Vocal Basal Ganglia

The anterior vocal pathway, a forebrain-basal ganglia loop, is important for the development and learning of song in birds and shows differential gene expression based on social context. We are interested in the role of this pathway and the basal ganglia in learned vocal communication.

Directed and undirected singing

Male singing towards a female (directed song; left) and male singing while not facing a male next to him (undirected song; right). Above each picture is an in-situ hybridization of a representative parasaggital brain section reacted to radioactively-labeled canary ZENK riboprobe (white silver grains) and stained with cresyl violet (red). Directed singing induces high expression in HVC (vocal nucleus of posterior pathways), low in lateral AreaX, lateral MAN, and RA; undirected song induces high expression in all four nuclei.

Sonograms of directed and undirected song

Sonograms from a male zebra finch when singing towards a female (left) and when singing not facing any bird (right). Yellow shaded are introductory notes, red shaded and letters A-G designate individual notes in the song motif. Except for number of introductory notes and song speed, the vocalizations are very similar. Thus, a small difference in behavior is accompanied by a dramatic difference in the brain.

The role of basal ganglia in learned vocal communication

The ability to learn (mimic) vocalizations is exceptional in the animal kingdom. While there are certainly differences between human speech and avian song, there is remarkable similarity of vocal brain pathways among vocal learning bird lineages, such that one group can be a useful model system for other vocal learning groups.

As first characterized in songbirds, two pathways have been found to be unique to vocal learners – posterior and anterior vocal pathways. After lesions in the posterior pathway birds are not able to sing (Nottebohm et al 1976; Simpson and Vicario 1990). Lesions in the anterior pathway lead to changes in song development in juveniles or in adults during new singing seasons. Adult birds with stable song (zebra finches) or adult birds in the current singing season ( canaries, white crown sparrows, song sparrows) sing normally after lesions in anterior pathway (Bottjer et al 1984; Nottebohm et al 1990; Sohrabji et al 1990; Suter et al 1990; Scharff and Nottebohm 1991; Nordeen and Nordeen 1993; Benton et al 1998; Williams and Mehta 1999; Brainard and Doupe 2000).

These findings suggest that the anterior pathway which contains the largest vocal nucleus, Area X within the basal ganglia, is important for vocal learning but not for vocal production. Therefore it is surprising that the vocal nuclei of the anterior pathway and one in the posterior show different gene expression patterns during song production in different social contexts. If a male zebra finch sings directed song to a female there is low expression of the immediate early gene ZENK in lateral part of AreaX and lateral part of MAN (anterior pathway vocal nuclei) and RA (posterior pathway vocal nucleus). On the other hand, if a male zebra finch sings undirected song in male or solo context there is high ZENK expression in all these nuclei (Fig. 1A, Jarvis et al 1998).

Vocal motor outputs of directed and undirected singing (measured from sound spectrograms) differ very little (Jarvis et al 1998; Hessler and Doupe 1999). Directed zebra finch song is preceded by more introductory notes than undirected song, it is sung slightly faster (Fig. 1B) and it is usually accompanied by a courtship dance. These vocal differences are hardly detectable by the human ear. Thus, two very similar vocal behaviors are accompanied by dramatically different brain activation patterns.

Why is there such a remarkable difference in ZENK expression during directed and undirected singing? Why is the anterior pathway active during the non-learning period? And what is the role of the basal ganglia in vocalization of adults? These are the questions which we are trying to answer.

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