Auditory brainstem responses in Cope’s gray treefrog (Hyla chrysoscelis): effects of frequency, level, sex and size

Abstract

Our knowledge of the hearing abilities of frogs and toads is largely defined by work with a few well-studied species. One way to further advance comparative work on anuran hearing would be greater use of minimally invasive electrophysiological measures, such as the auditory brainstem response (ABR). This study used the ABR evoked by tones and clicks to investigate hearing in Cope’s gray treefrog (Hyla chrysoscelis). The objectives were to characterize the effects of sound frequency, sound pressure level, and subject sex and body size on ABRs. The ABR in gray treefrogs bore striking resemblance to ABRs measured in other animals. As stimulus level increased, ABR amplitude increased and latency decreased, and for responses to tones, these effects depended on stimulus frequency. Frequency-dependent differences in ABRs were correlated with expected differences in the tuning of two sensory end organs in the anuran inner ear (the amphibian and basilar papillae). The ABR audiogram indicated two frequency regions of increased sensitivity corresponding to the expected tuning of the two papillae. Overall, there was no effect of subject size and only small effects related to subject sex. Together, these results indicate the ABR is an effective method to study audition in anurans.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Aitkin L, Nelson J, Shepherd R (1996) Development of hearing and vocalization in a marsupial, the Northern Quoll, Dasyurus hallucatus. J Exp Zool 276:394–402

    CAS  PubMed  Google Scholar 

  2. Amoser S, Ladich F (2005) Are hearing sensitivities of freshwater fish adapted to the ambient noise in their habitats? J Exp Biol 208:3533–3542

    PubMed  Google Scholar 

  3. Bartol SM, Musick JA, Lenhardt ML (1999) Auditory evoked potentials of the loggerhead sea turtle (Caretta caretta). Copeia 1999:836–840

    Google Scholar 

  4. Bee MA (2012) Sound source perception in anuran amphibians. Curr Opin Neurobiol 22:301–310

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Bibikov NG (2002) Addition of noise enhances neural synchrony to amplitude-modulated sounds in the frog’s midbrain. Hear Res 173:21–28

    CAS  PubMed  Google Scholar 

  6. Bibikov NG, Elepfandt A (2005) Auditory evoked potentials from medulla and midbrain in the clawed frog, Xenopus laevis laevis. Hear Res 204:29–36

    PubMed  Google Scholar 

  7. Boettcher FA, Mills JH, Norton BL, Schmiedt RA (1993) Age-related changes in auditory evoked potentials of gerbils. II. Response latencies. Hear Res 71:146–156

    CAS  PubMed  Google Scholar 

  8. Brittan-Powell EF, Dooling RJ (2004) Development of auditory sensitivity in budgerigars (Melopsittacus undulatus). J Acoust Soc Am 115:3092–3102

    PubMed  Google Scholar 

  9. Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112:999–1008

    PubMed  Google Scholar 

  10. Brittan-Powell EF, Lohr B, Hahn DC, Dooling RJ (2005) Auditory brainstem responses in the Eastern Screech Owl: an estimate of auditory thresholds. J Acoust Soc Am 118:314–321

    PubMed  Google Scholar 

  11. Brittan-Powell EE, Dooling RJ, Ryals B, Gleich O (2010a) Electrophysiological and morphological development of the inner ear in Belgian Waterslager canaries. Hear Res 269:56–69

    PubMed Central  PubMed  Google Scholar 

  12. Brittan-Powell EF, Christensen-Dalsgaard J, Tang YZ, Carr C, Dooling RJ (2010b) The auditory brainstem response in two lizard species. J Acoust Soc Am 128:787–794

    PubMed  Google Scholar 

  13. Capranica RR, Moffat JM (1983) Neurobehavioral correlates of sound communication in anurans. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 701–730

    Google Scholar 

  14. Caras ML, Brenowitz E, Rubel EW (2010) Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A 196:581–599

    Google Scholar 

  15. Carey MB, Zelick R (1993) The effect of sound level, temperature and dehydration on the brain-stem auditory-evoked potential in anuran amphibians. Hear Res 70:216–228

