We have traced central nervous pathways controlling bird song in the canary using a combination of behavioral and anatomical techniques. Unilateral electrolytic brain lesions were made in adult male canaries whose song had been previously recorded and analysed on a sound spectrograph. After several days of postoperative recording, the birds were sacrificed and their brains processed histologically for degeneration staining with the Fink-Heimer technique. Although large lesions in the neostriatum and rostral hyperstriatum had no effect on song, severe song deficits followed damage to a discrete large-celled area in the caudal hyperstriatum ventrale (HVc). Degenerating fibers were traced from this region to two other discrete nuclei in the forebrain: one in the parolfactory lobe (area X, a teardrop-shaped small-celled nucleus); and a round large-celled nucleus in the archistriatum (RA). Unilateral lesion of X had no effect on song; lesions of RA, however, caused severe song deficits. Degenerating fibers from RA joined the occipitomesencephalic tract and had widespread ipsilateral projections to the thalamus, nucleus intercollicularis of the midbrain, reticular formation, and medulla. It is of particular interest that direct connections were found onto the cells of the motor nucleus innervating the syrinx, the organ of song production. Unilateral lesions of n. intercollicularis (previously implicated in the control of vocal behavior) had little effect on song. One bilateral lesion of HVc resulted in permanent (9 months) and complete elimination of the audible components of song, although the bird assumed the posture and movements typical of song. Preliminary data suggest that lesions of the left hemisphere result in greater deficits than lesions of the right one. This finding is consistent with earlier reports that the left syrinx controls the majority of song components. Results reported here suggest a localization of vocal control in the canary brain with an overlying left hemispheric dominance.

Song production in song birds is controlled by an efferent pathway. Appended to this pathway is a "recursive loop" that is necessary for song acquisition but not for the production of learned song. Since zebra finches learn their song by imitating external models, we speculated that the importance of the recursive loop for learning might derive from its processing of auditory feedback during song acquisition. This hypothesis was tested by comparing the effects on song in birds deafened early in life and birds with early lesions in either of two nuclei--Area X and the lateral magnocellular nucleus of the anterior neostriatum (LMAN). These nuclei are part of the recursive loop. The three treatments affected song development differently, as reflected by various parameters of the adult song of these birds. Whereas LMAN lesions resulted in songs with monotonous repetitions of a single note complex, songs of Area X-lesioned birds consisted of rambling series of unusually long and variable notes. Furthermore, whereas song of LMAN lesioned birds stabilized early, song stability as seen in intact birds was never achieved in Area X-lesioned birds. Early deafness also resulted in poorly structured and unstable song. We conclude that Area X and LMAN contribute differently to song acquisition: the song variability that is typical of vocal development persists following early deafness or lesions of Area X but ends abruptly following removal of LMAN. Apparently, LMAN plays a crucial role in fostering the kinds of circuit plasticity necessary for learning.

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