Investigations of the development of auditory form and function have, with a few exceptions, thus far been largely restricted to birds and mammals, making it difficult to postulate evolutionary hypotheses. Teleost fishes represent useful models for developmental investigations of the auditory system due to their often extensive period of posthatching development and the diversity of auditory specializations in this group. Using the auditory brainstem response and morphological techniques we investigated the development of auditory form and function in zebrafish (Danio rerio) ranging in size from 10 to 45 mm total length. We found no difference in auditory sensitivity, response latency, or response amplitude with development, but we did find an expansion of maximum detectable frequency from 200 Hz at 10 mm to 4000 Hz at 45 mm TL. The expansion of frequency range coincided with the development of Weberian ossicles in zebrafish, suggesting that changes in hearing ability in this species are driven more by development of auxiliary specializations than by the ear itself. We propose a model for the development of zebrafish hearing wherein the Weberian ossicles gradually increase the range of frequencies available to the inner ear, much as middle ear development increases frequency range in mammals.
REFERENCES
1.
Bang
, P. I.
, Sewell
, W. F.
, and Malicki
, J. J.
(2001
). “Morphology and cell type heterogeneities of the inner ear epithelia in adult and juvenile zebrafish (Danio rerio)
,” J. Comp. Neurol.
438
, 173
–190
.2.
Blaxter
, J. H. S.
, and Batty
, R. S.
(1985
). “The development of startle responses in herring larvae
,” J. Mar. Biol. Assoc. U.K.
65
, 737
–750
.3.
Boatwright-Horowitz
, S. S.
, and Megela Simmons
, A.
(1995
). “Postmetamorphic changes in auditory sensitivity of the bullfrog midbrain
,” J. Comp. Physiol., A
177
, 577
–590
.4.
Boatwright-Horowitz
, S. S.
, and Megela Simmons
, A.
(1997
). “Transient ‘deafness’ accompanies auditory development during metamorphosis from tadpole to frog
,” Proc. Natl. Acad. Sci. U.S.A.
94
, 14877
–14882
.5.
Brittan-Powell
, E. F.
, and Dooling
, R. J.
(2000
). “Development of auditory sensitivity in budgerigars
,” J. Acoust. Soc. Am.
107
, 2785
.6.
Chang
, J. S. Y.
, Popper
, A. N.
, and Saidel
, W. M.
(1992
). “Heterogeneity of sensory hair cells in a fish ear
,” J. Comp. Neurol.
324
, 621
–640
.7.
Corwin
, J. T.
(1981
). “Postembryonic production and aging of inner ear hair cells in sharks
,” J. Comp. Neurol.
201
, 541
–553
.8.
Corwin
, J. T.
(1983
). “Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity
,” J. Comp. Neurol.
217
, 345
–356
.9.
Corwin
, J. T.
, Bullock
, T. H.
, and Schweitzer
, J.
(1982
). “The auditory brain stem response in five vertebrate classes
,” Electroencephalogr. Clin. Neurophysiol.
54
, 629
–641
.10.
Dingerkus
, G.
, and Uhler
, L. D.
(1977
). “Enzyme clearing of alcian blue stained whole small vertebrates for demonstration of cartilage
,” Stain Technol.
52
, 229
–232
.11.
Dmitrieva
, L. P.
, and Gottlieb
, G.
(1992
). “Development of brainstem auditory pathway in mallard duck embryos and hatchlings
,” J. Comp. Physiol., A
171
, 665
–671
.12.
Ehret
, G.
, and Romand
, R.
(1981
). “Postnatal development of absolute auditory thresholds in kittens
,” J. Comp. Physiol. Psychol.
95
, 304
–311
.13.
Fay
, R.
(1978
). “Coding of information in single auditory-nerve fibers of the goldfish
,” J. Acoust. Soc. Am.
63
, 136
–146
.14.
Fay
, R. R.
