Monitoring auditory brainstem responses (ABRs) is a common method of assessing auditory processing in non-model species. Although ABRs are widely used to compare auditory abilities across taxa, the extent to which different features of acoustic stimuli affect the ABR is largely unknown in most non-mammalian species. The authors investigated the effects of varying presentation rate and onset time to determine how different features of acoustic stimuli influence the ABR in Northern saw-whet owls (Aegolius acadicus), a species known for their unique auditory adaptations and hunting abilities. At presentation rates ranging from 21.1 to 51.1 s−1, there were no differences in the size or synchrony of ABRs, suggesting that stimuli can be presented at a relatively rapid rate to maximize the number of observations recorded for analysis. While increasing onset time was associated with a decrement in response size and synchrony, tonebursts with 1 ms onset times produced overgeneralized neural responses as a result of spectral splatter. This suggests that 2 to 3 ms onset times may balance the trade-off between response synchrony and frequency specificity when comparing relative neural recruitment across frequencies. These findings highlight the importance of considering stimulus parameters when interpreting ABR data.
References
1.
Atcherson
, S. R.
(2012
). “The auditory brainstem response
,” in Auditory Electrophysiology: A Clinical Guide
, edited by S. R.
Atcherson
and T. M.
Stoody
(Thieme Medical Publishers
, New York
), pp. 67
–83
.2.
Atcherson
, S. R.
, and Shoemaker
, S. S.
(2012
). “Fundamental principles of neuroanatomy and neurophysiology related to auditory evoked potentials
,” in Auditory Electrophysiology: A Clinical Guide
, edited by S. R.
Atcherson
and T. M.
Stoody
(Thieme Medical Publishers
, New York
), pp. 41
–55
.3.
Beatini
, J. R.
, Proudfoot
, G. A.
, and Gall
, M. D.
(2018
). “Frequency sensitivity in Northern saw-whet owls (Aegolius acadicus)
,” J. Comp. Physiol. A
204
, 145
–154
.4.
Bibikov
, N. G.
, and Elepfandt
, A.
(2005
). “Auditory evoked potentials from the medulla and midbrain in the clawed frog, Xenopus laevis laevis
,” Hear. Res.
204
, 29
–36
.5.
Boettcher
, F. A.
, White
, D. R.
, Mills
, J. H.
, and Schmiedt
, B. N.
(1995
). “Age-related changes in auditory evoked potentials of gerbils. III. Low frequency responses and repetition rates
,” Hear. Res.
87
, 208
–219
.6.
Brittan-Powell
, E. F.
, Christensen-Dalsgaard
, J.
, Tang
, Y.
, Carr
, C.
, and Dooling
, R. J.
(2010a
). “The auditory brainstem response in two lizard species
,” J. Acoust. Soc. Am.
128
, 787
–794
.7.
Brittan-Powell
, E. F.
, and Dooling
, R. J.
(2004
). “Development of auditory sensitivity in budgerigars (Melopsittacus undulatus)
,” J. Acoust. Soc. Am.
115
, 3092
–3102
.8.
Brittan-Powell
, E. F.
, Dooling
, R. J.
, and Gleich
, O.
(2002
). “Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus)
,” J. Acoust. Soc. Am.
112
, 999
–1008
.9.
Brittan-Powell
, E. F.
, Dooling
, R. J.
, Ryals
, B.
, and Gleich
, O.
(2010b
). “Electrophysiological and morphological development of the inner ear in Belgian Waterslager canaries
,” Hear. Res.
269
, 56
–69
.10.
Brittan-Powell
, E. F.
, Lohr
, B.
, Hahn
, D. C.
, and Dooling
, R. J.
(2005
). “Auditory brainstem responses in the Eastern screech owl: An estimate of auditory thresholds
,” J. Acoust. Soc. Am.
118
, 314
–321
.11.
Burkard
, R.
, and Hecox
, K. E.
(1987
). “The effect of broadband noise on the human brain-stem auditory evoked response. III. Anatomic locus
,” J. Acoust. Soc. Am.
