Localized neuronal activation in the zebra finch brain is related to the strength of song learning

Abstract

Songbirds (Oscines) learn their songs from a tutor. It is not known where in the brain the memories of these learned sounds are stored. Recent evidence suggests that song perception in songbirds involves neuronal activation in brain regions that have not traditionally been implicated in the control of song production or song learning, notably the caudal part of the neostriatum (NCM) and of the hyperstriatum ventrale. Zebra finch males (Taeniopygia guttata castanotis) were reared without their father and exposed to a tape-recorded song during the sensitive period for song learning. When, as adults, they were reexposed to the tutor song, the males showed increased expression of the protein products of the immediate early genes egr-1 (ZENK) and c-fos in the NCM and caudal hyperstriatum ventrale, but not in the conventional "song-control nuclei." The strength of the immediate early gene response (which is a reflection of neuronal activation) in the NCM correlated significantly and positively with the number of song elements that the birds had copied from the tutor song. These results show localized neural activation in response to tutor song exposure that correlates with the strength of song learning.

Figure 1

(a) A schematic diagram of a composite of parasagittal sections of the zebra finch brain. Drawing gives approximate positions of nuclei and brain regions. RA, robust nucleus of the archistriatum; LH, lamina hyperstriatica; Cb, cerebellum; DLM, medial part of the dorsolateral thalamic nucleus; nXIIts, tracheosyringeal portion of the nucleus hypoglossus. Dark arrows, caudal pathway; gray arrows, rostral pathway. (b) Photomicrograph of a parasaggital section of a zebra finch brain, stained for acetylcholinesterase. The section clearly shows HVC, Area X, lMAN, and RA.

Figure 2

Sonograms of a tutor song (a), of an experimental bird that shared the smallest number of elements with the tutor song (b), and that shared the greatest number of elements with the tutor song (c).

Figure 3

Photomicrographs of parasagittal sections of the zebra finch brain at the level of the NCM, showing egr-1 (ZENK)-like immunostaining. Overlay is the counting frame used (0.5 × 0.5 mm). The sections are from a bird in the control (a) and of a bird in the experimental group (b) that both showed a high degree of song learning. V, ventricle; Hp, hippocampus.

Figure 4

Mean number of immunoreactive (IR) cell nuclei per mm² for the experimental birds (filled bars) and controls (open bars) in the NCM (a), cHV (b), HVC (c), and Area X (d), for Fos (Left) and ZENK protein (Right). Only in the NCM and the cHV was there a significant increase in expression of both Fos and ZENK protein in the experimentals compared with the controls.

Figure 5

Scattergrams of the number of immunoreactive cell nuclei per mm² in the NCM, related to the fraction of the number of song elements that were shared with the tutor song. (a) Zenk protein. (b) Fos. In the experimental birds (filled symbols), there was a significant positive correlation for both Fos (r = 0.722, P < 0.03) and ZENK protein (r = 0.775, P < 0.02). There was no significant correlation in the control birds (open symbols) in these two conditions (r = 0.264 and r = 0.250, respectively). Lines are linear regression lines for the respective groups.