(2000). “Spectral contrasts underlying auditory stream segregation in goldfish (Carassius auratus),” JARO 01, 120–128.15.
Fay
, R. R.
, and Popper
, A. N.
(1974
). “Acoustic stimulation of the ear of the goldfish (Carassius auratus)
,” J. Exp. Biol.
61
, 243
–260
.16.
Fay
, R. R.
, and Popper
, A. N.
(2000
). “Evolution of hearing in vertebrates: the inner ears and processing
,” Hear. Res.
149
, 1
–10
.17.
Fineran
, J. J.
, and Hastings
, M. C.
(2000
). “A mathematical analysis of the peripheral auditory system mechanics in the goldfish (Carassius auratus)
,” J. Acoust. Soc. Am.
108
, 1308
–1321
.18.
Flock
, Å.
(1965
). “Electron microscopic and electrophysiological studies on the lateral line canal organ
,” Acta Oto-Laryngol., Suppl.
199
, 1
–90
.19.
Fuiman
, L. A.
, Poling
, K. R.
, and Higgs
, D. M.
(1998
). “Quantifying developmental progress for comparative studies of larval fishes
,” Copeia
1998
, 602
–611
.20.
Fuiman
, L. A.
, Smith
, M. E.
, and Malley
, V. N.
(1999
). “Ontogeny of routine swimming speed and startle responses in red drum, with a comparison of responses to acoustic and visual stimuli
,” J. Fish Biol.
55
, 215
–226
.21.
Furukawa
, T.
, and Ishii
, Y.
(1967
). “Neurophysiological studies on hearing in goldfish
,” J. Neurophysiol.
30
, 1377
–1403
.22.
Geal-Dor
, M.
, Freeman
, S.
, Li
, G.
, and Sohmer
, H.
(1993
). “Development of hearing in neonatal rats: air and bone conducted ABR thresholds
,” Hear. Res.
69
, 236
–242
.23.
Grande, T., and Young, B. (Submitted). “Ontogeny of the Weberian apparatus in the zebrafish Danio rerio (Ostariophysi, Cypriniformes),” Can J. Zool.
24.
Gray
, L.
(1993
). “Developmental changes in chickens’ masked thresholds
,” Dev. Psychobiol.
26
, 447
–457
.25.
Gray
, L.
, and Rubel
, E. W.
(1985
). “Development of absolute thresholds in chickens
,” J. Acoust. Soc. Am.
77
, 1162
–1172
.26.
Haddon
, C.
, and Lewis
, J.
(1996
). “Early ear development in the embryo of the zebrafish, Danio rerio
,” J. Comp. Neurol.
365
, 113
–128
.27.
Hall, J. W. (1992). Handbook of Auditory Evoked Responses (Allyn and Bacon, Boston).
28.
Hawkins
, A. D.
, and Sand
, O.
(1977
). “Directional hearing in the median vertical plane by the cod
,” J. Comp. Physiol. [A]
122
, 1
–8
.29.
Higgs
, D. M.
, Souza
, M. J.
, Wilkins
, H. R.
, Presson
, J. C.
, and Popper
, A. N.
(2002a). “Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio),” JARO 3, 174–184.30.
Higgs
, D. M.
, Souza
, M. J.
, Wilkins
, H. R.
, Presson
, J. C.
, and Popper
, A. N.
(2002b). “Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio) ERRATUM,” JARO 3, 222.31.
Hill
, K. G.
, Cone-Wesson
, B.
, and Liu
, G.-B.
(1998
). “Development of auditory function in the tammar wallaby Macropus eugenii
,” Hear. Res.
117
, 97
–106
.32.
Iwashita
, A.
, Sakamoto
, M.
, Kojima
, T.
, Watanabe
, Y.
, and Soeda
, H.
(1999). “Growth effects on the auditory threshold of Red Sea bream,” Nippon Suisan Gakkaishi 65, 833–838.33.
Kenyon
, T. N.
