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Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow

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Abstract

Song in oscine birds is a learned behavior that plays important roles in breeding. Pronounced seasonal differences in song behavior and in the morphology and physiology of the neural circuit underlying song production are well documented in many songbird species. Androgenic and estrogenic hormones largely mediate these seasonal changes. Although much work has focused on the hormonal mechanisms underlying seasonal plasticity in songbird vocal production, relatively less work has investigated seasonal and hormonal effects on songbird auditory processing, particularly at a peripheral level. We addressed this issue in Gambel’s white-crowned sparrow (Zonotrichia leucophrys gambelii), a highly seasonal breeder. Photoperiod and hormone levels were manipulated in the laboratory to simulate natural breeding and non-breeding conditions. Peripheral auditory function was assessed by measuring the auditory brainstem response (ABR) and distortion product otoacoustic emissions (DPOAEs) of males and females in both conditions. Birds exposed to breeding-like conditions demonstrated elevated thresholds and prolonged peak latencies when compared with birds housed under non-breeding-like conditions. There were no changes in DPOAEs, however, which indicates that the seasonal differences in ABRs do not arise from changes in hair cell function. These results suggest that seasons and hormones impact auditory processing as well as vocal production in wild songbirds.

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Abbreviations

ABR:

Auditory brainstem response

AR:

Androgen receptor

DPOAE:

Distortion product otoacoustic emission

ER:

Estrogen receptor

F1:

First primary tone

F2:

Second primary tone

LD:

Long day

L1:

Level of the first primary tone

L2:

Level of the second primary tone

NCM:

Caudomedial nidopallium

Q :

Quality factor

SD:

Short day

References

  • Achor LJ, Starr A (1980) Auditory brain stem responses in the cat. I. Intracranial and extracranial recordings. Electroencephalogr Clin Neurophysiol 48:154–173

    Article  PubMed  CAS  Google Scholar 

  • Akdogan O, Ozkan S (2006) Otoacoustic emissions in children with otitis media with effusion. Int J Pediatr Otorhinolaryngol 70:1941–1944

    Article  PubMed  Google Scholar 

  • Baptista LF, Morton ML (1981) Interspecific song acquisition by a white-crowned sparrow. Auk 98:383–385

    Google Scholar 

  • Baptista LF, Petrinovich L (1986) Song development in the white-crowned sparrow: social factors and sex differences. Anim Behav 34:1359–1371

    Article  Google Scholar 

  • Bergevin C, Freeman DM, Saunders JC, Shera CA (2008) Otoacoustic emissions in humans, birds, lizards, and frogs: evidence for multiple generation mechanisms. J Comp Physiol 194:665–683

    Article  Google Scholar 

  • Borg E, Engstrom B (1983) Hearing thresholds in the rabbit. A behavioral and electrophysiological study. Acta Otolaryngol 95:19–26

    Article  PubMed  CAS  Google Scholar 

  • Brenowitz EA (1981) ‘Territorial song’ as a flocking signal in red-winged blackbirds. Anim Behav 29:641–642

    Article  Google Scholar 

  • Brenowitz EA (1991) Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science (New York, NY) 251:303–305

    CAS  Google Scholar 

  • Brenowitz EA (2008) Plasticity of the song control system in adult birds. In: Zeigler P, Marler P (eds) Neuroscience of birdsong. Cambridge University Press, New York, p 332

    Google Scholar 

  • Brenowitz EA, Baptista LF, Lent K, Wingfield JC (1998) Seasonal plasticity of the song control system in wild Nuttall’s white-crowned sparrows. J Neurobiol 34:69–82

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Brown-Borg HM, Beck MM, Jones TA (1987) Origins of peripheral and brainstem auditory responses in the White Leghorn chick. Comp Biochem Physiol 88:391–396

    Article  CAS  Google Scholar 

  • Buchwald JS, Huang C (1975) Far-field acoustic response: origins in the cat. Science (New York, NY) 189:382–384