    CAS  PubMed  Google Scholar 

  16. Christensen-Dalsgaard J, Jørgensen MB (1996) Sound and vibration sensitivity of VIIIth nerve fibers in the grassfrog, Rana temporaria. J Comp Physiol A 179:437–445

    CAS  PubMed  Google Scholar 

  17. Christensen-Dalsgaard J, Walkowiak W (1999) In vitro and in vivo responses of saccular and caudal nucleus neurons in the grassfrog (Rana temporaria). Eur J Morphol 37:206–210

    CAS  PubMed  Google Scholar 

  18. Christensen-Dalsgaard J, Breithaupt T, Elepfandt A (1990) Underwater hearing in the clawed frog, Xenopus laevis: tympanic motion studied with laser vibrometry. Naturwissenschaften 77:135–137

    CAS  PubMed  Google Scholar 

  19. Christensen-Dalsgaard J, Jørgensen MB, Kanneworff M (1998) Basic response characteristics of auditory nerve fibers in the grassfrog (Rana temporaria). Hear Res 119:155–163

    CAS  PubMed  Google Scholar 

  20. Church MW, Williams HL, Holloway JA (1984) Brain-stem auditory evoked-potentials in the rat: effects of gender, stimulus characteristics and ethanol sedation. Electroencephalogr Clin Neurophysiol 59:328–339

    CAS  PubMed  Google Scholar 

  21. Corwin JT, Bullock TH, Schweitzer J (1982) The auditory brainstem response in five vertebrate classes. Electroencephalogr Clin Neurophysiol 54:629–641

    CAS  PubMed  Google Scholar 

  22. D’Angelo GJ, De Chicchis AR, Osborn DA, Gallagher GR, Warren RJ, Miller KV (2007) Hear range of white-tailed deer as determined by auditory brainstem response. J Wildl Manag 71:1238–1242

    Google Scholar 

  23. Diekamp B, Gerhardt HC (1995) Selective phonotaxis to advertisement calls in the gray treefrog Hyla versicolor: behavioral experiments and neurophysiological correlates. J Comp Physiol A 177:173–190

    CAS  PubMed  Google Scholar 

  24. Edwards CJ, Kelley DB (2001) Auditory and lateral line inputs to the midbrain of an aquatic anuran; Neuroanatomic studies in Xenopus laevis. J Comp Neurol 438:148–162

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Ehret G, Capranica RR (1980) Masking patterns and filter characteristics of auditory nerve fibers in the green treefrog (Hyla cinerea). J Comp Physiol A 141:1–12

    Google Scholar 

  26. Elliott TM, Christensen-Dalsgaard J, Kelley DB (2007) Tone and call responses of units in the auditory nerve and dorsal medullary nucleus of Xenopus laevis. J Comp Physiol A 193:1243–1257

    Google Scholar 

  27. Elliott TM, Christensen-Dalsgaard J, Kelley DB (2011) Temporally selective processing of communication signals by auditory midbrain neurons. J Neurophysiol 105:1620–1632

    PubMed  Google Scholar 

  28. Feng AS (1982) Quantitative analysis of intensity-rate and intensity-latency functions in peripheral auditory nerve fibers of northern leopard frogs (Rana pipiens). Hear Res 6:241–246

    CAS  PubMed  Google Scholar 

  29. Feng AS, Capranica RR (1976) Sound localization in anurans. I. Evidence of binaural interaction in dorsal medullary nucleus of bullfrogs (Rana catesbeiana). J Neurophysiol 39:871–881

    CAS  PubMed  Google Scholar 

  30. Feng AS, Capranica RR (1978) Sound localization in anurans II. Binaural interaction in superior olivary nucleus of the green tree frog (Hyla cinerea). J Neurophysiol 41:43–54

    CAS  PubMed  Google Scholar 

  31. Frishkopf LS, Capranica RR, Goldstein MH Jr (1968) Neural coding in the bullfrog’s auditory system a teleological approach. Proc IEEE 56:969–980

