Cross-species conservation in the regulation of parvalbumin by perineuronal nets

• Published in: Frontiers in neural circuits Vol. 17; p. 1297643
• Main Authors: Wang, Angela S, Wan, Xinghaoyun, Storch, Daria-Salina, Li, Vivian Y, Cornez, Gilles, Balthazart, Jacques, Cisneros-Franco, J Miguel, de Villers-Sidani, Etienne, Sakata, Jon T
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Research Foundation 19.12.2023; Frontiers Media S.A
• Subjects: Animal cognition; Animals; auditory cortex; Basal ganglia; Birds; Brain - metabolism; Brain research; Enzymes; Evolutionary conservation; Extracellular Matrix - metabolism; globus pallidus; Males; Mammals - metabolism; motor cortex; Nets; Neural plasticity; Neuromodulation; Neuronal Plasticity; Neurons; Neurons - metabolism; Neuroscience; Parvalbumin; Parvalbumins - metabolism; Passeri; Perineuronal nets; Sensory neurons; songbird; zebra finch; development; auditory cortex; basal ganglia; motor cortex; zebra finch; striatum; songbird; globus pallidus
• ISSN: 1662-5110; 1662-5110
• DOI: 10.3389/fncir.2023.1297643

Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.