    CAS  Google Scholar 

  • Burkard R, Jones S, Jones T (1994) Conventional and cross-correlation brain-stem auditory evoked responses in the white leghorn chick: rate manipulations. J Acoust Soc Am 95:2136–2144

    Article  PubMed  CAS  Google Scholar 

  • Burkard R, McGee J, Walsh EJ (1996) Effects of stimulus rate on the feline brain-stem auditory evoked response during development. I. Peak latencies. J Acoust Soc Am 100:978–990

    Article  PubMed  CAS  Google Scholar 

  • Catchpole CK, Slater PJB (1995) Bird song: biological themes and variations. University Press, Cambridge

    Google Scholar 

  • Coats AC (1978) Human auditory nerve action potentials and brain stem evoked responses. Arch Otolaryngol 104:709–717

    PubMed  CAS  Google Scholar 

  • Coats AC, Martin JL (1977) Human auditory nerve action potentials and brain stem evoked responses: effects of audiogram shape and lesion location. Arch Otolaryngol 103:605–622

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cynx J, Nottebohm F (1992) Role of gender, season, and familiarity in discrimination of conspecific song by zebra finches (Taeniopygia guttata). Proc Natl Acad Sci USA 89:1368–1371

    Article  PubMed  CAS  Google Scholar 

  • Dallos P (2008) Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 18:370–376

    Article  PubMed  CAS  Google Scholar 

  • Dallos P, Wu X, Cheatham MA, Gao J, Zheng J, Anderson CT, Jia S, Wang X, Cheng WH, Sengupta S, He DZ, Zuo J (2008) Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58:333–339

    Article  PubMed  CAS  Google Scholar 

  • De Groof G, Verhoye M, Poirier C, Leemans A, Eens M, Darras VM, Van der Linden A (2009) Structural changes between seasons in the songbird auditory forebrain. J Neurosci 29:13557–13565

    Article  PubMed  CAS  Google Scholar 

  • Del Negro C, Edeline JM (2002) Sex and season influence the proportion of thin spike cells in the canary HVc. Neuroreport 13:2005–2009

    Article  PubMed  Google Scholar 

  • Del Negro C, Kreutzer M, Gahr M (2000) Sexually stimulating signals of canary (Serinus canaria) songs: evidence for a female-specific auditory representation in the HVc nucleus during the breeding season. Behav Neurosci 114:526–542

    Article  PubMed  CAS  Google Scholar 

  • Del Negro C, Lehongre K, Edeline JM (2005) Selectivity of canary HVC neurons for the bird’s own song: modulation by photoperiodic conditions. J Neurosci 25:4952–4963

    Article  PubMed  CAS  Google Scholar 

  • Despland PA, Galambos R (1980) The auditory brainstem response (ABR) is a useful diagnostic tool in the intensive care nursery. Pediatr Res 14:154–158

    Article  PubMed  CAS  Google Scholar 

  • DeWolfe BB, Kaska DD, Peyton LJ (1974) Prominent variations in the songs of Gambel’s white-crowned sparrows. Bird Banding 45:224–252

    Google Scholar 

  • Dooling RJ, Lohr B, Dent ML (2000) Hearing in birds and reptiles. In: Dooling RJ, Popper AN, Fay RR (eds) Comparative hearing: birds and reptiles. Springer, New York, pp 308–359

    Google Scholar 

  • Forlano PM, Deitcher DL, Bass AH (2005) Distribution of estrogen receptor alpha mRNA in the brain and inner ear of a vocal fish with comparisons to sites of aromatase expression. J Comp Neurol 483:91–113

    Article  PubMed  CAS  Google Scholar 

  • Fusani L, Van’t Hof T, Hutchison JB, Gahr M (2000) Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J Neurobiol 43:254–268

    Article  PubMed  CAS  Google Scholar 

  • Fusani L, Hutchison JB, Gahr M (2001) Testosterone regulates the activity and expression of aromatase in the canary neostriatum. J Neurobiol 49:1–8

