Perineuronal nets in motor circuitry regulate the performance of learned vocalizations in songbirds

ABSTRACT The accurate and reliable production of learned behaviors can be important for survival and reproduction; for example, the performance of learned vocalizations (e.g., speech and birdsong) modulates the efficacy of social communication in humans and songbirds. Consequently, it is critical to understand the factors that regulate the performance of learned behaviors. Across various taxa, neural circuits that regulate motor learning are replete with perineuronal nets (PNNs), extracellular matrices that surround neurons and shape neural dynamics and plasticity. Perineuronal nets in circuits for sensory and cognitive processes have been found to affect sensory processing and behavioral plasticity. However, the function of PNNs in motor circuits remains largely unknown. Here, we analyzed the causal contribution of PNNs in motor circuitry to the performance of learned vocalizations in songbirds. Songbirds like the zebra finch are powerful models for this endeavor because the performance of their learned songs is regulated by activity within discrete and specialized circuits (i.e., song system) that are dense with PNNs. We first report that developmental increases in the density and intensity of PNNs throughout the song system [including in the motor nucleus HVC (acronym used as proper name)] are associated with developmental increases in song performance. We next discovered that enzymatically degrading PNNs in HVC acutely affected song performance. In particular, PNN degradation caused song structure to deviate from pre-surgery song due to changes in syllable sequencing and production. Collectively, our data provide compelling evidence for a causal contribution of PNNs to the performance of learned behaviors. SIGNIFICANCE STATEMENT Motor circuits are replete with perineuronal nets (PNNs) but little is known about their contribution to motor performance. Here, we analyzed how PNNs within vocal motor circuits modulate the ability of songbirds to consistently produce their learned songs. We report that developmental increases in PNN expression in vocal circuitry were associated with developmental increases in the ability to consistently perform their learned song. Moreover, degrading PNNs in the vocal motor nucleus HVC reduced the ability of adult birds to accurately produce their learned song. Our findings indicate a causal contribution of PNNs in motor circuitry to the performance of learned behaviors and, because PNNs are expressed in brain areas regulating speech, suggest that PNNs could modulate speech production in humans.

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