    Google Scholar 

  32. Fuzessery ZM, Feng AS (1981) Frequency representation in the dorsal medullary nucleus of the leopard frog, Rana pipiens. J Comp Physiol A 143:339–347

    Google Scholar 

  33. Fuzessery ZM, Feng AS (1982) Frequency selectivity in the anuran auditory midbrain: single unit responses to single and multiple tone stimulation. J Comp Physiol A 146:471–484

    Google Scholar 

  34. Gall MD, Brierley LE, Lucas JR (2011) Species and sex effects on auditory processing in brown-headed cowbirds and red-winged blackbirds. Anim Behav 81:973–982

    Google Scholar 

  35. Gerhardt HC (2005) Acoustic spectral preferences in two cryptic species of grey treefrogs: implications for mate choice and sensory mechanisms. Anim Behav 70:39–48

    Google Scholar 

  36. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and diverse solutions. University of Chicago Press, Chicago

    Google Scholar 

  37. Gerhardt HC, Schwartz JJ (2001) Auditory tuning, frequency preferences and mate choice in anurans. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 73–85

    Google Scholar 

  38. Gorga MP, Beauchaine KA, Reiland JK, Worthington DW, Javel E (1984) The effects of stimulus duration on ABR and behavioral thresholds. J Acoust Soc Am 76:616–619

    CAS  PubMed  Google Scholar 

  39. 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 

  40. Graham JW, Olchowski AE, Gilreath TD (2007) How many imputations are really needed? Some practical clarifications of multiple imputation theory. Prev Sci 8:206–213

    PubMed  Google Scholar 

  41. Greenhouse SW, Geisser S (1959) On methods in the analysis of profile data. Psychom 24:95–112

    Google Scholar 

  42. Hall JW (2007) New handbook of auditory evoked responses. Allyn & Bacon, Boston

    Google Scholar 

  43. Hecox K, Squires N, Galambos R (1976) Brainstem auditory evoked responses in man. I. Effect of stimulus rise–fall time and duration. J Acoust Soc Am 60:1187–1192

    CAS  PubMed  Google Scholar 

  44. Henry KS, Lucas JR (2008) Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds. Anim Behav 76:1659–1671

    Google Scholar 

  45. Henry KS, Lucas JR (2009) Vocally correlated seasonal auditory variation in the house sparrow (Passer domesticus). J Exp Biol 212:3817–3822

    CAS  PubMed  Google Scholar 

  46. Henry KS, Lucas JR (2010a) Auditory sensitivity and the frequency selectivity of auditory filters in the Carolina chickadee, Poecile carolinensis. Anim Behav 80:497–507

    Google Scholar 

  47. Henry KS, Lucas JR (2010b) Habitat-related differences in the frequency selectivity of auditory filters in songbirds. Func Ecol 24:614–624

    Google Scholar 

  48. Higgs DM, Brittan-Powell EF, Soares D, Souza MJ, Carr CE, Dooling RJ, Popper AN (2002) Amphibious auditory responses of the Amn alligator (Alligator mississipiensis). J Comp Physiol A 188:217–223

    CAS  Google Scholar 

  49. Hillery CM (1984a) Detection of amplitude-modulated tones by frogs: implications for temporal processing mechanisms. Hear Res 14:129–143

    CAS  PubMed  Google Scholar 

  50. Hillery CM (1984b) Seasonality of two midbrain auditory responses in the treefrog, Hyla chrysoscelis. Copeia 1984:844–852

    Google Scholar 

  51. Hillery CM, Narins PM (1984) Neurophysiological evidence for a traveling wave in the amphibian inner ear. Science 225:1037–1039

    CAS  PubMed  Google Scholar 

  52. Ho CCK, Narins PM (2006) Directionality of the pressure-difference receiver ears in the northern leopard frog, Rana pipiens pipiens. J Comp Physiol A 192:417–429

    Google Scholar 

  53. Horodysky AZ, Brill RW, Fine ML, Musick JA, Latour RJ (2008) Acoustic pressure and particle motion thresholds in six sciaenid fishes. J Exp Biol 211:1504–1511

