Perineuronal nets in subcortical auditory nuclei of four rodent species with differing hearing ranges

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Perineuronal nets (PNs) are aggregates of extracellular matrix molecules that surround some neurons in the brain (Karetko & Skangiel‐Kramska, 2009; Morawski, Brückner, Arendt, & Matthews, 2012, for review). In cortex, PNs are best known for surrounding parvalbumin‐positive fast‐spiking inhibitory interneurons, but PNs have also been associated with as many as one third of pyramidal cells (Härtig, Brauer, & Brückner, 1992; Hausen et al., 1996; Wegner et al., 2003). In the visual cortex, PNs develop at the close of the visual critical period, and extending the critical period with dark rearing delays the development of PNs (Pizzorusso et al., 2002; Ye & Miao, 2013). Further, abnormal patterns of ocular dominance due to early monocular deprivation can be corrected in adult rats via enzymatic digestion of PNs in the primary visual cortex (Pizzorusso et al., 2006). Similar results have been achieved in other areas: digestion of PNs in basolateral amygdala leads to formation of fear memories that are more vulnerable to erasure (Gogolla, Caroni, Lüthi, & Herry, 2009); digestion of PNs in striatum leads to a wider and more variable gait (Lee, Leamey, & Sawatari, 2012); digestion of PNs in auditory cortex does not affect initial learning of a go/no‐go task but facilitates reversal training (Happel et al., 2014). Throughout cortex, digestion of PNs leads to phenomena related to increased plasticity (reviewed by Sorg et al., 2016). Although regulation of plasticity, specifically inhibition of structural plasticity, is one of the main functions associated with PNs, they have also been suggested to affect synaptic plasticity, protect against oxidative stress, and support fast spiking in the cells they surround (Härtig et al., 1999; Corvetti & Rossi, 2005; Beurdeley et al., 2012; Suttkus, Rohn, Jäger, Arendt, & Morawski, 2012; Cabungcal et al., 2013; de Vivo et al., 2013).
Less research has been done involving PNs in subcortical areas. Subcortical PNs are especially associated with motor and auditory nuclei, although not exclusively (Seeger, Brauer, Härtig, & Brückner, 1994; Bertolotto, Manzardo, & Guglielmone, 1996; Sonntag, Blosa, Schmidt, Rübsamen, & Morawski, 2015). Neonatal conductive hearing loss affects PNs in several auditory brainstem nuclei of the superior olivary complex (SOC), and PNs develop in the medial nucleus of the trapezoid body (MNTB) coincident with the maturation of reliable fast spiking (Taschenberger & von Gersdorff, 2000; Myers, Ray, & Kulesza, 2012). Studies examining the function of PNs in the auditory brainstem (specifically the MNTB) have shown that PNs are important to proper spike timing and spike rate, which are in turn essential for encoding sound characteristics such as frequency, intensity, and location (Oertel, 1999; Eggermont, 2001; Blosa et al., 2015; Balmer, 2016). Even though the importance of PNs to auditory function seems clear, there are inconsistencies in the literature regarding PN distribution in the subcortical auditory system. For example, a study in rat found that PNs were more prominent in the cortical areas of the inferior colliculus (IC) and lacking in the central nucleus, while a study in guinea pig found that PNs were densest in the central nucleus (rat: Bertolotto et al., 1996; guinea pig: Foster, Mellott, & Schofield, 2014). This particular discrepancy may be due to a difference in PN distribution between these two species, or it could reflect differences in the methods employed to visualize PNs (an antibody stain in the first study, and a lectin stain in the second). Another point of uncertainty in the literature is whether PN staining varies along the tonotopic axes of auditory nuclei.
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