Perineuronal nets and vocal plasticity in songbirds: A proposed mechanism to explain the difference between closed‐ended and open‐ended learning

Abstract

Perineuronal nets (PNN) are aggregations of chondroitin sulfate proteoglycans surrounding the soma and proximal processes of neurons, mostly GABAergic interneurons expressing parvalbumin. They limit the plasticity of their afferent synaptic connections. In zebra finches PNN develop in an experience-dependent manner in the song control nuclei HVC and RA (nucleus robustus arcopallialis) when young birds crystallize their song. Because songbird species that are open-ended learners tend to recapitulate each year the different phases of song learning until their song crystallizes at the beginning of the breeding season, we tested whether seasonal changes in PNN expression would be found in the song control nuclei of a seasonally breeding species such as the European starling. Only minimal changes in PNN densities and total number of cells surrounded by PNN were detected. However, comparison of the density of PNN and of PNN surrounding parvalbumin-positive cells revealed that these structures are far less numerous in starlings that show extensive adult vocal plasticity, including learning of new songs throughout the year, than in the closed-ended learner zebra finches. Canaries that also display some vocal plasticity across season but were never formally shown to learn new songs in adulthood were intermediate in this respect. Together these data suggest that establishment of PNN around parvalbumin-positive neurons in song control nuclei has diverged during evolution to control the different learning capacities observed in songbird species. This differential expression of PNN in different songbird species could represent a key cellular mechanism mediating species variation between closed-ended and open-ended learning strategies.

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.…”

“…The borders of lMAN are however not clearly outlined by this staining and the volume of this nucleus could therefore not be determined. Photomicrographs of all stained sections containing the nuclei HVC, RA, or area X were acquired at 5Â magnification and the volume of these nuclei was quantified as previously described (Cornez et al, 2017b). First, the area of the regions of interest (ROIs; in mm 2 ) within each section was measured using the ImageJ software (NIH; https://imagej.nih.gov/ij).…”

“…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).…”

Inhibitory cell populations depend on age, sex, and prior experience across a neural network for Critical Period learning

“…The current results are intriguing because on the one hand, Field L does not demonstrate distinct response magnitude or selectivity properties for tutor song compared to conspecific song in normally-reared males, yet early song experience does alter the balance of responsiveness and selectivity to song compared to non-song sounds in Field L (Gehr et al, 2000;Maul et al, 2010;Woolley et al, 2010). Notably, other studies that measured parvalbumin protein-labeled cells did not detect alterations in Normally reared males across age (Braun et al, 1991;Cornez et al, 2017). It can, however, be difficult to link different levels of analysis with simple linear relationships.…”

Disruption of perineuronal nets increases the frequency of sharp wave ripples

“…PNN formation is neuronal activity dependent (Dityatev et al, 2007), and region specific development is influenced by relevant neuronal activity or lack thereof. PNNs are more numerous in song bird species with closed end song learning as opposed to those that display extensive adult vocal plasticity (Cornez et al, 2017). Moreover, PNN deposition and critical period closure in the visual cortex are both reduced by dark rearing (Gianfranceschi et al, 2003;Hockfield et al, 1990;Mower, 1991), and effects of monocular deprivation are mimicked by matrix degradation (Oray et al, 2004).…”