    PubMed  Google Scholar 

  54. Hu MY, Yan HY, Chung WS, Shiao JC, Hwang PP (2009) Acoustically evoked potentials in two cephalopods inferred using the auditory brainstem response (ABR) approach. Comp Biochem Physiol A 153:278–283

    Google Scholar 

  55. Hubl L, Schneider H (1979) Temperature and auditory thresholds: bioacoustic studies of the frogs Rana r. ridibunda, Hyla a. arborea and Hyla a. savignyi (Anura, amphibia). J Comp Physiol A 130:17–27

    Google Scholar 

  56. Jerger J, Hall J (1980) Effects of age and sex on auditory brainstem response. Arch Otolaryngol 106:387–391

    CAS  PubMed  Google Scholar 

  57. Katbamna B, Thodi C, Senturia JB, Metz DA (1992) Auditory evoked brainstem responses in the hibernating woodchuck Marmota monax. Comp Biochem Physiol A 102:513–517

    CAS  Google Scholar 

  58. Katbamna B, Brown JA, Collard M, Ide CF (2006a) Auditory brainstem responses to airborne sounds in the aquatic frog Xenopus laevis: correlation with middle ear characteristics. J Comp Physiol A 192:381–387

    Google Scholar 

  59. Katbamna B, Langerveld AJ, Ide CF (2006b) Aroclor 1254 impairs the hearing ability of Xenopus laevis. J Comp Physiol A 192:971–983

    CAS  Google Scholar 

  60. Keddy-Hector AC, Wilczynski W, Ryan MJ (1992) Call patterns and basilar papilla tuning in cricket frogs. II. Intrapopulation variation and allometry. Brain Behav Evol 39:238–246

    CAS  PubMed  Google Scholar 

  61. Kelley DB (2004) Vocal communication in frogs. Curr Opin Neurobiol 14:751–757

    CAS  PubMed  Google Scholar 

  62. Kenyon TN, Ladich F, Yan HY (1998) A comparative study of hearing ability in fishes: the auditory brainstem response approach. J Comp Physiol A 182:307–318

    CAS  PubMed  Google Scholar 

  63. Klishin VO, Diaz RP, Popov VV, Supin AY (1990) Some characteristics of hearing of the Brazilian manatee, Trichechus inunguis. Aquat Mamm 16:139–144

    Google Scholar 

  64. Klump GM, Benedix JH, Gerhardt HC, Narins PM (2004) AM representation in green treefrog auditory nerve fibers: neuroethological implications for pattern recognition and sound localization. J Comp Physiol A 190:1011–1021

    CAS  Google Scholar 

  65. Ladich F, Fay RR (2013) Auditory evoked potential audiometry in fish. Rev Fish Biol Fisheries 23:317–364

    Google Scholar 

  66. Ladich F, Yan HY (1998) Correlation between auditory sensitivity and vocalization in anabantoid fishes. J Comp Physiol A 182:737–746

    CAS  PubMed  Google Scholar 

  67. Lohr B, Brittan-Powell EF, Dooling RJ (2013) Auditory brainstem responses and auditory thresholds in woodpeckers. J Acoust Soc Am 133:337–342

    PubMed  Google Scholar 

  68. Lovell JM, Findlay MM, Moate RM, Yan HY (2005) The hearing abilities of the prawn Palaemon serratus. Comp Biochem Physiol A 140:89–100

    CAS  Google Scholar 

  69. Lucas JR, Freeberg TM, Krishnan A, Long GR (2002) A comparative study of avian auditory brainstem responses: correlations with phylogeny and vocal complexity, and seasonal effects. J Comp Physiol A 188:981–992

    CAS  Google Scholar 

  70. Lugli M, Yan HY, Fine ML (2003) Acoustic communication in two freshwater gobies: the relationship between ambient noise, hearing thresholds and sound spectrum. J Comp Physiol A 189:309–320

