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Development of hearing in the big brown bat

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Abstract

We studied the development of hearing in newborn pups of the big brown bat, Eptesicus fuscus. In the majority of pups, the opening of both outer auditory canals occurred on or before postnatal day (PND) 7, but in some, it extended to PND 11. Using repeated auditory brainstem response (ABR) recordings, we tracked the progressive development and maturation of auditory sensitivity in 22 E. fuscus pups every 3 days, from PND 10 to PND 31, with additional recordings in a subset of bats at 2 months, 3 months and 1 year of life. There was a profound increase in auditory sensitivity across development for frequencies between 4 and 100 kHz, with the largest threshold shifts occurring early in development between PND 10 and 19. Prior to PND 13–16 and when pups were still non-volant, most bats were unable to hear frequencies above 48 kHz; however, sensitivity to these higher ultrasonic frequencies increased with age. Notably, this change occurred near the age when young bats started learning how to fly and echolocate.

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Abbreviations

ABR:

Auditory brainstem response

PND:

Postnatal day

References

  • Anthwal N, Thompson H (2016) The development of the mammalian outer and middle ear. J Anat 228:217–232

    PubMed  Google Scholar 

  • Belknap DB, Suthers RA (1982) Brainstem auditory evoked responses to tone bursts in the echolocating bat, Rousettus. J Comp Physiol 146:283–289

    Google Scholar 

  • Blatchley BJ, Cooper WA, Coleman JR (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Dev Brain Res 32:75–84

    Google Scholar 

  • Boku S, Riquimaroux H, Simmons AM, Simmons JA (2015) Auditory brainstem response of the Japanese house bat (Pipistrellus abramus). J Acoust Soc Am 137:1063–1068

    PubMed  Google Scholar 

  • Brandt C, Malmkvist J, Nielsen RL, Brande-Lavridsen N, Surlykke A (2013) Development of vocalization and hearing in American mink (Neovison vison). J Exp Biol 216:3542–3550

    PubMed  Google Scholar 

  • Brown PE, Grinnell AD (1980) Echolocation ontogeny in bats. In: Busnel R-G, Fish JF (eds) Animal sonar systems, NATO Advanced Study Institutes Series, vol 28. Plenum Press, New York, pp 355–377

    Google Scholar 

  • Brown PE, Grinnell AD, Harrison JB (1978) The development of hearing in the pallid bat, Antrozous pallidus. J Comp Physiol 126:169–182

    Google Scholar 

  • Brown PE, Brown TW, Grinnell AD (1983) Echolocation, development, and vocal communication in the lesser bulldog bat, Noctilio albiventris. Behav Ecol Sociobiol 13:287–298

    Google Scholar 

  • Buchler ER (1980) The development of flight, foraging, and echolocation in the little brown bat (Myotis lucifugus). Behav Ecol Sociobiol 6:211–218

    Google Scholar 

  • Burkard R, Moss CF (1994) The brain-stem auditory-evoked response in the big brown bat (Eptesicus fuscus) to clicks and frequency-modulated sweeps. J Acoust Soc Am 96:801–810

    CAS  PubMed  Google Scholar 

  • Carter RT, Adams RA (2014) Ontogeny of the larynx and flight ability in Jamaican fruit bats (Phyllostomidae) with considerations for the evolution of echolocation. Anat Rec 297:1270–1277

    Google Scholar 

  • Carter RT, Adams RA (2015) Postnatal ontogeny of the cochlea and flight ability in Jamaican fruit bats (Phyllostomidae) with implications for the evolution of echolocation. J Anat 226:301–308

    PubMed  PubMed Central  Google Scholar 

  • Carter RT, Adams RA (2016) Integrating ontogeny of echolocation and locomotion gives unique insights into the origin of bats. J Mammal Evo 23:413–421

    Google Scholar 

  • Carter RT, Shaw JB, Adams RA (2014) Ontogeny of vocalization in Jamaican fruit bats with implications for the evolution of echolocation. J Zool 293:25–32