81
, 1050
–1063
.12.
Burkard
, R.
, and Voigt
, H. F.
(1989
). “Stimulus dependencies of the gerbil brain-stem auditory-evoked response (BAER). I: Effects of click level, rate, and polarity
,” J. Acoust. Soc. Am.
85
, 2514
–2525
.13.
Castellote
, M.
, Mooney
, T. A.
, Quakenbush
, L.
, Hobbs
, R.
, Goertz
, C.
, and Gaglione
, E.
(2014
). “Baseline hearing abilities and variability in wild beluga whales (Delphinapterus leucas)
,” J. Exp. Biol.
217
, 1682
–1691
.14.
Christensen
, C. B.
, Lauridsen
, H.
, Christensen-Dalsgaard
, J.
, Pedersen
, M.
, and Madsen
, P. T.
(2015
). “Better than fish on land? Hearing across metamorphosis in salamanders
,” Proc. R. Soc. London B Biol. Sci.
282
, 20141943
.15.
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
.16.
Counter
, S. A.
(1985
). “Brain-stem evoked potentials and noise effects in seagulls
,” Comp. Biochem. Physiol. A
81
, 837
–845
.17.
Crowell
, S. E.
, Wells-Berlin
, A. M.
, Carr
, C. E.
, Olsen
, G. H.
, Therrien
, R. E.
, Yannuzzi
, S. E.
, and Ketten
, D. R.
(2015
). “A comparison of auditory brainstem responses across diving bird species
,” J. Comp. Physiol. A
201
, 803
–815
.18.
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
.19.
Dyson
, M. L.
, Klump
, G. M.
, and Gauger
B.
(1998
). “Absolute hearing thresholds and critical masking ratios in the European barn owl: A comparison with other owls
,” J. Comp. Physiol. A
182
, 695
–702
.20.
Evans
, D. L.
, and Rosenfield
, R. N.
(1987
). “Remigial molt in fall migrant long-eared and Northern saw-whet owls
,” in Biology and Conservation of Northern Forest Owls: Symposium Proceedings
, edited by R. W.
Nero
, R. J.
Clark
, R. J.
Knapton
, and R. H.
Harme
(USDA Forest Service General Technical Reports
, Fort Collins, CO
), pp. 209
–214
.21.
Finneran
, J. J.
, Mulsow
, J.
, Houser
, D. S.
, and Burkard
, R. F.
(2018
). “Effects of noise burst rise time and level on bottlenose dolphin (Tursiops truncatus) auditory brainstem responses
,” J. Acoust. Soc. Am.
143
, 2914
–2921
.22.
Folsom
, R. C.
, and Aurich
, C. D.
(1987
). “Auditory brainstem responses in human adults and infants: Influence of stimulus onset
,” Audiology
26
, 117
–122
.23.
Gall
, M. D.
, Brierley
, L. E.
, and Lucas
, J. R.
(2011
).“Species and sex effects on auditory processing in brown-headed cowbirds and red-winged blackbirds
,” Anim. Behav.
81
, 973
–982
.24.
Gall
, M. D.
, Brierley
, L. E.
, and Lucas
, J. R.
(2012
). “The sender-receiver matching hypothesis: Support from the peripheral coding of acoustic features in songbirds
,” J. Exp. Biol.
215
, 3742
–3751
.25.
Gall
, M. D.
, and Lucas
, J. R.
(2010
). “Sex differences in auditory filters of brown-headed cowbirds (Molothrus ater)
,” J. Comp. Physiol. A
196
, 559
–567
.26.
Gall
, M. D.
, Salameh
, T. S.
, and Lucas
, J. R.
(2013
). “Songbird frequency selectivity and temporal resolution vary with sex and season
,” Proc. R. Soc. London B Biol. Sci.
280
, 20122296
.27.
Garabon
, J. R.
, and Higgs
, D. M.
(2017
). “The effects of stimulus parameters on auditory evoked potentials of Carassius auratus
,” J. Comp. Physiol. A
203
, 945
–951
.28.