    CAS  Google Scholar 

  71. Martin KJ, Alessi SC, Gaspard JC, Tucker AD, Bauer GB, Mann DA (2012) Underwater hearing in the loggerhead turtle (Caretta caretta): a comparison of behavioral and auditory evoked potential audiograms. J Exp Biol 215:3001–3009

    PubMed  Google Scholar 

  72. McFadden SL, Walsh EJ, McGee J (1996) Onset and development of auditory brainstem responses in the Mongolian gerbil (Meriones unguiculatus). Hear Res 100:68–79

    CAS  PubMed  Google Scholar 

  73. Meenderink SWF, Kits M, Narins PM (2010) Frequency matching of vocalizations to inner-ear sensitivity along an altitudinal gradient in the coqui frog. Biol Lett 6:278–281

    PubMed Central  PubMed  Google Scholar 

  74. Miranda JA, Wilczynski W (2009a) Female reproductive state influences the auditory midbrain response. J Comp Physiol A 195:341–349

    Google Scholar 

  75. Miranda JA, Wilczynski W (2009b) Sex differences and androgen influences on midbrain auditory thresholds in the green treefrog, Hyla cinerea. Hear Res 252:79–88

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Mooney TA, Hanlon RT, Christensen-Dalsgaard J, Madsen PT, Ketten DR, Nachtigall PE (2010) Sound detection by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure. J Exp Biol 213:3748–3759

    PubMed  Google Scholar 

  77. Mudry KM, Capranica RR (1987) Correlation between auditory thalamic area evoked responses and species-specific call characteristics II. Hyla cinerea (Anura: Hylidae). J Comp Physiol A 161:407–416

    CAS  PubMed  Google Scholar 

  78. Munro KJ, Shiu JN, Cox CL (1997) The effect of head size on the auditory brainstem response for two breeds of dog. Br J Audiol 31:309–314

    CAS  PubMed  Google Scholar 

  79. Nachtigall PE, Supin AY (2008) A false killer whale adjusts its hearing when it echolocates. J Exp Biol 211:1714–1718

    PubMed  Google Scholar 

  80. Nachtigall PE, Supin AY, Amundin M, Roken B, Moller T, Mooney TA, Taylor KA, Yuen M (2007) Polar bear Ursus maritimus hearing measured with auditory evoked potentials. J Exp Biol 210:1116–1122

    PubMed  Google Scholar 

  81. Narins PM, Capranica RR (1976) Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science 192:378–380

    CAS  PubMed  Google Scholar 

  82. Narins PM, Feng AS, Fay RR, Popper AN (2007) Hearing and sound communication in amphibians. Springer, New York

    Google Scholar 

  83. Noirot IC, Brittan-Powell EF, Dooling RJ (2011) Masked auditory thresholds in three species of birds, as measured by the auditory brainstem response (L). J Acoust Soc Am 129:3445–3448

    PubMed  Google Scholar 

  84. Penna M, Capranica RR, Somers J (1992) Hormone-induced vocal behavior and midbrain auditory sensitivity in the green treefrog, Hyla cinerea. J Comp Physiol A 170:73–82

    CAS  PubMed  Google Scholar 

  85. Popov VV, Supin AY (1990) Auditory brain stem responses in characterization of dolphin hearing. J Comp Physiol A 166:385–393

    CAS  PubMed  Google Scholar 

  86. Popov VV, Supin AY (2001) Contribution of various frequency bands to ABR in dolphins. Hear Res 151:250–260

    CAS  PubMed  Google Scholar 

  87. Ptacek MB, Gerhardt HC, Sage RD (1994) Speciation by polyploidy in treefrogs: multiple origins of the tetraploid, Hyla versicolor. Evol 48:898–908

    Google Scholar 

  88. Ramsier MA, Dominy NJ (2010) A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in Lemur catta and Nycticebus coucang. Am J Primatol 72:217–233

    PubMed  Google Scholar 

  89. Ratnam R, Feng AS (1998) Detection of auditory signals by frog inferior collicular neurons in the presence of spatially separated noise. J Neurophysiol 80:2848–2859

