Sexually dimorphic perineuronal net expression in the songbird

Sexual dimorphism of song behavior and its underlying brain architecture characterizes the vocal learning system of many songbirds (Nottebohm and Arnold [1] and Ball and MacDougall-Shackleton [2]). Females do not sing and their neural song control system is reduced compared to males. However, females do learn to discriminate male song during a sensitive period (Clayton [3] and Nelson et al. [4]). We reasoned that any song nuclei that might store developmental social learning in female zebra finches would be marked by extracellular perineuronal nets (PNNs), which limit plasticity at the ends of critical periods (Hockfield et al. [5] and Hensch [6]), stabilize learning (Wang and Fawcett [7]), and demarcate all song nuclei in male finches (Balmer et al. [8]). PNN expression patterns in four brain areas were compared in males and females: the Lateral Magnocellular Nucleus (LMAN) and a basal ganglia region that contains Area X in males, which together constitute an anterior cortical-basal ganglia pathway necessary for male song plasticity, and HVC and the Robust Nucleus of the Arcopallium (RA), which together form a posterior pathway that is critical for song production in males. We found a dichotomy of PNN expression in the female song system: the anterior cortical-basal ganglia pathway was highly enriched for PNNs and indistinguishable from males, whereas the posterior pathway was essentially devoid of PNNs. These data indicate that social signaling in the female song system may undergo a true critical period, similar to sensory systems, and that limiting this critical period selectively involves the song cortical-basal ganglia pathway.