Springville, CA
), pp. 77
–94
.3.
Baron
, G.
, Stephan
, H.
, and Frahm
, H. D.
(Eds.) (1996
). Comparative Neurobiology in Chiroptera
(Birkhäuser
, Basel
), Vol. 3
, pp. 1075
–1596
.4.
Bell
, G. P.
, and Fenton
, M. B.
(1986
). “Visual acuity, sensitivity and binocularity in a gleaning insectivorous bat, Macrotus californicus (Chiroptera: Phyllostomidae)
,” Anim. Behav.
34
, 409
–414
.5.
Brand
, A.
, Behrend
, O.
, Marquardt
, T.
, McAlpine
, D.
, and Grothe
, B.
(2002
). “Precise inhibition is essential for microsecond interaural time difference coding
,” Nature
417
, 543
–547
.6.
Bremen
, P.
, and Joris
, P. X.
(2013
). “Axonal recordings from medial superior olive neurons obtained from the lateral lemniscus of the chinchilla (Chinchilla laniger)
,” J. Neurosci.
33
, 17506
–17518
.7.
Christensen-Dalsgaard
, J.
(2005
). “Directional hearing in nonmammalian tetrapods
,” in Sound Source Localization
, edited by A. N.
Popper
and R. R.
Fay
(Springer Science
, New York
), pp. 67
–123
.8.
Covey
, E.
(2005
). “Neurobiological specializations in echolocating bats
,” Anat. Rec. A Discov. Mol. Cell. Evol. Biol.
287
, 1103
–1116
.9.
Ebert
, C. S.
, Blanks
, D. A.
, Patel
, M. R.
, Coffey
, C. S.
, Marshall
, A. F.
, and Fitzpatrick
, D. C.
(2008
). “Behavioral sensitivity to interaural time differences in the rabbit
,” Hear. Res.
235
, 134
–142
.10.
Elfner
, L. F.
, and Tomsic
, R. T.
(1968
). “Temporal and intensive factors in binaural lateralization of auditory transients
,” J. Acoust. Soc. Am.
43
, 746
–751
.11.
Erulkar
, S. D.
(1972
). “Comparative aspects of spatial localization of sound
,” Physiol. Rev.
52
, 236
–360
.12.
Fuzessery
, Z. M.
, Buttenhoff
, P.
, Andrews
, B.
, and Kennedy
, J. M.
(1993
). “Passive sound localization of prey by the Pallid bat (Antrozous p. pallidus)
,” J. Comp. Physiol. A
171
, 767
–777
.13.
Glendenning
, K. K.
, and Masterton
, R. B.
(1998
). “Comparative morphometry of mammalian central auditory systems: Variation in nuclei and form of the ascending system
,” Brain Behav. Evol.
51
, 59
–89
.14.
Grothe
, B.
(2000
). “The evolution of temporal processing in the medial superior olive, an auditory brainstem structure
,” Prog. Neurobiol.
61
, 581
–610
.15.
Grothe
, B.
(2003
). “New roles for synaptic inhibition in sound localization
,” Nat. Rev. Neurosci.
4
, 540
–550
.16.
Grothe
, B.
, Covey
, E.
, and Casseday
, H. H.
(2001
). “Medial superior olive of the Big brown bat: Neuronal responses to pure tones, amplitude modulations, and pulse trains
,” J. Neurophysiol.
86
, 2219
–2230
.17.
Grothe
, B.
, and Neuweiler
, G.
(2000
). “The function of the medial superior olive in small mammals: Temporal receptive fields in auditory analysis
,” J. Comp. Physiol. A
186
, 413
–423
.18.
Grothe
, B.
, and Park
, T. J.
(2000
). “Structure and function of the bat superior olivary complex
,” Microsc. Res. Tech.
51
, 382
–402
.19.
Grothe
, B.
, Pecka
, M.
, and McAlpine
, D.
(2010
). “Mechanisms of sound localization in mammals
,” Physiol. Rev.
90
, 983
–1012
.20.
Heffner
, H. E.
, and Heffner
, R. S.
