Timing of perineuronal net development in the zebra finch song control system correlates with developmental song learning

Abstract

The appearance of perineuronal nets (PNNs) represents one of the mechanisms that contribute to the closing of sensitive periods for neural plasticity. This relationship has mostly been studied in the ocular dominance model in rodents. Previous studies also indicated that PNN might control neural plasticity in the song control system of songbirds. To further elucidate this relationship, we quantified PNN expression and their localization around parvalbumin interneurons at key time-points during ontogeny in both male and female zebra finches, and correlated these data with the well-described development of song in this species. We also extended these analyses to the auditory system. The development of PNN during ontogeny correlated with song crystallization although the timing of PNN appearance in the four main telencephalic song control nuclei slightly varied between nuclei in agreement with the established role these nuclei play during song learning. Our data also indicate that very few PNN develop in the secondary auditory forebrain areas even in adult birds, which may allow constant adaptation to a changing acoustic environment by allowing synaptic reorganization during adulthood.

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

“…As aromatase is similarly expressed in NCM across development, changes in precursor androgens may explain previously observed age-dependent differences in baseline E2 in NCM across the critical period (Chao, et al, 2014), specifically in parallel with the maturation of the testes. Further, our findings with parvalbumin are in-line with recent findings that find that PV cell density is largely unchanged in across development in the NCM of in male and female zebra finches, as well as other auditory forebrain nuclei (Cornez et al, 2018). Therefore, PV-dependent inhibitory tone and estrogen production remain relatively unchanged across development, suggesting important roles throughout the juvenile period in males.…”

Development of Perineuronal Nets during Ontogeny Correlates with Sensorimotor Vocal Learning in Canaries

“…Half a series (two non-adjacent wells; 240 mm between sections) were double-labeled in a single assay for PV and chondroitin sulfate, one of the main components of the PNNs, following a previously described protocol (Balmer et al, 2009;Cornez et al, 2015Cornez et al, , 2017bCornez et al, , 2018. Briefly, sections were blocked in 5% normal goat serum (NGS) diluted in Tris-buffered saline (TBS) with 0.1% Triton X-100 (TBST) for 30 min.…”

“…Developmental song learning occurs during a sensitive period of neural plasticity associated with neurogenesis (Nordeen and Nordeen, 1988;Kirn and DeVoogd, 1989;Bottjer and Arnold, 1997) and synaptic pruning (Miller-Sims and Bottjer, 2012) in the song control system. Additionally it was recently suggested that perineuronal nets (PNNs) could play an important role in the regulation of sensitive periods for vocal learning in a closed-ended learner species, the zebra finch, Taeniopygia guttata (Balmer et al, 2009;Cornez et al, 2017bCornez et al, , 2018. PNN are aggregations of chondroitin sulfate proteoglycans, tenascin R, hyaluronic acid and binding proteins that form a scaffold mainly around fast spiking interneurons expressing parvalbumin (PV; Deepa et al, 2006;Wang and Fawcett, 2012).…”

“…Adult male zebra finches have more PNN in HVC than juveniles (Balmer et al, 2009) and their development around PV-interneurons is inhibited by acoustic isolation (Balmer et al, 2009). We previously reported that PNN develop in the song control system of male zebra finches between the end of the sensory and the end of the sensorimotor phase of song learning (Cornez et al, 2018) but the overlap between these two phases (Brainard and Doupe, 2002;Williams, 2004) makes it difficult to link PNN to a specific process. In contrast, song learning in canaries takes place over an extended period during ontogeny that only ends during the winter or early spring following hatching in the previous summer (Brainard and Doupe, 2002;Leitner et al, 2015).…”

Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats

“…PNN expression peaks in adulthood but is minimal in newborn and aged animals (Yamada & Jinno, ). The appearance of PNNs in juveniles coincides with the closing of critical developmental periods (Cornez et al, ; Pizzorusso et al, ), helping to solidify active synaptic networks (Dityatev et al, ). Loss of PNNs in the brain has been linked to brain diseases associated with neurological and cognitive dysfunction, including epilepsy (McRae & Porter, ), schizophrenia (Shah & Lodge, ), and Alzheimer's disease (Morawski, Brückner, Jäger, Seeger, & Arendt, ).…”