Gução
, A. C. B.
, Romero
, A. C. L.
, Lemes
, F. L.
, Regaçone
, S. F.
, Valenti
, V. E.
, and Frizzo
, A. C. F.
(2015
). “Auditory brainstem responses: Stimulus variations
,” J. Hum. Growth Dev.
25
, 292
–296
.29.
Guitérrez-Ibáñez
, C.
, Iwaniuk
, A. N.
, and Wylie
, D. R.
(2011
). “Relative size of auditory pathways in symmetrically and asymmetrically eared owls
,” Brain Behav. Evol.
78
, 286
–301
.30.
Hall
, J. W.
, III (2015
). eHandbook of Auditory Evoked Responses: Principles, Procedures, and Protocols
(Pearson Education Inc
, London
), Chap. 3, pp. 58
–108
.31.
Halvorsen
, M. B.
, Wysocki
, L. E.
, Stehr
, C. M.
, Baldwin
, D. H.
, Chicoine
, D. R.
, Scholz
, N. L.
, and Popper
, A. N.
(2009
). “Barging effects on sensory systems of Chinook salmon smolts
,” Trans. Am. Fish. Soc.
138
, 777
–789
.32.
Heinz
, R. D.
, Sinott
, J. M.
, and Sachs
, M. B.
(1977
). “Auditory sensitivity of the redwing blackbird (Agelaius phoeniceus) and brown-headed cowbird (Molothrus ater)
,” J. Comp. Physiol. Psych.
91
, 1365
–1376
.33.
Higgs
, D. M.
, Brittan-Powell
, E. F.
, Soares
, D.
, Souza
, M. J.
, Carr
, C. E.
, Dooling
, R. J.
, and Popper
, A. N.
(2002
). “Amphibious auditory responses of the American alligator (Alligator mississipiensis)
,” J. Comp. Physiol. A
18
, 217
–223
.34.
Iwaniuk
, A. N.
, Clayton
, D. H.
, and Wylie
, D. R. W.
(2006
). “Echolocation, vocal learning, auditory localization and the relative size of the avian auditory midbrain nucleus (MLd)
,” Behav. Brain Res.
167
, 305
–317
.35.
Jewett
, D. L.
, and Williston
, J. S.
(1971
). “Auditory-evoked far fields averaged from the scalp of humans
,” Brain
94
, 681
–696
.36.
Mason
, J. T.
, McClure
, C. J. W.
, and Barber
, J. R.
(2016
). “Anthropogenic noise impairs owl hunting behavior
,” Biol. Conserv.
199
, 29
–32
.37.
Mills
, J. H.
, Schmiedt
, R. A.
, and Kulish
, L. F.
(1990
). “Age-related changes in auditory potentials of Mongolian gerbil
,” Hear. Res.
46
, 201
–210
.38.
Mooney
, T. A.
, Castellote
, M.
, Quakenbush
, L.
, Hobbs
, R.
, Goertz
, C.
, and Gaglione
, E.
(2016
). “Measuring hearing in wild beluga whales
,” Adv. Exp. Med. Biol.
875
, 729
–735
.39.
Nachtigall
, P. E.
, Supin
, A. Y.
, Amundin
, M.
, Röken
, B.
, Møller
, T.
, Mooney
, T. A.
, Taylor
, K. A.
, and Yuen
, M.
(2007
). “Polar bear Ursus maritimus hearing measured with auditory evoked potentials
,” J. Exp. Biol.
210
, 1116
–1122
.40.
Norberg
, R. A.
(1977
). “Occurrence and independent evolution of bilateral ear asymmetry in owls and implications on owl taxonomy
,” Philos. Trans. R. Soc. London B Biol. Sci.
280
, 375
–408
.41.
Okanoya
, K.
, and Dooling
, R.
(1987
). “Strain differences in auditory thresholds in the canary (Serinus canaries)
,” J. Comp. Psych.
101
, 213
–215
.42.
