Advertisement

Journal of Ornithology

, Volume 148, Supplement 2, pp 231–239 | Cite as

Experience-dependence of neural responses to social versus isolate conspecific songs in the forebrain of female Zebra Finches

  • Mark E. HauberEmail author
  • Sarah M. N. Woolley
  • Frédéric E. Theunissen
Original Article

Abstract

Early exposure to conspecific song influences the ontogeny of behavioural discrimination between social and isolate songs of males in non-singing female Zebra Finches (Taeniopygia guttata). We explored the potential neural basis of this behavioural plasticity in song preference of female Zebra Finches, reared by both parents in a conspecific colony (controls) or by mothers only in sound-attenuation chambers (father-absent treatment). Comparing extracellular recordings of auditory neurons in the primary auditory forebrain area Field L showed that single units consistently responded with greater response strengths to male songs, over the synthetic stimuli of both frequency-matched pure tone assemblages and reversed conspecific songs, irrespective of females’ ontogenetic treatment. Contrary to expectations, consistent response selectivity for social versus isolate Zebra Finch songs was detected from neurons only in father-absent females and not in control subjects. These results based on statistical analyses of data from single neurons were confirmed by a contingency analysis that used female subjects as independent datapoints. Our findings suggest that differences in the early social and/or auditory experience affect the neurophysiological responses to specific classes of male songs in auditory forebrain neurons of female Zebra Finches. Contrary to expectations, patterns of neuronal discrimination in the Field L complex do not parallel patterns of experience-dependent behavioural discrimination between social and isolate conspecific songs.

Keywords

Conspecific Forebrain Naïve Oscine Recognition systems 

Notes

Acknowledgments

For assistance, comments, and discussions we are grateful to N. Amin, D. Campbell, T. Fremouw, F. Kubke, E. Lacey, B. Raymond, S. Shaevitz, M. Wild, and two referees. This study was funded by grants from the National Institutes of Health, the UC Berkeley Field Station for Behavioral Research, the University of Auckland Research Council, and the New Zealand Marsden Fund. All animal ethics protocols were approved by IACUC at UC Berkeley. We are grateful to K. Sockman and E. MacDougall-Shackleton for inviting us to participate in the “Flexibility in mating signals and mate choice: ultimate and proximate bases” Symposium at the 24th International Ornithological Congress, Hamburg, Germany.

