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EDITORIAL FOCUS
; Reynolds et al. 2001; Schultz 2002). Song learning in songbirds has become a key model for the study of motor learning in vertebrates and is hypothesized to be analogous to motor learning in mammals. In particular, area X, a component of the avian striatum in the anterior forebrain pathway (AFP), is essential to song learning and adult song plasticity (e.g., Bottjer et al. 1984; Brainard and Doupe 2000). The AFP is the functional analogue of the mammalian direct pathway of the basal ganglia (Farries and Perkel 2002) and processes song-related auditory feedback. Moreover, it is proposed that some component of the AFP generates an error signal that guides the pathway to produce the target song (Brainard and Doupe 2001). The hypothesis that song learning in birds is analogous to motor learning in mammals is supported further by similarities in physiological mechanisms of which the action of dopamine is a key example: as in mammalian striatum, dopamine in avian area X modulates the excitability of the major, spiny cell type and the strength (long-term depression and potentiation) of excitatory inputs to these cells (Ding and Perkel 2002, 2004; Ding et al. 2003). Now Gale and Perkel add to this growing hypothesis with a study in this issue of the Journal of Neurophysiology (p. 1871-1879) using a technology to explore in real time the release, receptor regulation, and uptake of dopamine in area X. Gale and Perkel reveal that the regulated availability of dopamine in songbird area X shares multiple key features with its mammalian homologue.
Given that the last common ancestor of mammals and birds lived 
290 million years ago (Kardong 1998), not to mention the fact that song system nuclei are often assumed to be highly specialized, the basal ganglia of birds and mammals share a remarkable number of morphological and physiological traits. For example, like the mammalian striatum, area X has GABAergic projection neurons and putative interneuron populations that are cholinergic or contain nitric oxide synthase or parvalbumin (see Farries and Perkel 2002). These four neuron types all possess electrophysiological features characteristic of their mammalian counterparts (Farries and Perkel 2000, 2002). Intriguingly, a fifth neuron type not found in mammalian striatum nonetheless probably represents a mammalian pallidum-like cell that provides within area X an equivalent pathway to the mammalian "direct" striatopallidothalamic pathway (see Farries and Perkel 2002).
The study by Gale and Perkel in this issue layers another dimension to the evidence for functional homology of avian and mammalian striata. The authors have explored the dynamic release of dopamine in area X from the dopaminergic input provided by the midbrain ventral tegmental area. In any given nucleus, the functions of dopamine will depend critically on the factors that regulate its dynamic availability; these include the function of uptake transporter proteins and the dynamic properties of release including regulation by receptors on dopamine axons (Cragg and Rice 2004; Schmitz et al. 2003; Wightman and Robinson 2002). By exploiting "real-time" detection methods, namely fast-scan cyclic voltammetry and constant potential amperometry at carbon-fiber microelectrodes, Gale and Perkel have investigated these key factors. They reveal that action-potential evoked dopamine release is powerfully regulated by D2-like dopamine autoreceptors, exhibits short-term depression and that the lifetime of extracellular dopamine is constrained by monoamine uptake transporters. The time constants and kinetics of control are strikingly similar to those found in rodent and primate striata (e.g., Cragg 2003; Schmitz et al. 2003). Such parallels suggest that dopamine could endow the songbird striatum with the repertoire of motor and motivational functions seen for dopamine in mammals (Schultz 2002; Wightman and Robinson 2002).
These harmonious parallels between songbird and mammalian striata are not without a few discordant surprises. Notably, the authors were unable to detect any regulation of DA release in area X by acetylcholine at nicotinic receptors. By contrast, acetylcholine release from cholinergic interneurons in mammalian striatum powerfully governs the dynamic probability of dopamine release (Rice and Cragg 2004; Zhang and Sulzer 2004), a feature that intriguingly mirrors the strong (albeit inverse) correlation between acetylcholine and dopamine neuron activity documented during conditioning and learned events in primates (Morris et al. 2004). This distinction, or otherwise, may be illuminated with time.
Yet clearly, we can think of the songbird striatum as a structure with significant analogy to the mammalian striatum according to cellular physiology and dopamine neurochemistry. Birdsong can remain high on its perch as a leading model for studying sensorimotor learning in vertebrate basal ganglia. With the characteristics of dopamine dynamics in songbird now in hand, the ground is prepared for exploration of basal ganglia dopamine in song learning in situ. May the chorus begin.
University Department of Pharmacology, Oxford, United Kingdom
Address for reprint requests and other correspondence:Address correspondence to: S. J. Cragg, University Department of Pharmacology, Mansfield Rd., Oxford, OX1 3QT, UK (E-mail: stephanie.cragg{at}pharm.ox.ac.uk)
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