    Article  PubMed  CAS  Google Scholar 

  • Gelinas D, Callard GV (1997) Immunolocalization of aromatase- and androgen receptor-positive neurons in the goldfish brain. Gen Comp Endocrinol 106:155–168

    Article  PubMed  CAS  Google Scholar 

  • Goense JB, Feng AS (2005) Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain. J Neurobiol 65:22–36

    Article  PubMed  Google Scholar 

  • Hall JW (1992) Handbook of auditory evoked responses. Allyn and Bacon, Needham Heights

    Google Scholar 

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

    Google Scholar 

  • Harris FP (1990) Distortion-product otoacoustic emissions in humans with high frequency sensorineural hearing loss. J Speech Hear Res 33:594–600

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hultcrantz M, Simonoska R, Stenberg AE (2006) Estrogen and hearing: a summary of recent investigations. Acta Otolaryngol 126:10–14

    Article  PubMed  CAS  Google Scholar 

  • Jerger J, Mauldin L (1978) Prediction of sensorineural hearing level from the brain stem evoked response. Arch Otolaryngol 104:456–461

    PubMed  CAS  Google Scholar 

  • Jewett DL, Romano MN, Williston JS (1970) Human auditory evoked potentials: possible brain stem components detected on the scalp. Science (New York, NY) 167:1517–1518

    CAS  Google Scholar 

  • Katayama A (1985) Postnatal development of auditory function in the chicken revealed by auditory brain-stem responses (ABRs). Electroencephalogr Clin Neurophysiol 62:388–398

    Article  PubMed  CAS  Google Scholar 

  • Kemp DT (1978) Stimulated acoustic emissions from within the human auditory system. J Acoust Soc Am 64:1386–1391

    Article  PubMed  CAS  Google Scholar 

  • Kemp DT (2002) Otoacoustic emissions, their origin in cochlear function, and use. Br Med Bull 63:223–241

    Article  PubMed  Google Scholar 

  • Kettembeil S, Manley GA, Siegl E (1995) Distortion-product otoacoustic emissions and their anaesthesia sensitivity in the European starling and the chicken. Hear Res 86:47–62

    Article  PubMed  CAS  Google Scholar 

  • Liberman MC, Tartaglini E, Fleming JC, Neufeld EJ (2006) Deletion of SLC19A2, the high affinity thiamine transporter, causes selective inner hair cell loss and an auditory neuropathy phenotype. J Assoc Res Otolaryngol 7:211–217

    Article  PubMed  CAS  Google Scholar 

  • Lonsbury-Martin BL, Cutler WM, Martin GK (1991) Evidence for the influence of aging on distortion-product otoacoustic emissions in humans. J Acoust Soc Am 89:1749–1759

    Article  PubMed  CAS  Google Scholar 

  • 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 188:981–992

    Article  CAS  Google Scholar 

  • Lucas JR, Freeberg TM, Long GR, Krishnan A (2007) Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches. J Comp Physiol 193:201–215

    Article  Google Scholar 

  • Maney DL, Cho E, Goode CT (2006) Estrogen-dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23:1523–1529

    Article  PubMed  Google Scholar 

  • Margoliash D (1983) Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J Neurosci 3:1039–1057

    PubMed  CAS  Google Scholar 

  • Marler P, Peters S, Ball GF, Dufty AM Jr, Wingfield JC (1988) The role of sex steroids in the acquisition and production of birdsong. Nature 336:770–772

    Article  PubMed  CAS  Google Scholar 

  • McClintock M (1971) Menstrual synchrony and suppression. Nature 229:244

    Article  PubMed  CAS  Google Scholar 

  • McEwen BS (1991) Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol Sci 12:141–147

    Article  PubMed  CAS  Google Scholar 

  • McFadden D (2009) Masculinization of the mammalian cochlea. Hear Res 252:37–48

    Article  PubMed  Google Scholar 

  • McFadden D, Pasanen EG, Raper J, Lange HS, Wallen K (2006) Sex differences in otoacoustic emissions measured in rhesus monkeys (Macaca mulatta). Horm Behav 50:274–284

