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
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).
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).
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,
J.J., Van Mil, D. & Houx, B.B. (1999) Song learning with audiovisual
compound stimuli in the zebra finch. Anim. Behav., 58, 1285-1292.
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 ]
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.
J.J. & Macphail, E.M. (2001) A critique of the neuroecology of
learning and memory. Trends Cogn. Sci. 5, 426-433.
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.
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.
J.J. & Eda-Fujiwara, H. (2003) Bird brains and songs: neural
mechanisms of birdsong perception and memory. Anim. Biol., 53,
N.J., Bolhuis, J.J. & den Boer-Visser, A.M. (2004) An analysis of
the neural representation of birdsong memory. J. Neurosci., 24,
- 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.
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.
J.J. & Gahr, M. (2006) Neural mechanisms of birdsong memory. Nature Rev. Neurosci.,
S.M.H. & Bolhuis, J.J. (2007) Bird song memory: A
neural dissociation between song recognition and production. Curr.
Biol., 17, 789-793.
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.
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.
J.J. & Wynne, C.D.L. (2009) Can evolution explain how minds work? Nature, 458, 832-833.
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.
J.J. & Eda-Fujiwara, H. (2010) Birdsong and the brain: The syntax of
memory. NeuroReport 21, 395-398.
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.
J.J., Okanoya, K. & Scharff, C. (2010) Twitter evolution: Converging
mechanisms in birdsong and human speech. Nature Reviews Neuroscience, 11, 747-759.
S., Mello, C.V. & Bolhuis, J.J. (2011). From
songs to synapses: Molecular mechanisms of birdsong memory. BioEssays,
R.C., Okanoya, K, Beckers, G.J.L. & Bolhuis, J.J. (2011) Songs to
syntax: The linguistics of birdsong. Trends in Cognitive Sciences,
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.