References

  1. Amin N, Grace GA, Theunissen FE (2004) Neural response to bird’s own song and tutor song in the zebra finch field L and caudal mesopallium. J Comp Physiol A 190:469–489CrossRefGoogle Scholar
  2. Amin N, Doupe A, Theunissen FE (2007) Development of selectivity for natural sounds in the songbird auditory forebrain. J Neurophysiol 97:3517–3531PubMedCrossRefGoogle Scholar
  3. Bailey DJ, Rosebush JC, Wade J (2002) The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J Neurobiol 52:43–51PubMedCrossRefGoogle Scholar
  4. Bailey DJ, Wade J (2003) Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Mol Brain Res 116:147–154PubMedCrossRefGoogle Scholar
  5. Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in birds. Trends Ecol Evol 20:143–149PubMedCrossRefGoogle Scholar
  6. Bolhuis JJ, Gahr M (2006) Neural mechanisms of birdsong memory. Nat Rev Neurosci 7:347–357PubMedCrossRefGoogle Scholar
  7. Braaten RF, Reynolds K (1999) Auditory preference for conspecific song in isolation-reared zebra finches. Anim Behav 58:105–111PubMedCrossRefGoogle Scholar
  8. Brenowitz EA, Beecher MD (2005) Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 28:127–132PubMedCrossRefGoogle Scholar
  9. Cardin JA, Schmidt MF (2003) Song system auditory responses are stable and highly tuned during sedation, rapidly modulated and unselective during wakefulness, and suppressed by arousal. J Neurophysiol 90:2884–2899PubMedCrossRefGoogle Scholar
  10. Chew SJ, Vicario DS, Nottebohm F (1996) A large-capacity memory system that recognizes the calls and songs of individual birds. Proc Natl Acad Sci USA 93:1950–1955PubMedCrossRefGoogle Scholar
  11. Cousillas H, Richard J-P, Mathelier M, Henry L, George I, Hausberger M (2004) Experience-dependent neuronal specialization and functional organization in the central auditory area of a songbird. Eur J Neurosci 19:3343–3376PubMedCrossRefGoogle Scholar
  12. Cousillas H, George I, Mathelier M, Richard J-P, Henry L, Hausberger M (2006) Social experience influences the development of a central auditory area. Naturwissenschaften 93:588–596PubMedCrossRefGoogle Scholar
  13. Fortune ES, Margoliash D (2004) Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata). J Comp Neurol 325:388–404CrossRefGoogle Scholar
  14. Gentner TZ, Margoliash D (2003) Neuronal populations and feature detectors representing learned auditory objects. Nature 424:669–674PubMedCrossRefGoogle Scholar
  15. Grace JA, Amin NA, Singh NC, Theunissen FE (2003) Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89:472–487PubMedCrossRefGoogle Scholar
  16. Hauber ME, Sherman PW (2001) Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci 24:609–616PubMedCrossRefGoogle Scholar
  17. Hauber ME, Cassey P, Woolley SMN, Theunissen FE (2007) Neurophysiological response selectivity for conspecific songs over synthetic sounds in the auditory forebrain of non-singing female songbirds. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:765–774PubMedCrossRefGoogle Scholar
  18. Hsu A, Woolley SMN, Fremouw T, Theunissen FE (2004) Modulation and phase spectrum of natural sounds enhance neural discrimination performed by single auditory neurons. J Neurosci 24:9201–9221PubMedCrossRefGoogle Scholar
  19. Janata P, Margoliash D (1999) Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci 19:5108–5118PubMedGoogle Scholar
  20. Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu W-C (2001) seudoreplication in playback experiments, revisited a decade later. Anim Behav 61:1029–1033CrossRefGoogle Scholar
  21. Lauay C, Gerlach NM, Adkins-Regan E, Devoogd TJ (2004) Female zebra finches require early song exposure to prefer high-quality song as adults. Anim Behav 68:1249–1255CrossRefGoogle Scholar
  22. Lauay C, Komorowski RW, Beaudin AE, DeVoogd TJ (2005) Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song. J Comp Neurol 487:119–126PubMedCrossRefGoogle Scholar
  23. MacDougall-Shackleton SA, Hulse SH, Ball GF (1998) Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 9:3047–3052PubMedCrossRefGoogle Scholar
  24. Maney DL, MacDougall-Shackleton EA, MacDougall-Shackleton SA, Ball GF, Hahn TP (2003) Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J Comp Physiol A 189:667–674CrossRefGoogle Scholar
  25. Nelson DA, Marler PA (2005) Do birds’ nestmates learn the same songs? Anim Behav 69:1007–1010CrossRefGoogle Scholar
