Journal of Comparative Physiology A

, Volume 193, Issue 2, pp 201–215 | Cite as

Seasonal variation in avian auditory evoked responses to tones: a comparative analysis of Carolina chickadees, tufted titmice, and white-breasted nuthatches

  • Jeffrey R. Lucas
  • Todd M. Freeberg
  • Glenis R. Long
  • Ananthanarayan Krishnan
Original Paper

Abstract

We tested for seasonal plasticity of the peripheral auditory system of three North American members of the Sylvioidea: Carolina chickadees (Poecile carolinensis), tufted titmice (Baeolophus bicolor), and white-breasted nuthatches (Sitta carolinensis). We measured three classes of auditory evoked responses (AER) to tone stimuli: sustained receptor/neural responses to pure-tone condensation waveforms, the frequency-following response (FFR), and the earliest peak of the AER to stimulus onset (tone onset response). Seasonal changes were detected in all classes of AERs in chickadees and nuthatches. Seasonal changes in titmice were restricted to the tone onset response. Interestingly, changes detected in chickadees (and to a lesser extent in titmice) were generally in an opposite direction to changes seen in nuthatches, with chickadees exhibiting greater amplitude AER responses in the spring than in winter, and nuthatches exhibiting greater amplitude AER responses in winter than in spring. In addition, the seasonal differences in the sustained responses tended to be broad-band in the chickadees but restricted to a narrower frequency range in nuthatches. In contrast, seasonal differences in the onset response were over a broader frequency range in titmice than in chickadees and nuthatches. We discuss some possible mechanistic and functional explanations for these seasonal changes.

Keywords

Auditory evoked response (AER) Frequency following response (FFR) Seasonality Bird hearing Vocal complexity 

List of abbreviations

AER

Auditory evoked response

CM

Cochlear microphonic

FFR

Frequency following response

FFR2

Second harmonic of the frequency following response

CM + FFR

Sustained response including both cochlear microphonic and frequency following response

Notes

Acknowledgments

Thanks to Ben Fanson, Kerry Fanson, Ken Henry and Mark Nolen for feedback on the manuscript. Ken Henry helped with system calibration. This work was approved 18 June, 1999 by the Purdue University Animal Care Committee under IACUC no. 99–003. Todd M. Freeberg wishes to acknowledge postdoctoral support by an NIH training grant to the Department of Audiology and Speech Sciences at Purdue University that made this research possible.

