Skip to main content
SpringerLink
Log in

Functional differences in forebrain auditory regions during learned vocal recognition in songbirds

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Converging evidence implicates the auditory forebrain regions caudal medial mesopallium (formerly cmHV) and caudal medial nidopallium in the perceptual processing of conspecific vocalizations in songbirds. Little is known however, about more specific processing within these regions especially during song-based perceptual behaviors. One hallmark of the caudal medial mesopallium and caudal medial nidopallium, areas analogous to mammalian secondary auditory cortical structures, is their robust expression of the immediate-early-gene zenk in response to conspecific songs. Using European starlings operantly trained to recognize the songs of individual conspecifics, we show that the levels and patterns of zenk protein expression in the caudal medial nidopallium and caudal medial mesopallium differ when song recognition demands are placed on the system. In the caudal medial mesopallium, expression is significantly elevated above basal levels during the recognition of familiar songs, the acquisition of novel associations for familiar songs, and the acquisition of novel song discriminations. In the caudal medial nidopallium, however, expression is significantly elevated above basal levels only during the acquisition of novel song discriminations. The results directly implicate the caudal medial nidopallium and caudal medial mesopallium in at least a portion of the auditory processes underlying vocal recognition. Moreover, the observed differences between these regions imply the functional localization (or at least the concentration) of different auditory processing mechanisms within the caudal medial nidopallium and the caudal medial mesopallium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–d
Fig. 2
Fig. 3a, b
Fig. 4a–c
Fig. 5a, b

Similar content being viewed by others

Notes

  1. See Reiner et al. 2004 for recent changes in avian brain nomenclature

Abbreviations

CM:

Caudal mesopallium

CLM:

Caudal lateral mesopallium

CMM:

Caudal medial mesopallium

NCM:

Caudal medial nidopallium

References

  • Adret-Hausberger M, Jenkins PF (1988) Complex organization of the warbling song in starlings. Behaviour 107:138–156

    Google Scholar 

  • Bolhuis JJ, Zijlstra GG, den Boer-Visser AM, Van Der Zee EA (2000) Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc Natl Acad Sci U S A 97:2282–2285

    Article  CAS  PubMed  Google Scholar 

  • Bonke D, Scheich H, Langner G (1979) Responsiveness of units in the auditory neostriatum of the Guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli. I. Tonotopy and functional zones. J Comp Physiol A 132:243–255

    Google Scholar 

  • Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695–701

    Article  CAS  PubMed  Google Scholar 

  • Chaiken M, Böhner J, Marler P (1993) Song acquisition in European starlings, Sturnus vulgaris: a comparison of the songs of live-tutored, tape-tutored, untutored, and wild-caught males. Anim Behav 46:1079–1090

    Article  Google Scholar 

  • Chew SJ, Mello CV, Nottebohm F, Jarvis E, Vicario DS (1995) Decrements in auditory responses to a repeated conspecific song are long lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci U S A 92:3406–3410

    CAS  PubMed  Google Scholar 

  • Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474–476

    Article  CAS  PubMed  Google Scholar 

  • Eens M, Pinxten M, Verheyen RF (1989) Temporal and sequential organization of song bouts in the European starling. Ardea 77:75–86

    Google Scholar 

  • Eens M, Pinxten M, Verheyen RF (1991) Organization of song in the European starling: species-specificity and individual differences. Belg J Zool 121:257–278

    Google Scholar 

  • Falls (1982) Individual recognition by sounds in birds. In: Kroodsma DE, Miller EH (eds) Acoustic communication in birds, vol 2. Academic Press, New York, pp 237–278

  • Gentner TQ, Hulse SH (1998) Perceptual mechanisms for individual recognition in European starlings (Sturnus vulgaris). Anim Behav 56:579–594

    Article  PubMed  Google Scholar 

  • Gentner TQ, Hulse SH (2000) Perceptual classification based on the component structure of song in European starlings. J Acoust Soc Am 107:3369–3381

    Article  CAS  PubMed  Google Scholar 

  • Gentner TQ, Margoliash D (2003a) Neuronal populations and single cells representing learned auditory objects. Nature 424:669–674

    Article  CAS  PubMed  Google Scholar 

  • Gentner TQ, Margoliash D (2003b) Song recognition neurons in awake birds. Soc Neurosci Abs 33:942.13

    Google Scholar 

  • Gentner TQ, Hulse SH, Bentley GE, Ball GF (2000) Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J Neurobiol 42:117–133

    Article  CAS  PubMed  Google Scholar 

  • Gentner TQ, Hulse SH, Duffy D, Ball GF (2001) Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48–58