(1996
). “Ontogenetic changes in the auditory sensitivity of damselfishes (Pomacentridae)
,” J. Comp. Physiol., A
179
, 553
–561
.34.
Kenyon
, T. N.
, Ladich
, F.
, and Yan
, H. Y.
(1998
). “A comparative study of hearing ability in fishes: the auditory brainstem response approach
,” J. Comp. Physiol.
182
, 307
–318
.35.
Klein
, A. J.
(1984
). “Frequency and age-dependent auditory evoked potential thresholds in infants
,” Hear. Res.
16
, 291
–297
.36.
Kuse
, H.
, and Okaniwa
, A.
(1993
). “Postnatal development of the auditory brainstem response (ABR) in beagles
,” Exp. Anim.
42
, 377
–382
.37.
Lanford
, P. J.
, Platt
, C.
, and Popper
, A. N.
(2000
). “Structure and function in the saccule of the goldfish (Carassius auratus): a model of diversity in the non-amniote ear
,” Hear. Res.
143
, 1
–13
.38.
Lombarte
, A.
, and Popper
, A. N.
(1994
). “Quantitative analyses of postembryonic hair cell addition in the otolithic endorgans of the inner ear of the European hake, Merluccius merluccius (Gadiformes, Teleostei)
,” J. Comp. Neurol.
345
, 419
–428
.39.
Lu
, Z.
, and Popper
, A. N.
(2001
). “Neural response directionality correlates of hair cell orientation in a teleost fish
,” J. Comp. Physiol., A
187
, 453
–465
.40.
Mann
, D.
, Higgs
, D.
, Tavolga
, W.
, Souza
, M.
, and Popper
, A. N.
(2001
). “Ultrasound detection by clupeiform fishes
,” J. Acoust. Soc. Am.
109
, 3048
–3054
.41.
Moeng
, R.
, and Popper
, A. N.
(1984
). “Auditory responses of saccular neurons of the catfish, Ictalurus punctatus
,” J. Comp. Physiol.
155
, 615
–624
.42.
Moore
, D. R.
, and Irvine
, I. F.
(1979
). “The development of some peripheral and central auditory responses in the neonatal cat
,” Brain Res.
163
, 49
–59
.43.
Platt
, C.
(1977
). “Hair cell distribution and orientation in goldfish otolith organs
,” J. Comp. Neurol.
172
, 283
–298
.44.
Platt
, C.
(1993
). “Zebrafish inner ear sensory surfaces are similar to those in goldfish
,” Hear. Res.
65
, 133
–140
.45.
Popper
, A. N.
(1971
). “The effects of fish size on auditory capacities of the goldfish
,” J. Aud Res.
XI
, 239
–247
.46.
Popper
, A. N.
, and Hoxter
, B.
(1984
). “Growth of a fish ear: 1. Quantitative analysis of hair cell and ganglion cell proliferation
,” Hear. Res.
15
, 133
–142
.47.
Popper
, A. N.
, Chan
, A. T. H.
, and Clarke
, N. L.
(1973
). “An evaluation of methods for behavioral investigations of teleost audition
,” Behav. Res. Methods Instrum.
5
, 470
–472
.48.
Popper
, A. N.
, Saidel
, W. M.
, and Chang
, J. S. Y.
(1993
). “Two types of sensory hair cell in the saccule of a teleost fish
,” Hear. Res.
64
, 211
–216
.49.
Popper A. N., Rogers P. H., Saidel W. M., and Cox, M. (1988). “The role of the fish ear in sound processing,” in Sensory Biology of Aquatic Animals, edited by J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (Springer-Verlag, New York), pp. 687–710.
50.
Pujol
, R.
, and Marty
, R.
(1970
). “Postnatal maturation in the cochlea of the cat
,” J. Comp. Neurol.
139
, 115
–126
.51.
Riley
, B. B.
, Zhu
, C.
, Janetopoulos
, C.