References

  1. Ball GF (1999) The neuroendocrine basis of seasonal changes in vocal behavior among songbirds. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, pp 213–253Google Scholar
  2. Ball GF, Riters LV, Balthazart J (2002) Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front Neuroendocrinol 23:137–178PubMedCrossRefGoogle Scholar
  3. Bekesy G (1950) D-C potentials and energy balance of the cochlear partition. J Acoust Soc Am 22:576–582Google Scholar
  4. Bloomfield LL, Phillmore LS, Weisman RG, Sturdy CB (2005) Note types and coding in parid vocalizations: III. The chick-a-dee call of the Carolina chickadee (Poecile carolinensis). Can J Zool 83:820–833CrossRefGoogle Scholar
  5. Bottjer SW, Johnson F (1997) Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol 33:602–618PubMedCrossRefGoogle Scholar
  6. Brenowitz EA (2004) Plasticity of the adult avian song control system. Ann NY Acad Sci 1016:560–585PubMedCrossRefGoogle Scholar
  7. Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132PubMedCrossRefGoogle Scholar
  8. Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses (ABR) in adult budgerigars (Melopsittacus undulates). J Acoust Soc Am 112: 999–1008PubMedCrossRefGoogle Scholar
  9. Britten-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 118:314–321CrossRefGoogle Scholar
  10. Brown-Borg HM, Beck MM, Jones TA (1987) Origin of peripheral and brainstem auditory responses in the white leghorn chick. Comp Biochem Physiol 88A:391–396CrossRefGoogle Scholar
  11. Calhoun S, Hulse SH, Braaten RF, Page SC, Nelson RJ (1993) Responsiveness to conspecific and alien song by canaries (Serinus canaria) and European starlings (Sturnus vulgaris) as a function of photoperiod. J Comp Psychol 107:235–241CrossRefGoogle Scholar
  12. Chaplin SB (1974) Daily energetics of the black-capped chickadee, Parus atricapillus, in winter. J Comp Physiol 89:321–330CrossRefGoogle Scholar
  13. Chimento TC, Schreiner CE (1990) Selectively eliminating cochlear microphonic contamination from the frequency-following response. Electroencephalogr Clin Neurophysiol 75:88–96PubMedGoogle Scholar
  14. Christie PJ, Mennill DJ, Ratcliffe LM (2004) Pitch shifts and song structure indicate male quality in the dawn chorus of black-capped chickadees. Behav Ecol Sociobiol 55:341–348CrossRefGoogle Scholar
  15. Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96:638–646CrossRefGoogle Scholar
  16. Cotanche DA (1999) Structural recovery from sound and amino-glycoside damage in the avian cochlea. Audiol Neurootol 4:271–285PubMedCrossRefGoogle Scholar
  17. Cotanche DA, Lee KH, Stone JS, Picard DA (1994) Hair cell regeneration in the bird cochlea following noise damage or ototoxic drug damage. Anat Embryol 189:1–18PubMedCrossRefGoogle Scholar
  18. 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 89:1368–1371PubMedCrossRefGoogle Scholar
  19. 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 114:526–542PubMedCrossRefGoogle Scholar
  20. Del Negro C, Lehongre K, Edeline J (2005) Selectivity of canary HVC neurons for the bird’s own song: modulation by photoperiodic conditions. J Neurosci 25:4952–4963PubMedCrossRefGoogle Scholar
  21. Dooling RJ (1982) Auditory perception in birds. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds. Academic, New York, pp 95–130Google Scholar
  22. Dooling RJ (1992) Hearing in birds. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 545–559Google Scholar
  23. Dooling RJ, Walsh JK (1976) Auditory evoked response correlates of hearing in the parakeet (Melopsittacus undulates). Physiol Psychol 4:224–232Google Scholar
  24. Dooling RJ, Ryals BM, Manabe K (1997) Recovery of hearing and vocal behavior after hair-cell regeneration. Proc Natl Acad Sci USA 94:14206–14210PubMedCrossRefGoogle Scholar
  25. Dooling RJ, Lohr B, Dent ML (2000) Hearing in birds and reptiles. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles. Springer, Berlin Heidelberg, New York, pp 308–359Google Scholar
  26. Ficken MS, Ficken RW, Witkin SR (1978) Vocal repertoire of the black-capped chickadee. Auk 95:34–48Google Scholar
  27. Gardi HN, Merzenich MM, KcKean C (1979) Origins of the scalp-recorded frequency-following responses in the cat. Audiology 18:353–381Google Scholar
  28. Goense JBM, Feng AS (2005) Seasonal changes in frequency tuning and temporal processing in single neurons in the frog auditory midbrain. J Neurobiol 65:22–36PubMedCrossRefGoogle Scholar
  29. Hall JW III (1992) Handbook of auditory-evoked responses. Allyn and Bacon, BostonGoogle Scholar
  30. Hoorman J, Falkenstein M, Hohnsbein J, Blanke L (1992) The human frequency-following response (FFR): normal variability and relation to the click-evoked brainstem response. Hear Res 59:179–188CrossRefGoogle Scholar
  31. Huis in’t Veld F, Osterhammel P, Terkildsen K (1977) Frequency following auditory brainstem responses in man. Scand Audiol 6:27–34PubMedGoogle Scholar
  32. Johnson KL, Nicol TG, Kraus N (2005) Brain stem response to speech: a biological marker of auditory processing. Ear Hear 26:424–434PubMedCrossRefGoogle Scholar
  33. Krishnan A (1999) Human frequency-following responses to two-tone approximations of steady-state vowels. Audiol Neurootol 4:95–103PubMedCrossRefGoogle Scholar
  34. Krishnan A, Parkinson J (2000) Human frequency-following response: representation of tonal sweeps. Audiol Neurootol 5:312–321PubMedCrossRefGoogle Scholar
  35. Lima SL (1992) Vigilance and foraging substrate: antipredatory considerations in a nonstandard environment. Behav Ecol Sociobiol 30:283–289CrossRefGoogle Scholar
