Dynamics of perineuronal nets over amphibian metamorphosis.

Abstract

Extracellular matrix materials known as perineuronal nets (PNNs) have been shown to have remarkable consequences for the maturation of neural circuits and stabilization of behavior. It has been proposed that, due to the possibly long-lived biochemical nature of their components, PNNs may be an important substrate by which long-term memories are stored in the central nervous system. However, little empirical evidence exists that shows that PNNs are themselves stable once established. Thus, the question of their temporal dynamics remains unresolved. We leverage the dramatic morphological and behavioral transformations that occur during amphibian metamorphosis to show that PNNs can be highly dynamic in nature. We used established lectin histochemistry to show that PNNs undergo drastic reconstruction during the metamorphic transition. Pre-metamorphic tadpoles have abundant lectin-labeled pericellular material, which we interpret to be PNNs, surrounding neurons throughout the central nervous system. During the metamorphic transition, these structures degrade, and begin to reform in the months following metamorphosis. We show that PNN sizes and staining intensity further change over metamorphosis, suggesting compositional rearrangement. We found PNNs in brain regions with putative homology to regions in mammals with known PNN function, and in other shared regions where PNN function is unknown. Our results suggest that PNNs are susceptible to remodeling by endogenous mechanisms during development. Interpreting the roles of PNNs in circuit maturation and stability requires understanding their temporal relationship with the neurons and synapses they surround. Our work provides further impetus to investigate this relationship in tandem with developmental and behavioral studies.