    Article  CAS  PubMed  Google Scholar 

  • Grace JA, Amin N, Singh NC, Theunissen FE (2003) Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89:472–487

    PubMed  Google Scholar 

  • Guzowski JF, Setlow B, Wagner EK, McGaugh L (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089–5098

    CAS  PubMed  Google Scholar 

  • Hausberger M (1997) Social influences on song acquisition and sharing in the European starling (Sturnus vulgaris). In: Snowden C, Hausberger M (eds) Social influences on vocal development. Cambridge University Press, Cambridge, pp 128–156

    Google Scholar 

  • Hausberger M, Cousillas H (1995) Categorization in birdsong: from behavioural to neuronal responses. Behav Processes 35:83–91

    Article  Google Scholar 

  • Hulse SH (1995) The discrimination-transfer procedure for studying auditory perception and perceptual invariance in animals. In: Klump GM, Dooling RJ, Fay RR, Stebbins WC (eds) Methods in comparative psychoacoustics, vol 10. Birkhäuser, Basel, Switzerland, pp 319–330

  • Jarvis ED, Mello CV, Nottebohm F (1995) Associative learning and stimulus novelty influence the song-induced expression of an immediate early gene in the canary forebrain. Learn Mem 2:62–80

    CAS  PubMed  Google Scholar 

  • Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif-268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289–296

    Article  CAS  PubMed  Google Scholar 

  • Leppelsack HJ (1983) Analysis of song in the auditory pathway of songbirds. In: Evert JP, Capranica BR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 783–799

    Google Scholar 

  • Leppelsack HJ, Vogt M (1976) Responses of auditory neurons in forebrain of a songbird to stimulation with species-specific sounds. J Comp Physiol A 107:263–274

    Google Scholar 

  • Macmillan NA, Creelman CD (1991) Detection theory: a user’s guide. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 189:667–674

    Article  CAS  Google Scholar 

  • Mello CV, Ribeiro S (1998) ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426–438

    Article  CAS  PubMed  Google Scholar 

  • Mello CV, Vicario DS, Clayton DF (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 89:6818–6822

    CAS  PubMed  Google Scholar 

  • Mello CV, Nottebohm F, Clayton D (1995) Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene’s response to that song in zebra finch telencephalon. J Neurosci 15:6919–6925

    CAS  PubMed  Google Scholar 

  • Müller CM, Leppelsack HJ (1985) Feature extraction and tonotopic organization in the avian forebrain. Exp Brain Res 59:587–599

    PubMed  Google Scholar 

  • Reiner A et al (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414

    Article  PubMed  Google Scholar 

  • Ribeiro S, Cecchi GA, Magnasco MO, Mello CV (1998) Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 21:359–371

    Article  CAS  PubMed  Google Scholar 

  • Sen K, Theunissen FE, Doupe AJ (2001) Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86:1445–1458

    CAS  PubMed  Google Scholar 

  • 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 Biol Sci 269:2479–2485

    Article  PubMed  Google Scholar 

  • Stoddard PK (1996) Vocal recognition of neighbors by territorial passerines. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 356-374

  • Stripling R, Volman SF, Clayton DF (1997) Response modulation in the zebra finch neostriatum: relationship to nuclear gene expression. J Neurosci 17:3883–3893

    CAS  PubMed  Google Scholar 

  • Terpstra NJ, Bolhuis JJ, den Boer-Visser AM (2004) An analysis of the neural representation of birdsong memory. J Neurosci 24:4971–4977

    Article  CAS  PubMed  Google Scholar 

  • Theunissen FE, Doupe AJ (1998) Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches. J Neurosci 18:3786–3802

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the NIH R0135467 to G.F.B., and DC00389 to T.Q.G. All experiments reported here comply with the Principles of animal care, publication No. 86-23, revised 1985 of the National Institutes of Health, and with the current applicable laws of the United States of America.

Author information

Author notes

  1. Timothy Q. Gentner

    Present address: Department of Psychology, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, 92093-0109, USA

Authors and Affiliations

  1. Department of Organismal Biology and Anatomy, University of Chicago, 1027 E. 57th Street, Chicago, IL, 60637, USA

    Timothy Q. Gentner

  2. Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD, 21218, USA

    Stewart H. Hulse & Gregory F. Ball

Authors
  1. Timothy Q. Gentner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stewart H. Hulse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gregory F. Ball
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy Q. Gentner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gentner, T.Q., Hulse, S.H. & Ball, G.F. Functional differences in forebrain auditory regions during learned vocal recognition in songbirds. J Comp Physiol A 190, 1001–1010 (2004). https://doi.org/10.1007/s00359-004-0556-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-004-0556-x

Keywords

Search

Navigation