    Article  PubMed  Google Scholar 

  • Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ (2007a) Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045–12057

    Article  PubMed  CAS  Google Scholar 

  • Meitzen J, Perkel DJ, Brenowitz EA (2007b) Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J Comp Physiol 193:677–683

    Article  Google Scholar 

  • Meitzen J, Thompson CK, Choi H, Perkel DJ, Brenowitz EA (2009a) Time course of changes in Gambel’s white-crowned sparrow song behavior following transitions in breeding condition. Horm Behav 55:217–227

    Article  PubMed  Google Scholar 

  • Meitzen J, Weaver AL, Brenowitz EA, Perkel DJ (2009b) Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions. J Neurosci 29:6558–6567

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Miranda JA, Wilczynski W (2009b) Sex differences and androgen influences on midbrain auditory thresholds in the green tree-frog, Hyla cinera. Hear Res. doi:10.1016/j.heares.2009.04.004

  • Mitsushima D, Takase K, Funabashi T, Kimura F (2009) Gonadal steroids maintain 24 h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J Neurosci 29:3808–3815

    Article  PubMed  CAS  Google Scholar 

  • Moller AR, Jannetta PJ (1981) Compound action potentials recorded intracranially from the auditory nerve in man. Exp Neurol 74:862–874

    Article  PubMed  CAS  Google Scholar 

  • Moller AR, Jannetta PJ (1983) Interpretation of brainstem auditory evoked potentials: results from intracranial recordings in humans. Scand Audiol 12:125–133

    PubMed  CAS  Google Scholar 

  • Moller AR, Jannetta PJ, Moller MB (1981) Neural generators of brainstem evoked potentials. Results from human intracranial recordings. Ann Otol Rhinol Laryngol 90:591–596

    PubMed  CAS  Google Scholar 

  • Moore MC (1982) Hormonal response of free-living male white-crowned sparrows to experimental manipulation of female sexual behavior. Horm Behav 16:323–329

    Article  PubMed  CAS  Google Scholar 

  • Nehls HB (1981) Familiar birds of the northwest. Portland Audubon Society, Portland

    Google Scholar 

  • Noirot IC, Adler HJ, Cornil CA, Harada N, Dooling RJ, Balthazart J, Ball GF (2009) Presence of aromatase and estrogen receptor alpha in the inner ear of zebra finches. Hear Res 252:49–55

    Article  PubMed  CAS  Google Scholar 

  • Nottebohm F (1981) A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science (New York, NY) 214:1368–1370

    CAS  Google Scholar 

  • Okanoya K, Dooling RJ (1988) Hearing in the swamp sparrow (Melospiza georgiana) and the song sparrow (Melospiza melodia). Anim Behav 36:726–732

    Article  Google Scholar 

  • Pak MW, Ng MH, Leung CB, van Hasselt CA (2000) Cochlear deafness in a Chinese family with Fechtner’s syndrome. Am J Otol 21:345–350

    Article  PubMed  CAS  Google Scholar 

  • Park KH, Meitzen J, Moore IT, Brenowitz EA, Perkel DJ (2005) Seasonal-like plasticity of spontaneous firing rate in a songbird pre-motor nucleus. J Neurobiol 64:181–191

    Article  PubMed  Google Scholar 

  • Ponton CW, Moore JK, Eggermont JJ (1996) Auditory brain stem response generation by parallel pathways: differential maturation of axonal conduction time and synaptic transmission. Ear Hear 17:402–410

    Article  PubMed  CAS  Google Scholar 

  • Probst R, Lonsbury-Martin BL, Martin GK (1991) A review of otoacoustic emissions. J Acoust Soc Am 89:2027–2067