  36. Lucas JR, Freeberg TM (2007) “Information” and the chick-a-dee call: communicating with a complex vocal system. In: Otter KA (ed) Ecology and behaviour of chickadees and titmice: an integrated approach. Oxford University Press, New York, (in press)Google Scholar
  37. Lucas JR, Peterson L, Boudinier R (1993) The effects of time constraints and changes in body mass and satiation on the simultaneous expression of caching and diet-choice decisions. Anim Behav 45:639–658CrossRefGoogle Scholar
  38. 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 188:981–992CrossRefGoogle Scholar
  39. Lucas JR, Freeberg TM, Egbert J, Schwabl H (2007) Corticosterone, body mass, and caching rates of Carolina chickadees from disturbed and undisturbed sites. Horm Behav 49:634–643CrossRefGoogle Scholar
  40. Margoliash D (1997) Functional organization of forebrain pathways for song production and perception. J Neurobiol 33:671–693PubMedCrossRefGoogle Scholar
  41. Moore IT, Wingfield JC, Brenowitz EA (2004) Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J Neurosci 24:10182–10185PubMedCrossRefGoogle Scholar
  42. Nottebohm F (1981) A brain for all seasons: Cyclical anatomical changes in song-control nuclei of the canary brain. Science 214:429–436CrossRefGoogle Scholar
  43. Nottebohm F (1999) The anatomy and timing of vocal learning in birds. In: Hauser MD, Konishi M (eds) The design of animal communication. MIT Press, Cambridge, pp. 63–110Google Scholar
  44. Nowicki S, Nelson DA (1990) Defining natural categories in acoustic signals: comparison of 3 methods applied to chick-a-dee call notes. Ethol 86:89–101CrossRefGoogle Scholar
  45. Offutt GC (1965) Behavior of the tufted titmouse before and during the nesting season. Wilson Bull 77:382–387Google Scholar
  46. Phillmore LS, Sturdy CB, Turyk MRM, Weisman RG (2002) Discrimination of individual vocalizations by black-capped chickadees (Poecile atricapilla). Anim Learn Behav 30:43–52PubMedGoogle Scholar
  47. Pravosudov VV, Grubb TC Jr (1993) White-breasted nuthatch (Sitta carolinensis). In: Poole A, Gill F (eds) The birds of North America, No. 54. American Ornithologists’ Union, Washington, pp 1–15Google Scholar
  48. Pyle P (1997) Identification guide to North American birds. Slate Creek Press, BolinasGoogle Scholar
  49. Reeves BJ, Beecher MD, Brenowitz EA (2003) Seasonal changes in avian song control circuits do not cause seasonal changes in song discrimination in song sparrows. J Neurobiol 57:119–129PubMedCrossRefGoogle Scholar
  50. Ritchison G (1983) Vocalizations of the white-breasted nuthatch. Wilson Bull 95:440–451Google Scholar
  51. Saunders JC, Pallone RL, Rosowski JJ (1980) Frequency selectivity in parakeet hearing: behavioral and physiological evidence. In: Nöring R (ed) Proceedings of the 27th International Congress of Ornithology. Deutsche Ornithologen-Gesellschaft, Berlin, pp 615–619Google Scholar
  52. Schroeder DJ, Wiley RH (1983) Communication with shared song themes in tufted titmice. Auk 100:414–424Google Scholar
  53. Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds: a study in molecular evolution. Yale University Press, New HavenGoogle Scholar
  54. Sisneros JA, Bass AH (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23:1049–1058PubMedGoogle Scholar
  55. Sisneros JA, Forlano PM, Deitcher DL, Bass AH (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305:404–407PubMedCrossRefGoogle Scholar
  56. Smith SM (1991) The black-capped chickadee: behavioral ecology and natural history. Comstock, IthacaGoogle Scholar
  57. Smith ST (1972) Communication and other social behavior in Parus carolinensis. Publ Nuttall Ornithol Club 11:1–125Google Scholar
  58. Sohmer H, Pratt H, Kinarti R (1977) Sources of frequency following responses (FFR) in man. Electroencephalogr Clin Neurophysiol 42:656–664PubMedCrossRefGoogle Scholar
  59. Stillman RD, Crow G, Moushegian G (1978) Components of the frequency-following potential in man. Electroencephalogr Clin Neurophysiol 44:438–446PubMedCrossRefGoogle Scholar
  60. Thirakhupt K (1985) Foraging ecology of sympatric parids: individual and populational responses to winter food scarcity. Ph.D. thesis, Purdue University, West Lafayette, IndianaGoogle Scholar
  61. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251–258PubMedCrossRefGoogle Scholar
  62. Woolley SM, Wissman AM, Rubel EW (2001) Hair cell regeneration and recovery of auditory thresholds following aminoglycoside ototoxicity in Bengalese finches. Hear Res 153:181–195PubMedCrossRefGoogle Scholar
  63. Yovanov S, Feng AS (1983) Effects of estradiol on auditory evoked responses from the frog’s auditory midbrain. Neurosci Lett 36:291–297CrossRefGoogle Scholar
  64. Young ED, Sachs MB (1979) Representation of steady-state vowels in the temporal aspects of the discharge patterns of populations of auditory-nerve fibers. J Acoust Soc Am 66:1381–1403PubMedCrossRefGoogle Scholar
  65. Zakon HH (1987) Hormone-mediated plasticity in the electrosensory system of weakly electric fish. Trends Neurosci 10:416–421CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Jeffrey R. Lucas
    • 1
  • Todd M. Freeberg
    • 3
  • Glenis R. Long
    • 4
  • Ananthanarayan Krishnan
    • 2
  1. 1.Department of Biological Sciences, Lilly Hall of Life SciencePurdue UniversityWest LafayetteUSA
  2. 2.Department of Speech, Language, and Hearing SciencesPurdue UniversityWest LafayetteUSA
  3. 3.Department of PsychologyUniversity of TennesseeKnoxvilleUSA
  4. 4.Speech and Hearing Sciences Program, Graduate CenterCity University of New YorkNew YorkUSA

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