Phillips
, D. P.
, and Burkard
, R.
(1999
). “Response magnitude and timing of auditory response initiation in the inferior colliculus of the awake chinchilla
,” J. Acoust. Soc. Am.
105
, 2731
–2737
.43.
Picton
, T. W.
(2011
). Human Auditory Evoked Potentials
(Plural Publishing
, San Diego, CA
), Chap. 8, pp. 213
–245
.44.
Picton
, T. W.
, Hillyard
, S. A.
, Krausz
, H. I.
, and Galambos
, R.
(1974
). “Human auditory evoked potentials. I. Evaluation of components
,” Electroencephalogr. Clin. Neurophysiol.
36
, 179
–190
.45.
Piniak
, W. E. D.
, Mann
, D. A.
, Harms
, C. A.
, Jones
, T. T.
, and Eckert
, S. A.
(2016
). “Hearing in the juvenile green sea turtle (Chelonia mydas): A comparison of underwater and aerial hearing using auditory evoked potentials
,” PLoS One
11
, e0159711
.46.
Popov
, V. V.
, Sysueva
, E. V.
, Nechaev
, D. I.
, Rozhnov
, V. V.
, and Supin
, A. Y.
(2016
). “Auditory evoked potentials in the auditory system of a beluga whale Delphinapterus leucas to prolonged sound stimuli
,” J. Acoust. Soc. Am.
139
, 1101
–1109
.47.
Pyle
, P.
(1997
). “Flight-feather molt patterns and age in North American owls
,” Am. Birding Assoc. Monogr. Field Ornithol.
2
, 1
–32
.48.
Smith
, C. A.
, Konishi
, M.
, and Schuff
, N.
(1985
). “Structure of the barn owl's (Tyto alba) inner ear
,” Hear. Res.
17
, 237
–247
.49.
Stapells
, D.
, and Oates
, P.
(1997
). “Estimation of the pure-tone audiogram by the auditory brainstem response: A review
,” Audiol. Neurotol.
2
, 257
–280
.50.
Stapells
, D.
, and Picton
, T. W.
(1981
). “Technical aspects of brainstem evoked potential audiometry using tones
,” Ear Hear.
2
, 20
–29
.51.
Vélez
, A.
, Gall
, M. D.
, and Lucas
, J. R.
(2015
). “Seasonal plasticity in auditory processing of the envelope and temporal fine structure of sounds in three songbirds
,” Anim. Behav.
103
, 53
–63
.52.
Walsh
, E. J.
, McGee
, J.
, and Javel
, E.
(1986
). “Development of auditory-evoked potentials in the cat. III. Wave amplitudes
,” J. Acoust. Soc. Am.
79
, 745
–754
.53.
Weidensaul
, C. S.
, Colvin
, B. A.
, Brinker
, B. F.
, and Huy
, J. S.
(2011
). “Use of ultraviolet light as an aid in age classification of owls
,” Wilson J. Ornithol.
123
, 373
–377
.54.
Womack
, M. C.
, Christensen-Dalsgaard
, J.
, Coloma
, L. A.
, Chaparro
, J. C.
, and Hoke
, K. L.
(2017
). “Earless toads sense low frequencies but miss the high notes
,” Proc. R. Soc. London B Biol. Sci.
284
, 20171670
.55.
Wong
, A.
, and Gall
, M. D.
(2015
). “Frequency sensitivity in the auditory periphery of male and female black-capped chickadees (Poecile atricapillus)
,” Zoology
118
, 357
–363
.56.
Zeyl
, J. N.
, and Johnston
, C. E.
(2015
). “Amphibious auditory evoked potentials in four North American Testudines genera spanning the aquatic–terrestrial spectrum
,” J. Comp. Physiol. A
201
, 1011
–1018
.57.
Zeyl
, J. N.
, and Johnston
, C. E.
(2016
). “Comparative and developmental patterns of amphibious auditory function in salamanders
,” J. Comp. Physiol. A
202
, 879
–894
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