Trends in Neurosciences
Birdbrains could teach basal ganglia research a new song
Introduction
The cortical–basal ganglia circuit has been implicated in the learning and execution of sequences of movements 1, 2, 3, 4, 5. Advancing this concept in mammals has been hindered by the complexity of the connections within the basal ganglia. Despite the general structure of functional loops connecting the cortex and basal ganglia 6, 7, the complex pattern of convergent and divergent projections, and the sparse connectivity within these structures 8, 9, has not enabled specific behavioral repertoires to be linked to specific circuits.
We propose that several major obstacles to understanding cortical–basal ganglia function could be reduced by using more comparative and neuroethological approaches to the problem. Birds possess virtually all mammalian basal ganglia structures, and their pallial inputs and thalamic and brainstem outputs, with some intriguing differences that could shed light on function. Moreover, a subset of birds, the songbirds, learn to produce their complex, sequenced vocal motor output using sensory feedback [10], and have specialized a portion of their forebrain–basal ganglia circuitry expressly for the purpose of song learning. Because this specialized cortical–basal ganglia circuit, known as the anterior forebrain pathway (AFP), is discrete and devoted to a specific well-defined behavior, rather than a broad range of motor behaviors, it should be particularly tractable for investigating how basal ganglia structures contribute to the learning and performance of motor skills.
Here, we review the anatomical and electrophysiological studies that support the strong parallels between avian and mammalian basal ganglia circuitry, and the functional investigations of the songbird AFP that are beginning to suggest the behavior-related signals it carries.
Section snippets
Modern views of the avian telencephalon
A glance at a traditional avian atlas would suggest that almost the entire avian telencephalon is basal ganglia, because most of the structures of the lateral telencephalic wall have names with the word ‘striatum’ as a root. However, modern neuroanatomical, molecular biological and neurochemical studies have shown that the avian basal ganglia have much the same telencephalic extent as in mammals (Figure 1). The voluminous territory above the basal ganglia in birds is now recognized as
Area X and the AFP for song
The AFP (Figure 2) of oscine songbirds is essential for vocal learning and plasticity. Area X, a key nucleus of the AFP, lies within the medial striatum, suggesting that the AFP is a cortical–basal ganglia circuit devoted to song-related functions. Area X receives afferents from two pallial nuclei, HVC (used as the proper name) and the lateral magnocellular nucleus of the anterior nidopallium (LMAN), and it projects to the medial portion of the dorsolateral thalamic nucleus (DLM). The AFP thus
AFP function in learning of behavior
Songbirds learn their complex, sequenced vocal motor behavior (Figure 4b) in early life, in a process (Figure 4a) with parallels to human speech learning, especially in its marked dependence on hearing self and others. The AFP is crucial for this learning. Lesions of Area X (the striatal–pallidal portion of the AFP) or of LMAN [the AFP outflow nucleus, equivalent to cortical targets of the mammalian basal ganglia (Figure 2)] both result in dramatic disruption of song when the lesions are made
Cellular plasticity in the song system
Cellular mechanisms that could contribute to learning occur in at least two nuclei of the songbird AFP. Collateral synapses within the pallial nucleus LMAN show activity-dependent LTP [80]. This form of plasticity depends on postsynaptic action-potential timing and on activation of NMDA receptors, which undergo striking developmental changes in this nucleus [84]. LMAN LTP occurs in 20-day-old zebra finches, at an age when birds can be memorizing the tutor song but are not yet singing. However,
Concluding remarks
In conclusion, the recent advances in avian basal ganglia research, together with the revolution in avian neuroanatomical nomenclature, illustrate the usefulness of avian models for the study of cortical–basal ganglia function. Whereas the complexity of mammalian basal ganglia circuitry makes several experiments technically infeasible, the specialization of nuclei for specific behaviors in songbirds should facilitate investigation of the neuronal computations underlying sensorimotor tasks,
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