    Article  PubMed  CAS  Google Scholar 

  • Riters LV, Baillien M, Eens M, Pinxten R, Foidart A, Ball GF, Balthazart J (2001) Seasonal variation in androgen-metabolizing enzymes in the diencephalon and telencephalon of the male European starling (Sturnus vulgaris). J Neuroendocrinol 13:985–997

    Article  PubMed  CAS  Google Scholar 

  • Rosenhamer HJ, Lindstrom B, Lundborg T (1981) On the use of click-evoked electric brainstem responses in audiological diagnosis. IV. Interaural latency differences (wave V) in cochlear hearing loss. Scand Audiol 10:67–73

    PubMed  CAS  Google Scholar 

  • Sanford SE, Lange HS, Maney DL (2009) Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev Neurobiol 70:73–86

    Google Scholar 

  • Schank JC (2001) Measurement and cycle variability: reexamining the case for ovarian-cycle synchrony in primates. Behav Process 56:131–146

    Article  Google Scholar 

  • Schumacher M, Balthazart J (1986) Testosterone-induced brain aromatase is sexually dimorphic. Brain Res 370:285–293

    Article  PubMed  CAS  Google Scholar 

  • Sisneros JA (2009) Seasonal plasticity of auditory saccular sensitivity in the vocal plainfin midshipman fish, Porichthys notatus. J Neurophysiol 102:1121–1131

    Article  PubMed  Google Scholar 

  • Sisneros JA, Bass AH (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23:1049–1058

    PubMed  CAS  Google Scholar 

  • Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science (New York, NY) 305:404–407

    CAS  Google Scholar 

  • Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995) Seasonal changes in song nuclei and song behavior in Gambel’s white-crowned sparrows. J Neurobiol 28:114–125

    Article  PubMed  CAS  Google Scholar 

  • Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17:6001–6010

    PubMed  CAS  Google Scholar 

  • Soha JA, Marler P (2000) A species-specific acoustic cue for selective song learning in the white-crowned sparrow. Anim Behav 60:297–306

    Article  PubMed  Google Scholar 

  • Sohmer H, Feinmesser M, Szabo G (1974) Sources of electrocochleographic responses as studied in patients with brain damage. Electroencephalogr Clin Neurophysiol 37:663–669

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Hartman VN, Wingfield JC, Brenowitz EA (1999) Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J Comp Neurol 409:224–236

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Schlinger BA, Wingfield JC, Saldanha CJ (2003) Brain aromatase, 5 alpha-reductase, and 5 beta-reductase change seasonally in wild male song sparrows: relationship to aggressive and sexual behavior. J Neurobiol 56:209–221

    Article  PubMed  CAS  Google Scholar 

  • Soma KK, Tramontin AD, Featherstone J, Brenowitz EA (2004) Estrogen contributes to seasonal plasticity of the adult avian song control system. J Neurobiol 58:413–422

    Article  PubMed  CAS  Google Scholar 

  • Starr A, Hamilton AE (1976) Correlation between confirmed sites of neurological lesions and abnormalities of far-field auditory brainstem responses. Electroencephalogr Clin Neurophysiol 41:595–608

    Article  PubMed  CAS  Google Scholar 

  • Steimer T, Hutchison JB (1981) Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature 292:345–347

    Article  PubMed  CAS  Google Scholar 

  • Stenberg AE, Wang H, Sahlin L, Hultcrantz M (1999) Mapping of estrogen receptors alpha and beta in the inner ear of mouse and rat. Hear Res 136:29–34

    Article  PubMed  CAS  Google Scholar 

  • Stenberg AE, Wang H, Fish J 3rd, Schrott-Fischer A, Sahlin L, Hultcrantz M (2001) Estrogen receptors in the normal adult and developing human inner ear and in Turner’s syndrome. Hear Res 157:87–92

    Article  PubMed  CAS  Google Scholar 

  • Stevens SS, Poulton EC (1956) The estimation of loudness by unpracticed observers. J Exp Psychol 51:71–78