  26. Phan ML, Pytte CL, Vicario DS (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci USA 103:1088–1093PubMedCrossRefGoogle Scholar
  27. Pytte CL, Suthers RA (1999) A bird’s own song contributes to conspecific sang perception. Neuroreport 10:1773–1778PubMedCrossRefGoogle Scholar
  28. Reiner A, Perkel DJ, Bruce L, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter GF, Wild M, Ball GF, Durand S, Gunturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414PubMedCrossRefGoogle Scholar
  29. Riebel K (2000) Early exposure to song leads to repeatable preferences for male song in female zebra finches. Proc R Soc Lond B 267:2553–2558CrossRefGoogle Scholar
  30. Riebel K (2003a) The ‘mute’ sex revisited: vocal production and perception learning in female songbirds. Adv Study Behav 33:49–86CrossRefGoogle Scholar
  31. Riebel K (2003b) Developmental influences on song perception in female zebra finches, Taeniopygia guttata: is there a sensitive phase for song preference learning? Anim Biol 53:73–87CrossRefGoogle Scholar
  32. Riebel K, Smallegange IM (2003) Does zebra finch (Taeniopygia guttata) preference for the (familiar) father’s song generalize to the songs of unfamiliar brothers? J Comp Psychol 117:61–66PubMedCrossRefGoogle Scholar
  33. Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ (2002) Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc R Soc Lond B 269:729–733CrossRefGoogle Scholar
  34. Riebel K, Hall ML, Langmore NE (2005) Female songbirds still struggling to be heard. Trends Ecol Evol 20:419–420PubMedCrossRefGoogle Scholar
  35. Seddon N (2005) Ecological adaptation and species recognition drives vocal evolution in Neotropical suboscine birds. Evolution 59:200–215PubMedGoogle Scholar
  36. Sockman KW, Gentner TQ, Ball GF (2002) Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc R Soc Lond B 269:2479–2485CrossRefGoogle Scholar
  37. Terpstra NJ, Bolhuis JJ, Riebel K, van der Burg JMM, den Boer-Visser AM (2006) Localized brain activation specific to auditory memory in a female songbird. J Neurobiol 494:784–791Google Scholar
  38. Theunissen FE, Sen K, Doupe AJ (2000) Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J Neurosci 20:2315–2331PubMedGoogle Scholar
  39. Tomaszycki ML, Sluzas EM, Sundberg KA, Newman SW, DeVoogd TJ (2006) Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: effects of rearing environment. J Neurobiol 66:1175–1182PubMedCrossRefGoogle Scholar
  40. Wang L, Narayan R, Grana G, Shamir M, Sen K (2007) Cortical discrimination of complex natural stimuli: can single neurons match behavior? J Neurosci 27:582–589PubMedCrossRefGoogle Scholar
  41. Wild JM (1995) Convergence of somatosensory and auditory projections in the avian torus semicircularis, including the central auditory nucleus. J Comp Neurol 358:465–486PubMedCrossRefGoogle Scholar
  42. Williams H (1990) Models for song learning in the zebra finch: fathers or others. Anim Behav 39:745–757CrossRefGoogle Scholar
  43. Williams H, Kilander K, Sotanski ML (1993) Untutored song, reproductive success and song learning. Anim Behav 45:695–705CrossRefGoogle Scholar
  44. Woolley SMN, Casseday JH (2004) Response properties of single neurons in the zebra finch auditory midbrain: response patterns, frequency coding, intensity coding and spike latencies. J Neurophysiol 91:136–151PubMedCrossRefGoogle Scholar
  45. Woolley SMN, Casseday JH (2005) Processing of modulated sounds in the zebra finch auditory midbrain: responses to noise, frequency sweeps and sinusoidal amplitude modulations. J Neurophysiol 94:1143–1157PubMedCrossRefGoogle Scholar
  46. Woolley SMN, Gill P, Theunissen FE (2006) Stimulus-dependent auditory tuning results in synchronized population coding of vocalizations in the songbird midbrain. J Neurosci 26:2499–2512PubMedCrossRefGoogle Scholar
  47. Woolley SMN, Fremouw TE, Hsu A, Theunissen FE (2005) Spectro-temporal modulation tuning as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8:1371–1379PubMedCrossRefGoogle Scholar
  48. Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2007

Authors and Affiliations

  • Mark E. Hauber
    • 1
    Email author
  • Sarah M. N. Woolley
    • 2
  • Frédéric E. Theunissen
    • 3
  1. 1.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  2. 2.Department of PsychologyColumbia UniversityNew York CityUSA
  3. 3.Department of Psychology and Helen Wills Neuroscience InstituteUniversity of CaliforniaBerkeleyUSA

Personalised recommendations