Neural Mechanisms of Birdsong Memory

Johan J. Bolhuis

Sanne Moorman

Thijs Zandbergen

Principal collaborators:

Hiroko Eda-Fujiwara (Tokyo, Japan)

Claudio Mello (Oregon, USA)

Birdsong project News:

NEW: ‘Birdsong neurolinguistics: songbird context-free grammar claim is premature’, by Beckers, Bolhuis, Okanoya & Berwick in NeuroReport.

NEW: Trends Cogn. Sci. paper 'Songs to syntax: The linguistics of birdsong', by Berwick, Okanoya, Beckers & Bolhuis

 

NEW: Twitter Evolution - Cover article in Nature Reviews Neuroscience by Bolhuis, Okanoya and Scharff on the parallels between birdsong and human speech

[NRNcover]

NEW: To sleep, perchance to learn? Article in Proc. Roy. Soc. B by Gobes, Zandbergen & Bolhuis showing song learning-related brain activity during sleep in zebra finches

NEW: Bolhuis, J.J. & Eda-Fujiwara, H. (2010) Birdsong and the brain: The syntax of memory. NeuroReport 21, 395-398.

 

 

Brain mechanisms of birdsong memory – An outline of our research

We study the neural mechanisms of learning and memory through an analysis of birdsong learning in zebra finches. The process through which young songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorisation followed by a period during which the individual develops its own vocalisations.

image004.jpg

The avian ‘song system’ (figure above), a network of brain nuclei, is the likely neural substrate for the second phase of sensorimotor learning. In contrast, the neural representation of song memory acquired in the first phase is most probably localised outside the song system, notably in the NCM and CMM, regions within the avian equivalent of auditory association cortex (Bolhuis & Gahr, 2006).

In zebra finches, neuronal activation (measured as expression of immediate early genes) in the NCM correlated with the number of song elements that a male had learned from its tutor, suggesting that the NCM may be (part of) the neural substrate for stored tutor song (Fig. a below) (Bolhuis et al., 2000, 2001; Terpstra et al., 2004). Female zebra finches do not sing, but nevertheless they can learn the characteristics of male song, and they develop a perceptual preference for their father’s song over novel song. Females that were re-exposed to their father’s  song showed increased neuronal activation in the CMM only, compared to novel song. Thus, the CMM may be (part of) the neural substrate for the representation of the memory of their father’s song (Terpstra et al, 2006 - Fig. c below).

image005.jpg

 

Lesions to the NCM in zebra finch males impaired recognition of tutor song, but did not affect production of the bird’s own song (Gobes & Bolhuis, 2007). Thus, in both humans and songbirds the cognitive systems of vocal production and auditory recognition memory are subserved by distinct brain regions.

For a recent review, see: Bolhuis, J.J. & Gahr, M. (2006) Neural mechanisms of birdsong memory. Nature Reviews Neuroscience, 7,  347-357.

Publications

  • Bolhuis, J.J., Van Mil, D. & Houx, B.B. (1999) Song learning with audiovisual compound stimuli in the zebra finch. Anim. Behav., 58, 1285-1292.
  • Bolhuis, J.J., Zijlstra, G.G.O., Den Boer-Visser, A.M. & Van der Zee, E.A. (2000) Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. USA, 97, 2282-2285. [pdf file ]
  • Bolhuis, J.J., Hetebrij, E., Den Boer-Visser, A.M., De Groot, J.H & Zijlstra, G.G.O. (2001) Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches. Eur. J. Neurosci., 13, 2165-2170.
  • Bolhuis, J.J. & Macphail, E.M. (2001) A critique of the neuroecology of learning and memory. Trends Cogn. Sci. 5, 426-433.
  • Riebel, K., Smallegange, I.M., Terpstra, N.J. & Bolhuis, J.J. (2002) Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc. Roy. Soc. Lond., B. 269, 729-733.
  • Eda-Fujiwara, H., Satoh, R., Bolhuis, J.J. & Kimura, T. (2003) Neuronal activation in female budgerigars is localized and related to male song complexity. Eur. J. Neurosci., 17, 149-154.
  • Bolhuis, J.J. & Eda-Fujiwara, H. (2003) Bird brains and songs: neural mechanisms of birdsong perception and memory. Anim. Biol., 53, 129-145.
  • Terpstra, N.J., Bolhuis, J.J. & den Boer-Visser, A.M. (2004) An analysis of the neural representation of birdsong memory. J. Neurosci., 24, 4971-4977.
  • Terpstra, N.J., Bolhuis, J.J., den Boer-Visser, A.M. & ten Cate, C. (2005).  Neuronal activation related to auditory perception in the brain of a non-songbird, the ring dove. J. Comp. Neurol., 488, 342-351.
  • Terpstra, N.J., Bolhuis, J.J., Riebel, K., Van der Burg, J.M.M. & den Boer-Visser, A.M. (2006) Localised Brain Activation Specific to Auditory Memory in a Female Songbird. J. Comp. Neurol., 494, 784-791.
  • Bolhuis, J.J. & Gahr, M. (2006) Neural mechanisms of birdsong memory. Nature Rev. Neurosci., 7, 347-357
  • Gobes, S.M.H.  & Bolhuis, J.J. (2007) Bird song memory: A neural dissociation between song recognition and production. Curr. Biol., 17, 789-793.
  • Bolhuis, J.J. (2008) Chasin’ the trace: The neural substrate of bird song memory. In: Neuroscience of Birdsong (H. P. Zeigler & P. Marler, Eds.) Cambridge University Press, pp. 269-279.
  • Boumans, T., Gobes, S.M.H., Poirier, C., Theunissen, F.E., Vandersmissen, L., Pintjens, W., Verhoye, M., Bolhuis, J.J. & Van der Linden, A. (2008) Functional MRI of auditory responses in the zebra finch forebrain reveals a hierarchical organisation based on signal strength but not selectivity. PLoS One, 3, e3184.
  • Bolhuis, J.J. & Wynne, C.D.L. (2009) Can evolution explain how minds work? Nature, 458, 832-833.
  • Gobes, S.M.H., ter Haar, S.M., Vignal, C., Vergne, A.L., Mathevon, N. & Bolhuis, J.J. (2009) Differential responsiveness in brain and behavior to sexually dimorphic long calls in male and female zebra finches. J. Comp. Neurol., 516,312-320.
  • Bolhuis, J.J. & Eda-Fujiwara, H. (2010) Birdsong and the brain: The syntax of memory. NeuroReport 21, 395-398.
  • Gobes, S.M.H., Zandbergen, M.A. & Bolhuis, J.J. (2010) Memory in the making: Localized brain activation related to song learning in young songbirds. Proc. Roy. Soc. Lond., B., 277, 3343-3351.
  • Bolhuis, J.J., Okanoya, K. & Scharff, C. (2010) Twitter evolution: Converging mechanisms in birdsong and human speech. Nature Reviews Neuroscience, 11, 747-759.
  • Moorman, S., Mello, C.V. & Bolhuis, J.J. (2011). From songs to synapses: Molecular mechanisms of birdsong memory. BioEssays, 33, 377-385
  • Berwick, R.C., Okanoya, K, Beckers, G.J.L. & Bolhuis, J.J. (2011) Songs to syntax: The linguistics of birdsong. Trends in Cognitive Sciences, 15, 113-121.
  • Beckers, G.J.L., Bolhuis, J.J., Okanoya, K. &  Berwick, R.C. (2012) Birdsong neurolinguistics: Songbird context-free grammar claim is premature. NeuroReport, 23, 139-145.




 

For information about the avian brain, and links to other birdsong labs: www. avianbrain.org

 

 

 

 

 

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