    CAS  PubMed  Google Scholar 

  90. Rubin DB (1976) Inference and missing data. Biom 63:581–590

    Google Scholar 

  91. Schafer JL (1999) Multiple imputation: a primer. Stat Methods Med Res 8:3–15

    CAS  PubMed  Google Scholar 

  92. Schafer JL, Olsen MK (1998) Multiple imputation for multivariate missing-data problems: a data analyst’s perspective. Multivar Behav Res 33:545–571

    Google Scholar 

  93. Schrode K, Ward JL, Vélez A, Bee MA (2012) Female preferences for spectral call properties in the western genetic lineage of Cope’s gray treefrog (Hyla chrysoscelis). Behav Ecol Sociobiol 66:1595–1606

    PubMed Central  PubMed  Google Scholar 

  94. Schwartz JJ, Simmons AM (1990) Encoding of a spectrally complex natural call in the bullfrog’s auditory nerve. J Comp Physiol A 166:489–499

    CAS  PubMed  Google Scholar 

  95. Seaman RL (1991) Method to record evoked-potentials from the frog 8th nerve. Hear Res 51:301–305

    CAS  PubMed  Google Scholar 

  96. Shofner WP, Feng AS (1981) Post-metamorphic development of the frequency selectivities and sensitivities of the peripheral auditory system of the bullfrog, Rana catesbeiana. J Exp Biol 93:181–196

    Google Scholar 

  97. Simmons AM, Ferragamo M (1993) Periodicity extraction in the anuran auditory nerve. I. “Pitch-shift” effects. J Comp Physiol A 172:57–69

    CAS  PubMed  Google Scholar 

  98. Simmons DD, Bertolotto C, Narins PM (1992) Innervation of the amphibian and basilar papillae in the leopard frog: reconstructions of single labeled fibers. J Comp Neurol 322:191–200

    CAS  PubMed  Google Scholar 

  99. Simmons AM, Reese G, Ferragamo M (1993) Periodicity extraction in the anuran auditory nerve. II. Phase and temporal fine-structure. J Acoust Soc Am 93:3374–3389

    CAS  PubMed  Google Scholar 

  100. Simmons AM, Sanderson MI, Garabedian CE (2000) Representation of waveform periodicity in the auditory midbrain of the bullfrog, Rana catesbeiana. J Assoc Res Otolaryngol 1:2–24

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Simmons DD, Meenderink SWF, Vassilakis PN (2007) Anatomy, physiology, and function of the auditory end-organs in the frog inner ear. In: Narins PA, Feng AS, Fay RR, Popper AN (eds) Hearing and sound communication in amphibians. Springer, New York, pp 184–220

    Google Scholar 

  102. Smith ME, Kane AS, Popper AN (2004) Noise-induced stress response and hearing loss in goldfish (Carassius auratus). J Exp Biol 207:427–435

    PubMed  Google Scholar 

  103. Song L, McGee J, Walsh EJ (2006) Frequency- and level-dependent changes in auditory brainstem responses (ABRs) in developing mice. J Acoust Soc Am 119:2242–2257

    PubMed  Google Scholar 

  104. Stiebler IB, Narins PM (1990) Temperature-dependence of auditory nerve response properties in the frog. Hear Res 46:63–81

    CAS  PubMed  Google Scholar 

  105. Supin AY, Popov VV, Klishin VO (1993) ABR frequency tuning curves in dolphins. J Comp Physiol A 173:649–656

    CAS  PubMed  Google Scholar 

  106. Szymanski MD, Supin AY, Bain DE, Henry KR (1998) Killer whale (Orcinus orca) auditory evoked potentials to rhythmic clicks. Mar Mamm Sci 14:676–691

    Google Scholar 

  107. 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 

  108. Uetake K, Yayou KI, Okamoto T (1996) Auditory brainstem response and objective assessment of hearing thresholds in cowshed calves. J Ethol 14:73–75

    Google Scholar 

  109. Uzuka Y, Furuta T, Yamaoka M, Ohnishi T, Tsubone H, Sugano S (1996) Threshold changes in auditory brainstem response (ABR) due to the administration of kanamycin in dogs. Exp Anim 45:325–331

