Reorganization of a telencephalic motor region during sexual differentiation and vocal learning in zebra finches.

Male zebra finches learn to produce a vocal pattern during a sensitive period of development, whereas females do not. The motor output of telencephalic song processing is RA (the robust nucleus of the archistriatum), a region containing a population of projection neurons that descend to the hindbrain (nXIIts, the tracheo-syringeal portion of the hypoglossal nerve nucleus). In turn, nXIIts neurons innervate the vocal organ (syrinx). Previous work shows that the number of RA neurons is monomorphic in fledgling males and females. RA neuron number in males does not change thereafter, but females show a substantial developmental loss of RA neurons. Because the developmental sex difference in RA neuron number implies a change in the number of projection neurons within RA, we have made injections of retrograde tracer into the hindbrain to measure the percentage of RA neurons that project to nXIIts as a function of age in females and vocal development in males. In juveniles of both sexes, we found that close to two-thirds of RA neurons project to nXIIts. However, the percentage of RA neurons projecting to nXIIts declined by 44% during female development, and by 14% during a specific stage of male vocal development (the transition from subsong to plastic song). These data indicate that in addition to regulation of RA neuron number, sexual differentiation and vocal learning correlate with a significant decrease in the amount of descending input to the vocal organ. The loss of projection neurons during vocal learning is surprising in light of the stability of RA neuron number in males, and our findings suggest that the behavioral transition from subsong to plastic song may involve a restricted period of RA neuron loss and replacement and/or axon rearrangement.