, and Aufderheide
, K. J.
(1997
). “A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish
,” Dev. Biol.
191
, 191
–201
.52.
Rogers, P. H., and Cox, M. (1988). “Underwater sound as a biological stimulus,” in Sensory Biology of Aquatic Animals, edited by J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (Springer-Verlag, New York), pp. 131–150.
53.
Rogers
, P. H.
, Popper
, A. N.
, Cox
, M.
, and Saidel
, W. M.
(1988
). “Processing of acoustic signals in the auditory system of bony fish
,” J. Acoust. Soc. Am.
83
, 338
–349
.54.
Rubel, E. W. (1978). “Ontogeny of structure and function in the vertebrate auditory system,” in Handbook of Sensory Physiology Vol. IX, edited by M. Jacobson (Springer-Verlag, New York), pp. 135–237.
55.
Saunders
, J. C.
, Relkin
, E. M.
, Rosowski
, J. J.
, and Bahl
, C.
(1983
). “Changes in middle-ear input admittance during postnatal auditory development in chicks
,” Hear. Res.
24
, 227
–235
.56.
Schofner
, W. P.
, and Feng
, A. S.
(1981
). “Post-metamorphic development of the frequency selectivities and sensitivities of the peripheral auditory system of the bullfrog Rana catesbiana
,” J. Neurophysiol.
93
, 181
–196
.57.
Schuijf
, A.
, and Buwalda
, R. J. A.
(1975
). “On the mechanism of directional hearing in cod (Gadus morhua L.)
,” J. Comp. Physiol.
98
, 333
–343
.58.
von Frisch
, K.
(1938
). “The sense of hearing in fish
,” Nature (London)
141
, 8
–11
.59.
Walsh
, E. J.
, McGee
, J.
, and Javel
, E.
(1986a
). “Development of auditory-evoked potentials in the cat. I. Onset of response and development of sensitivity
,” J. Acoust. Soc. Am.
79
, 712
–724
.60.
Walsh
, E. J.
, McGee
, J.
, and Javel
, E.
(1986b
). “Development of auditory-evoked potentials in the cat. II. Wave latencies
,” J. Acoust. Soc. Am.
79
, 725
–744
.61.
Walsh
, E. J.
, McGee
, J.
, and Javel
, E.
(1986c
). “Development of auditory-evoked potentials in the cat. III. Wave amplitudes
,” J. Acoust. Soc. Am.
79
, 745
–754
.62.
Waterman
, R. E.
, and Bell
, D. H.
(1984
). “Epithelial fusion during early semicircular canal formation in the embryonic zebrafish, Danio rerio
,” Anat. Rec.
210
, 101
–114
.63.
Werner, L. A., and Gray, L. (1998). “Behavioral studies of hearing development,” in Development of the Auditory System, edited by E. W. Rubel, A. N. Popper, and R. R. Fay (Springer-Verlag, New York), pp. 12–79.
64.
Wysocki
, L. E.
, and Ladich
, F.
(2001
). “The ontogenetic development of auditory sensitivity, vocalization and acoustic communication in the labyrinth fish Trichopsis vittata
,” J. Comp. Physiol., A
187
, 177
–187
.65.
Yan
, H. Y.
, and Curtsinger
, W. S.
(2000
). “The otic gasbladder as an ancillary auditory structure in a mormyrid fish
,” J. Comp. Physiol., A
186
, 595
–602
.66.
Yan
, H. Y.
, Fine
, M. L.
, Horn
, N. S.
, and Colón
, W. E.
(2000
). “Variability in the role of the gasbladder in fish audition
,” J. Comp. Physiol., A
186
, 435
–445
.67.
Zar, J. H. (1984). Biostatistical Analysis, 2nd ed. (Prentice–Hall, Englewood Cliffs, NJ).
This content is only available via PDF.
© 2003 Acoustical Society of America.
2003
Acoustical Society of America
You do not currently have access to this content.