    Article  PubMed  CAS  Google Scholar 

  • Swett MB, Breuner CW (2008) Interaction of testosterone, corticosterone and corticosterone binding globulin in the white-throated sparrow (Zonotrichia albicollis). Comp Biochem Physiol A Mol Integr Physiol 151:226–231

    Article  PubMed  CAS  Google Scholar 

  • Terleph TA, Lu K, Vicario DS (2008) Response properties of the auditory telencephalon in songbirds change with recent experience and season. PLoS ONE 3:e2854

    Article  PubMed  CAS  Google Scholar 

  • Tramontin AD, Hartman VN, Brenowitz EA (2000) Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J Neurosci 20:854–861

    PubMed  CAS  Google Scholar 

  • Tramontin AD, Wingfield JC, Brenowitz EA (2003) Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurobiol 57:130–140

    Article  PubMed  CAS  Google Scholar 

  • Tremere LA, Jeong JK, Pinaud R (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29:5949–5963

    Article  PubMed  CAS  Google Scholar 

  • Vyas A, Harding C, Borg L, Bogdan D (2009) Acoustic characteristics, early experience, and endocrine status interact to modulate female zebra finches’ behavioral responses to songs. Horm Behav 55:50–59

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC, Farner DS (1978) The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol Reprod 19:1046–1056

    Article  PubMed  CAS  Google Scholar 

  • Wingfield JC, Crim JW, Mattocks PW Jr, Farner DS (1979) Responses of photosensitive and photorefractory male white-crowned sparrows (Zonotrichia leucophrys gambelii) to synthetic mammalian luteinizing hormone releasing hormone (syn-LHRH). Biol Reprod 21:801–806

    Article  PubMed  CAS  Google Scholar 

  • Woolley SM, Wissman AM, Rubel EW (2001) Hair cell regeneration and recovery of auditory thresholds following aminoglycoside ototoxicity in Bengalese finches. Hear Res 153:181–195

    Article  PubMed  CAS  Google Scholar 

  • Zakon HH (1998) The effects of steroid hormones on electrical activity of excitable cells. Trends Neurosci 21:202–207

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Brandon Warren, Karin Lent, and Mike Famulare for technical assistance, Kristen Richards Preble for animal care, Jason Sanchez for threshold verification, and members of the Brenowitz and Rubel laboratories for constructive discussion and support. This work was supported by the NIH/NIDCD Grants DC000033, DC003829, DC004661, the Seattle Chapter of Achievement Rewards for College Scientists Foundation (MLC), and the Washington Research Foundation (MLC). All procedures were approved by the Institutional Animal Care and Use Committee at the University of Washington, Seattle.

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Authors and Affiliations

  1. Neurobiology and Behavior Graduate Program, University of Washington, Mail Stop 351525, Seattle, WA, 98195, USA

    Melissa L. Caras

  2. Virginia Merrill Bloedel Hearing Research Center, University of Washington, Mail Stop 357923, Seattle, WA, 98195, USA

    Edwin W. Rubel

  3. Virginia Merrill Bloedel Hearing Research Center, University of Washington, Seattle, WA, 98195, USA

    Eliot Brenowitz & Edwin W. Rubel

  4. Department of Psychology, University of Washington, Mail Stop 351525, Seattle, WA, 98195, USA

    Eliot Brenowitz & Edwin W. Rubel

  5. Department of Biology, University of Washington, Seattle, WA, 98195, USA

    Eliot Brenowitz

  6. Department of Otolaryngology-HNS, University of Washington, Seattle, WA, 98195, USA

    Edwin W. Rubel

  7. Department of Physiology and Biophysics, University of Washington, Seattle, WA, 98195, USA

    Edwin W. Rubel

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  1. Melissa L. Caras
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  2. Eliot Brenowitz
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Correspondence to Edwin W. Rubel.

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Caras, M.L., Brenowitz, E. & Rubel, E.W. Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A 196, 581–599 (2010). https://doi.org/10.1007/s00359-010-0545-1

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