    Google Scholar 

  • Church MW, Williams HL, Holloway JA (1984) Postnatal development of the brainstem auditory evoked potential and far-field cochlear microphonic in non-sedated rat pups. Dev Brain Res 14:23–31

    Google Scholar 

  • Dalland JI (1965) Hearing sensitivity in bats. Science 150:1185–1186

    CAS  PubMed  Google Scholar 

  • Esser K-H, Schmidt U (1990) Behavioral auditory thresholds in neonate lesser spear-nosed bats, Phyllostomus discolor. Naturwissenschaften 77:292–294

    CAS  PubMed  Google Scholar 

  • Fenton MD, Grinnell AD, Popper AN, Fay RR (eds) (2016) Bat bioacoustics. Springer handbook of auditory research, vol 54. Springer, New York

    Google Scholar 

  • Geal-Dor M, Freeman S, Li G, Sohmer H (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hear Res 69:236–242

    CAS  PubMed  Google Scholar 

  • Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W (1988) Auditory brainstem responses to tone bursts in normally hearing subjects. J Speech Hear Res 31:87–97

    CAS  PubMed  Google Scholar 

  • Gould E (1971) Studies of maternal-infant communication and development of vocalizations in the bats Myotis and Eptesicus. Comm Behav Biol 5:263–313

    Google Scholar 

  • Gould E (1975a) Neonatal vocalizations in bats of eight genera. J Mammal 56:15–29

    CAS  PubMed  Google Scholar 

  • Gould E (1975b) Experimental studies of the ontogeny of ultrasonic vocalizations in bats. Dev Psychobiol 8:333–346

    PubMed  Google Scholar 

  • Grinnell AD (1963) The neurophysiology of audition in bats: resistance to interference. J Physiol 167:114–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heffner HE, Heffner RS (2003) Audition. In: Davis S (ed) Handbook of research methods in experimental psychology. Blackwell, Malden, pp 413–440

    Google Scholar 

  • Hörpel SG, Firzlaff U (2020) Post-natal development of the envelope following response to amplitude modulated sounds in the bat Phyllostomus discolor. Hear Res 388:107904

    PubMed  Google Scholar 

  • Jewett DL, Romano MN (1972) Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res 36:101–115

    CAS  PubMed  Google Scholar 

  • Koay G, Heffner HE, Heffner RS (1997) Audiogram of the big brown bat (Eptesicus fuscus). Hear Res 105:202–210

    CAS  PubMed  Google Scholar 

  • Koay G, Heffner RS, Heffner HE (1998) Hearing in a megachiropteran fruit bat (Rousettus aegyptiacus). J Comp Psychol 112:371–382

    CAS  PubMed  Google Scholar 

  • Koay G, Heffner RS, Bitter KS, Heffner HE (2003) Hearing in American leaf-nosed bats. II: Carollia perspicillata. Hear Res 178:27–34

    PubMed  Google Scholar 

  • Konstantinov AI (1973) Development of echolocation in bats in postnatal ontogenesis. Period Biol 75:13–19

    Google Scholar 

  • Kössl M, Foeller E, Drexl M, Vater M, Mora E, Coro F, Russell IJ (2003) Postnatal development of cochlear function in the mustached bat, Pteronotus parnellii. J Neurophysiol 90(4):2261–2273

    PubMed  Google Scholar 

  • Kössl M, Voss C, Mora EC, Macias S, Foeller E, Vater M (2012) Auditory cortex of newborn bats is prewired for echolocation. Nat Comm 3(1):1–7

    Google Scholar 

  • Kraemer A, Baxter C, Hendrix A, Carr CE (2017) Development of auditory sensitivity in the barn owl. J Comp Physiol A 203:843–853

    Google Scholar 

  • Kurta A, Baker RH (1990) Eptesicus fuscus. Mammalian Species 356:1–10

    Google Scholar 

  • Lary S, Briassoulis G, de Vries L, Dubowitz LMS, Dubowitz V (1985) Hearing threshold in preterm and term infants by auditory brainstem response. J Pediatr 107:593–599

    CAS  PubMed  Google Scholar 

  • Linnenschmidt M, Wiegrebe L (2019) Ontogeny of auditory brainstem responses in the bat, Phyllostomus discolor. Hear Res 373:85–95