(1995
). “Conditioned avoidance
,” in Methods in Comparative Psychoacoustics
, edited by G. M.
Klump
, R. J.
Dooling
, R. R.
Fay
, and W. C.
Stebbins
(Birkhäuser
, Basel
), pp. 79
–93
.21.
Heffner
, H. E.
, and Heffner
, R. S.
(2003
). “Audition
,” in Handbook of Research Methods in Experimental Psychology
, edited by S.
Davis
(Blackwell
, Boston, MA
), pp. 413
–440
.43.
Heffner
, H. E.
, and Heffner
, R. S.
(2014
). “The behavioral study of mammalian hearing
,” in Perspectives on Auditory Research
, edited by A. N.
Popper
and R. R.
Fay
(Springer
, New York
), pp. 269
–285
.22.
Heffner
, R. S.
, and Heffner
, H. E.
(1982
). “Hearing in the elephant (Elephas maximus): Absolute sensitivity, frequency discrimination, and sound localization
,” J. Comp. Physiol. Psychol.
96
, 926
–944
.23.
Heffner
, R. S.
, and Heffner
, H. E.
(1986
). “Localization of tones by horses: Use of binaural cues and the role of the superior olivary complex
,” Behav. Neurosci.
100
, 93
–103
.24.
Heffner
, R. S.
, and Heffner
, H. E.
(1987
). “Localization of noise, use of binaural cues, and a description of the superior olivary complex in the smallest carnivore, the Least weasel (Mustela nivalis)
,” Behav. Neurosci.
101
, 701
–708, 744, 745
.25.
Heffner
, R. S.
, and Heffner
, H. E.
(1988
). “Sound localization and use of binaural cues by the gerbil (Meriones unguiculatus)
,” Behav. Neurosci.
102
, 422
–428
.26.
Heffner
, R. S.
, and Heffner
, H. E.
(1989
). “Sound localization, use of binaural cues and the superior olivary complex in pigs
,” Brain Behav. Evol.
33
, 248
–258
.27.
Heffner
, R. S.
, and Heffner
, H. E.
(1990
). “Vestigial hearing in a fossorial mammal, the pocket gopher (Geomys bursarius)
,” Hear. Res.
46
, 239
–252
.28.
Heffner
, R. S.
, and Heffner
, H. E.
(1992a
). “Evolution of sound localization in mammals
,” in The Evolutionary Biology of Hearing
, edited by D. B.
Webster
, R. R.
Fay
, and A. N.
Popper
(Springer
, New York
), pp. 691
–715
.29.
Heffner
, R. S.
, and Heffner
, H. E.
(1992b
). “Hearing and sound localization in Blind mole rats, Spalax ehrenbergi
,” Hear. Res.
62
, 206
–216
.30.
Heffner
, R. S.
, and Heffner
, H. E.
(1992c
). “Visual factors in sound localization in mammals
,” J. Comp. Neurol.
317
, 219
–232
.31.
Heffner
, R. S.
, and Heffner
, H. E.
(1993
). “Degenerate hearing and sound localization in Naked mole rats (Heterocephalus glaber), with an overview of central auditory structures
,” J. Comp. Neurol.
331
, 418
–433
.32.
Heffner
, R. S.
, Heffner
, H. E.
, Kearns
, D.
, Vogel
, J.
, and Koay
, G.
(1994
). “Sound localization in chinchillas, I: Left/right discriminations
,” Hear. Res.
80
, 247
–257
.33.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(1999
). “Sound localization in an Old-world fruit bat (Rousettus aegyptiacus): Acuity, use of binaural cues, and relationship to vision
,” J. Comp. Psychol.
113
, 297
–306
.34.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2001a
). “Audiograms of five species of rodents: Implications for the evolution of hearing and the encoding of pitch
,” Hear. Res.
157
, 138
–152
.35.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2001b
). “Sound-localization acuity changes with age in C5BL/6J mice
,” in The Auditory Biology of the Laboratory Mouse: From Behavior to Molecular Biology
, edited by J.