    CAS  PubMed  Google Scholar 

  110. Walsh EJ, McGee J, Javel E (1986) Development of auditory-evoked potentials in the cat. II. Wave latencies. J Acoust Soc Am 79:725–744

    CAS  PubMed  Google Scholar 

  111. Wilczynski W, Capranica RR (1984) The auditory system of anuran amphibians. Prog Neurobiol 22:1–38

    CAS  PubMed  Google Scholar 

  112. Wilczynski W, Ryan MJ (2010) The behavioral neuroscience of anuran social signal processing. Curr Opin Neurobiol 20:754–763

    CAS  PubMed Central  PubMed  Google Scholar 

  113. Wilczynski W, Keddy-Hector AC, Ryan MJ (1992) Call patterns and basilar papilla tuning in cricket frogs. I. Differences among populations and between sexes. Brain Behav Evol 39:229–237

    CAS  PubMed  Google Scholar 

  114. Wilczynski W, McClelland BE, Rand AS (1993) Acoustic, auditory, and morphological divergence in three species of neotropical frog. J Comp Physiol A 172:425–438

    CAS  PubMed  Google Scholar 

  115. Will U, Fritzsch B (1988) The eighth nerve of amphibians: peripheral and central distribution. In: Fritzsch B, Wolkowiak W, Ryan MJ, Wilczynski W, Hetheringon T (eds) The Evolution of the amphibian auditory system. Wiley, New York, pp 159–183

    Google Scholar 

  116. Wysocki LE, 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

    CAS  PubMed  Google Scholar 

  117. Wysocki LE, Ladich F (2003) The representation of conspecific sounds in the auditory brainstem of teleost fishes. J Exp Biol 206:2229–2240

    PubMed  Google Scholar 

  118. Yu ZL, Qiu Q, Xu ZM, Shen JX (2006) Auditory response characteristics of the piebald odorous frog and their implications. J Comp Physiol A 192:801–806

    Google Scholar 

  119. Zakon H, Capranica RR (1981) An anatomical and physiological study of regeneration of the eighth nerve in the leopard frog. Brain Res 209:325–338

    CAS  PubMed  Google Scholar 

  120. Zakon HH, Wilczynski W (1988) The physiology of the anuran eighth nerve. In: Fritzsch B, Wolkowiak W, Ryan MJ, Wilczynski W, Hetherington T (eds) The evolution of the amphibian auditory system. Wiley, New York, pp 125–155

    Google Scholar 

  121. Zhang D, Cui JG, Tang YZ (2012) Plasticity of peripheral auditory frequency sensitivity in Emei music frog. PLoS ONE 7:e45792

    CAS  PubMed Central  PubMed  Google Scholar 

  122. Zhou X, Jen PHS, Seburn KL, Frankel WN, Zheng QY (2006) Auditory brainstem responses in 10 inbred strains of mice. Brain Res 1091:16–26

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Alejandro Vélez for helpful feedback on an earlier version of the manuscript, Justin Becknell for the illustration in Fig. 1, Madeleine Linck, Don Pereira, and Ed Quinn for access to study sites and collection permissions, and many undergraduate students for help collecting frogs. We also thank Ed Smith for programming. This work was supported by the National Institutes Health in the form of R01 DC009582 to author M. A. Bee at the University of Minnesota, P30 DC004664 to R. J. Dooling at the University of Maryland and T32 NS048944 to T. J. Ebner at the University of Minnesota.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Katrina M. Schrode.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 46 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schrode, K.M., Buerkle, N.P., Brittan-Powell, E.F. et al. Auditory brainstem responses in Cope’s gray treefrog (Hyla chrysoscelis): effects of frequency, level, sex and size. J Comp Physiol A 200, 221–238 (2014). https://doi.org/10.1007/s00359-014-0880-8

Download citation

Keywords

  • Auditory brainstem response
  • Audiogram
  • Communication
  • Gray treefrog
  • Hearing