    PubMed  Google Scholar 

  • Liu Y, Feng J, Jiang YL, Wu L, Sun KP (2007) Vocalization development of greater horseshoe bat, Rhinolophus ferrumequinum (Rhinolophidae, Chiroptera). Folia Zool 56:126–136

    Google Scholar 

  • Mayberry HW, Faure PA (2015) Morphological, olfactory, and vocal development in big brown bats. Biol Open 4:22–34

    Google Scholar 

  • Mayberry HW, Faure PA, Ratcliffe JM (2019) Sonar strobe groups and buzzes are produced before powered flight is achieved in the juvenile big brown bat, Eptesicus fuscus. J Exp Biol 222:jeb209163

    Article  PubMed  Google Scholar 

  • Melcher JR, Kiang NYS (1996) Generators of the brainstem auditory evoked potential in cat III: identified cell populations. Hear Res 93:52–71

    CAS  PubMed  Google Scholar 

  • Monroy JA, Carter ME, Miller KE, Covey E (2011) Development of echolocation and communication vocalizations in the big brown bat, Eptesicus fuscus. J Comp Physiol A 197:459–467

    Google Scholar 

  • Moss CF, Schnitzler H-U (1995) Behavioral studies of auditory information processing. In: Popper AN, Fay RR (eds) Hearing by bats, Springer handbook of auditory research, vol 5. Springer-Verlag, New York, pp 87–145

    Google Scholar 

  • O’Farrell MJ, Studier EH (1973) Reproduction, growth, and development in Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). Ecology 54:18–30

    Google Scholar 

  • Obrist MK, Wenstrup JJ (1998) Hearing and hunting in red bats (Lasiurus borealis, Vespertilionidae): audiogram and ear properties. J Exp Biol 201:143–154

    CAS  PubMed  Google Scholar 

  • Orr RT (1954) Natural history of the pallid bat, Antrozous pallidus (LeConte). Proc Cal Acad Sci 28:165–246

    Google Scholar 

  • Rubel EW (1978) Ontogeny of structure and function in the vertebrate auditory system. In: Jacobson M (ed) Development of sensory systems, Handbook of sensory physiology, vol IX. Springer-Verlag, Berlin, pp 135–237

    Google Scholar 

  • Rübsamen R (1987) Ontogenesis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi (audition and vocalization in early postnatal development). J Comp Physiol A 161:899–913

    PubMed  Google Scholar 

  • Rübsamen R (1992) Postnatal development of central auditory frequency maps. J Comp Physiol A 170:129–143

    PubMed  Google Scholar 

  • Rübsamen R, Neuweiler G, Marimuthu G (1989) Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code. J Comp Physiol A 165(6):755–769

    PubMed  Google Scholar 

  • Schlenther D, Voss C, Kössl M (2014) Influence of ketamine-xylazine anesthesia on cubic and quadratic high-frequency distortion-product otoacoustic emissions. J Assoc Res Otolaryngol 15:695–705

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schweitzer L (1987) Development of brainstem auditory evoked responses in the hamster. Hear Res 25:249–255

    CAS  PubMed  Google Scholar 

  • Shaw NA (1988) The auditory evoked potential in the rat—a review. Progress Neurobiol 31:19–45

    CAS  Google Scholar 

  • Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol 135:61–84

    Google Scholar 

  • Simmons JA, Moss CF, Ferragamo M (1990) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A 166:449–470

    CAS  PubMed  Google Scholar 

  • Simmons AM, Boku S, Riquimaroux H, Simmons JA (2015) Auditory brainstem responses of Japanese house bats (Pipistrellus abramus) after exposure to broadband ultrasonic noise. J Acoust Soc Am 138:2430–2437

    CAS  PubMed  Google Scholar 

  • Skrinyer AJ, Faure PA, Dannemiller S, Ball HC, Delaney KH, Orman R, Stewart M, Cooper LN (2017) Care and husbandry of the world’s only flying mammals. Lab Anim Sci Profession June:24–27

