GIGA Neuroscience, University of Liege, Liege 4000, Belgium.
Department of Psychology, University of Maryland, College Park, MD 20742, USA.
Horm Behav. 2020 Mar;119:104643. doi: 10.1016/j.yhbeh.2019.104643. Epub 2019 Dec 6.
Perineuronal nets (PNN) of the extracellular matrix are dense aggregations of chondroitin-sulfate proteoglycans that usually surround fast-spiking parvalbumin-expressing inhibitory interneurons (PV). The development of PNN around PV appears specifically at the end of sensitive periods of visual learning and limits the synaptic plasticity in the visual cortex of mammals. Seasonal songbirds display a high level of adult neuroplasticity associated with vocal learning, which is regulated by fluctuations of circulating testosterone concentrations. Seasonal changes in testosterone concentrations and in neuroplasticity are associated with vocal changes between the non-breeding and breeding seasons. Increases in blood testosterone concentrations in the spring lead to the annual crystallization of song so that song becomes more stereotyped. Here we explore whether testosterone also regulates PNN expression in the song control system of male and female canaries. We show that, in both males and females, testosterone increases the number of PNN and of PV neurons in the three main telencephalic song control nuclei HVC, RA (nucleus robustus arcopallialis) and Area X and increases the PNN localization around PV interneurons. Singing activity was recorded in males and quantitative analyses demonstrated that testosterone also increased male singing rate, song duration and song energy while decreasing song entropy. Together, these data suggest that the development of PNN could provide the synaptic stability required to maintain the stability of the testosterone-induced crystallized song. This provides the new evidence for a role of PNN in the regulation of adult seasonal plasticity in seasonal songbirds.
周围神经毡(PNN)是细胞外基质中的密集聚集物,通常围绕快速发射的表达 parvalbumin 的抑制性中间神经元(PV)。PNN 围绕 PV 的发育似乎专门出现在视觉学习敏感时期的末期,并限制了哺乳动物视觉皮层中的突触可塑性。季节性鸣禽表现出高水平的与发声学习相关的成年神经可塑性,这种可塑性受循环睾酮浓度的波动调节。睾酮浓度和神经可塑性的季节性变化与繁殖季节和非繁殖季节之间的发声变化有关。春季血液中睾酮浓度的增加导致歌曲的年度结晶,从而使歌曲变得更加刻板。在这里,我们探讨睾酮是否也调节雄性和雌性金丝雀歌唱控制系统中的 PNN 表达。我们表明,在雄性和雌性中,睾酮都会增加三个主要的端脑歌唱控制核(HVC、RA(厚脑盖弓状核)和 Area X)中 PNN 和 PV 神经元的数量,并增加 PNN 对 PV 中间神经元的定位。在雄性中记录了歌唱活动,定量分析表明,睾酮还增加了雄性的歌唱率、歌唱持续时间和歌唱能量,同时降低了歌唱熵。这些数据表明,PNN 的发育可能为维持睾酮诱导的结晶歌曲的稳定性提供了所需的突触稳定性。这为 PNN 在季节性鸣禽的季节性成年可塑性调节中的作用提供了新的证据。