Dopaminergic system in birdsong learning and maintenance

Abstract

Dopamine function in birdsong has been studied extensively in recent years. Several song and auditory nuclei are innervated by midbrain dopaminergic fibers and contain neurons with various dopamine receptors. During sexually motivated singing, activity of midbrain dopaminergic neurons in the ventral tegmental area and dopamine release in the striatal Area X, involved in song learning and maintenance, are higher. In this review we provide an overview of the dopaminergic system and neurotransmission in songbirds and the outline of possible involvement of dopamine in control of song learning, production, and maintenance. Based on both behavioral and computational biology data, we describe several models of song learning and the proposed role of dopamine in them. Special attention is given to possible role of dopamine in incentive salience (wanting) and reward prediction error signaling during song learning and maintenance, as well as the role of dopamine-mediated synaptic plasticity in reward processing. Finally, the role of dopamine in determination of personality traits in relation to birdsong is discussed.

Fig. 1

Expression of dopamine receptors in adult zebra finch male brain. Calibration bar shows pseudocolour coding of the mRNA signal strength on autoradiograms of sagittal sections. In the first raw are representative autoradiograms of the D1-like dopamine receptor family, in the second row the D2-like dopamine receptor family. Drawing delineates some of the brain regions on the sections with the focus on song nuclei. Abbreviations: A – arcopallium, DM - dorsal medial nucleus of the midbrain, DNH - dorsal nucleus of the hyperpallium, GP - globus pallidus, H – hyperpallium, HVC - nucleus HVC (a letter based name), IH - interstitial layer of the hyperpallium, LArea X - lateral part of AreaX of striatum, LMAN - lateral magnocellular nucleus of anterior nidopallium, L2 - Field L2, MLd - dorsal part of the lateral mesencephalic nucleus, MV - ventral mesopallium, RA - robust nucleus of the arcopallium, SVZ - subventricular zone, TeO - optic tectum

Fig 2

Birdsong reinforcement learning scheme. Red arrows show glutamatergic input; blue arrows show GABA-ergic input; green arrows show dopaminergic input; black arrows show other connections with unspecified input. D1A, D1B, D2, and D3 are dopamine receptors present and/or present at higher levels in the song nucleus than in the immediate surrounding area (bold). Based on Doya and Sejnowski (1995, and Fiete et al. (2007).

Fig. 3

A possible scheme of the cascades involved in dopamine modulated synaptic plasticity in the AreaX, based on mammalian data. DA acting through the D1-like receptors elevates the level of cAMP and stimulates protein kinase A (PKA) (Stoof and Kebabian, 1981) which in turn activates phosphorylation of dopamine and cAMP-regulated phosphoprotein (DARPP-32). DA acting through the D2-like receptors inhibits PKA (Centonze et al., 2001) and reduces DARPP-32 phosphorylation (Gould and Manji, 2005). DARPP-32 plays a central role in dopaminergic and glutamatergic signaling, and is integrating the activity of these two pathways. In elevated calcium levels the dephosphorylated DARPP-32 leads to dephosphorylation of glutamate receptors while the activated calcium calmodulin-dependent protein kinase II (CaMKII) increases the phosporylation of glutamate receptors (Worgotter and Porr, 2005). The calcium influx through NMDA receptors leads to rapid phosphorylation of MAPK/ERK and to activation of cAMP response element binding protein (CREB) (West et al., 2002; Zhou et al., 2009). CREB can be activated also by PKA through MAPK/ERK (Gerits et al., 2008). CREB and the ternary complex factor Elk-1can increase the transcription of many genes, including c-fos and ZENK (Davis et al., 2000).