Changes in perineuronal net components correlate with functional modifications of vestibular nuclear neurons in the rat

Abstract

To determine if the perineuronal net (PN) within the vestibular nucleus (VN) is involved in plasticity of the central vestibular network, the organization of the PN was examined during (1) postnatal development and (2) compensation after the loss of ipsilateral afferent inputs (unilateral labyrinthectomy, UL). The PN around NeuN-positive VN neurons was visualized by staining with Wisteria floribunda agglutinin (WFA) for terminal N-acetylgalactosamine components or with antibody against neurocan for a core protein component of PN. Both components of PN indicated diffuse organization in neonatal rats but progressively evolved into a consolidated network from postnatal day (P) 9, reaching the adult organization by P21. This temporal profile of PN maturation correlated with those of VN neuronal discharge properties and the geotaxic reflex. These results suggest that PN formation in the VN constitutes part of the maturation of the vestibular system. After UL in adult rats, the WFA-positive PN network on the lesioned side became fuzzy at 3-5 days post-lesion but not on the labyrinth-intact side. By 11-14 days after UL, PN resumed the normal organization. In contrast, no change was observable in the neurocan-positive PN on both lesioned and intact sides. We further demonstrated that vast majority of PN-surrounded cells in the VN was GABAergic in nature. Since GABAergic neurons are known to play a crucial role in regulating commissural compensation between VN on the two sides, the fuzziness revealed by WFA-positivity after UL suggests involvement in the regulation of vestibular compensation. Taken together, our findings suggest that the carbohydrate and core protein components of the PN serve differential roles in modulating neuronal functions of the central vestibular system.