Willott
(CRC Press
, New York
), pp. 31
–35
.36.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2001c
). “Sound localization in a New-world frugivorous bat, Artibeus jamaicensis: Acuity, use of binaural cues, and relationship to vision
,” J. Acoust. Soc. Am
109
, 412
–421
.37.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2006
). “Hearing in large (Eidolon helvum) and small (Cynopterus brachyotis) non-echolocating fruit bats
,” Hear. Res.
221
, 17
–25
.38.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2007
). “Sound-localization acuity and its relation to vision in large and small fruit-eating bats: I. Echolocating species, Phyllostomus hastatus and Carollia perspicillata
,” Hear. Res.
234
, 1
–9
.39.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2008
). “Sound-localization acuity and its relation to vision in large and small fruit-eating bats: II. Non-echolocating species, Eidolon helvum and Cynopterus brachyotis
,” Hear. Res.
241
, 80
–86
.40.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2010a
). “Use of binaural cues for sound localization in large and small non-echolocating bats: Eidolon helvum and Cynopterus brachyotis
,” J. Acoust. Soc. Am.
127
, 3837
–3845
.41.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2010b
). “Use of binaural cues for sound localization in two species of Phyllostomidae: The Greater spear-nosed bat (Phyllostomus hastatus) and the Short-tailed fruit bat (Carollia perspicillata)
,” J. Comp. Psychol.
124
, 447
–454
.42.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2013
). “Hearing in American leaf-nosed bats. IV: The common vampire bat, Desmodus rotundus
,” Hear. Res.
296
, 42
–50
.44.
Heffner
, R. S.
, Koay
, G.
, and Heffner
, H. E.
(2014
). “Hearing in alpacas (Vicugna pacos): Audiogram, localization acuity, and use of binaural locus cues
,” J. Acoust. Soc. Am.
135
, 778
–788
.45.
Hope
, G. M.
, and Bhatnagar
, K. P.
(1979
). “Electrical response of bat retina to spectral stimulation: Comparison of four microchiropteran species
,” Experientia
35
, 1189
–1191
.46.
Huffman
, R. F.
, and Covey
, E.
(1995
). “Origin of ascending projections to the nuclei of the lateral lemniscus in the Big brown bat, Eptesicus fuscus
,” J. Comp. Neurol.
357
, 532
–545
.47.
Hutson
, K. A.
(2000
). “Auditory brainstem nuclei in a New World fruit bat: Carollia perspicillata
,” Neuroscience Abstracts No. 252.9.48.
Inbody
, S. B.
, and Feng
, A. S.
(1981
). “Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat
,” Brain Res.
210
, 361
–366
.49.
Irvine
, D. R. F.
(1992
). “Physiology of the auditory brainstem
,” in The Mammalian Auditory Pathway: Neurophysiology
, edited by A. N.
Popper
and R. R.
Fay
(Springer
, New York
), pp. 153
–231
.50.
Joris
, P. X.
, and Yin
, T. C.
(1995
). “Envelope coding in the lateral superior olive: I. Sensitivity to interaural time differences
,” J. Neurophysiol.
73
, 1043
–1062
.51.
Kapfer
, C.
, Seidl
, A. H.
, Schweizer
, H.
, and Grothe
, B.
(2002
). “Experience-dependent refinement of inhibitory inputs to auditory coincidence-detector neurons
,” Nat. Neurosci.
5
, 247
–253
.52.
Klumpp
, R. G.
, and Eady
, H. R.
(1956
). “Some measurements of interaural time difference thresholds
,” J. Acoust. Soc. Am.
28
, 859
–860
.53.
Koay
, G.
, Bitter
, K. S.
, Heffner
, H. E.
, and Heffner
, R. S.
(2002a
). “Hearing in American leaf-nosed bats. I: Phyllostomus hastatus
,” Hear. Res.
171
, 96
–102
.54.
Koay
, G.
, Heffner
, R. S.
, and Heffner
, H. E.
(2002b
). “Behavioral audiograms of homozygous medJ mutant mice with sodium channel deficiency and their unaffected littermates
,” Hear. Res.
171
, 111
–118
.55.
Koay
, G.
, Kearns
, D.
, Heffner
, H. E.
, and Heffner
, R. S.