  • Smith DI, Kraus N (1987) Postnatal development of the auditory brainstem response (ABR) in the unanesthetized gerbil. Hear Res 27:157–164

    CAS  PubMed  Google Scholar 

  • Smotherman M, Bakshi K (2019) Forward masking enhances the auditory brainstem response in the free-tailed bat, Tadarida brasiliensis, during a critical time window for sonar reception. J Acoust Soc Am 145(1):EL19–EL24

    Article  PubMed  Google Scholar 

  • Sterbing SJ (2002) Postnatal development of vocalizations and hearing in the phyllostomid bat, Carollia perspicillata. J Mammal 83:516–525

    Google Scholar 

  • Szymanski MD, Bain DE, Kiehl K, Pennington S, Wong S, Henry KR (1999) Killer whale (Orcinus orca) hearing: auditory brainstem response and behavioral audiograms. J Acoust Soc Am 106:1134–1141

    CAS  PubMed  Google Scholar 

  • Thiagavel J, Cechetto C, Santana SE, Jakobsen L, Warrant EJ, Ratcliffe JM (2018) Auditory opportunity and visual constraint enabled the evolution of echolocation in bats. Nat Comm 9(1):1–10

    CAS  Google Scholar 

  • Vater M, Kössl M, Foeller E, Coro F, Mora E, Russell IJ (2003) Development of echolocation calls in the mustached bat, Pteronotus parnellii. J Neurophysiol 90:2274–2290

    CAS  PubMed  Google Scholar 

  • Walsh EJ, McGee J, Javel E (1986) Development of auditory-evoked potentials in the cat. III. Wave amplitudes. J Acoust Soc Am 79:745–754

    CAS  PubMed  Google Scholar 

  • Wang L, Lin A, Xiao Y, Jiang T, Feng J (2014) Postnatal development in the big-footed bat, Myotis macrodactylus: wing morphology, echolocation calls, and flight. Acta Theriol 59:435–441

    Google Scholar 

  • Wang Z, Zhu T, Xue H, Fang N, Zhang J, Zhang L, Pang J, Teeling EC, Zhang S (2017) Prenatal development supports a single origin of laryngeal echolocation in bats. Nat Ecol Evol 1:0021

    Google Scholar 

  • Wenstrup JJ (1984) Auditory sensitivity in the fish-catching bat, Noctilio leporinus. J Comp Physiol A 155:91–101

    Google Scholar 

  • Wetekam J, Reissig C, Hechavarria JC, Kössl M (2020) Auditory brainstem responses in the bat Carollia perspicillata: threshold calculation and relation to audiograms based in otoacoustic emission measurement. J Comp Physiol A 206:95–101

    Google Scholar 

  • Yuen MML, Nachtigall PE, Breese M, Supin AY (2005) Behavioral and auditory evoked potential audiograms of a false killer whale (Pseudorca crassidens). J Acoust Soc Am 118:2688–2695

    PubMed  Google Scholar 

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Acknowledgements

We thank Dr. Kathleen Delaney, Dr. Timothy Ryan, Ms. Dawn Graham, and the staff of the Psychology Animal Facility for veterinary and animal care support. We also thank lab members for help with catching bats and colony care. Research supported by an Operating Grant from the Institute of Neuroscience, Mental Health and Addiction of the Canadian Institutes of Health Research, and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada awarded to PAF. The McMaster Bat Lab is also supported by infrastructure grants from the Canada Foundation for Innovation and the Ontario Innovation Trust.

Funding

This research was supported by Natural Sciences and Engineering Research Council of Canada (Grants RGPIN-2020-06906, RGPIN-2015-4879) and Canadian Institutes of Health Research (Grant 136823)

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Correspondence to Paul A. Faure.

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All experimental procedures were approved by the Animal Research Ethics Board of McMaster University and conformed to the Guide to the Care and Use of Experimental Animals published by the Canadian Council on Animal Care.

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Möckel, D., Groulx, T. & Faure, P.A. Development of hearing in the big brown bat. J Comp Physiol A 207, 27–42 (2021). https://doi.org/10.1007/s00359-020-01452-4

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