(1998
). “Passive sound localization ability of the Big brown bat (Eptesicus fuscus)
,” Hear. Res.
119
, 37
–48
.73.
Kuhn
, G. F.
(1997
). “Model for the interaural time differences in the azimuthal plane
,” J. Acoust. Soc. Am.
62
, 157
–167
.56.
Kuwabara
, N.
, and Bhatnagar
, K. P.
(1999
). “The superior olivary complex of the vampire bat, Desmodus rotundus (Chiroptera: Phyllostomidae)
,” Acta Chiropterologica
1
, 81
–92
.57.
Manske
, U.
, and Schmidt
, U.
(1976
). “Visual acuity of the vampire bat, Desmodus rotundus, and its dependence upon light intensity
,” Z. Tierpsychol.
42
, 215
–221
.58.
Masterton
, R. B.
, Thompson
, G. C.
, Bechtold
, J. K.
, and RoBards
, M. J.
(1975
). “Neuroanatomical basis of binaural phase-difference analysis for sound localization: A comparative study
,” J. Comp. Physiol. Psychol.
89
, 379
–386
.59.
McFadden
, D.
, and Passanen
, E. G.
(1976
). Lateralization at high frequencies based on interaural time differences. J. Acoust. Soc. Am.
59
, 634
–639
.60.
Mills
, A. W.
(1958
). “On the minimum audible angle
,” J. Acoust. Soc. Am.
30
, 237
–246
.61.
Mills
, A. W.
(1972
). “Auditory localization
,” in Foundations of Modern Auditory Theory
, edited by J. V.
Tobias
(Academic
, New York
), Vol. 2
, pp. 303
–348
.62.
Obrist
, M. K.
, Fenton
, M. B.
, Eger
, J. J.
, and Schlegel
, P. A.
(1993
). “What ears do for bats: A comparative study of pinna sound pressure transformation in Chiroptera
,” J. Exp. Biol.
180
, 119
–152
.63.
Perrott
, D. R.
(1969
). “Role of signal onset in sound localization
,” J. Acoust. Soc. Am.
45
, 436
–445
.64.
Pettigrew
, J. D.
, Dreher
, B.
, Hopkins
, C. S.
, McCall
, M. J.
, and Brown
, M.
(1988
). “Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: Implications for visual acuity
,” Brain, Behav. Evol.
32
, 39
–56
.65.
Plack
, C. J.
(2005
). The Sense of Hearing
(Routledge Press
, Florence, KY
).66.
Schmidt
, U.
(1988
). “Orientation and sensory functions in Desmodus rotundus
,” in Natural History of Vampire Bats
, edited by A. M.
Greenhall
and U.
Schmidt
(CRC
, Boca Raton, FL
), pp. 143
–166
.67.
Schwartz
, I. R.
(1992
). “The superior olivary complex and lateral lemniscal nuclei
,” in The Mammalian Auditory Pathway: Neuroanatomy
, edited by D. B.
Webster
, A. N.
Popper
, and R. R.
Fay
(Springer
, New York
), pp. 117
–167
.68.
Simmons
, J. A.
, and Simmons
, A. M.
(2011
). “Bats and frogs and animals in between: Evidence for a common central timing mechanism to extract periodicity pitch
,” J. Comp. Physiol. A
197
, 585
–594
.69.
Skottun
, B. C.
(1998
). “Sound localization and neurons
,” Nature
393
, 531
.70.
Wesolek
, C. M.
, Koay
, G.
, Heffner
, R. S.
, and Heffner
, H. E.
(2010
). “Laboratory rats (Rattus norvegicus) do not use binaural phase differences to localize sound
,” Hear. Res.
265
, 54
–62
.72.
Zook
, J. M.
, and Casseday
, J. H.
(1980
). “Identification of auditory centers in lower brain stem of two species of echolocating bats: Evidence from injection of horseradish peroxidase into inferior colliculus
,” in Proceedings of the Fifth International Bat Research Conference
, edited by D. E.
Wilson
and A. L.
Gardner
(Texas Tech Press
, Lubbock, TX
), pp. 51
–59
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