Neuroanatomical profiling of the rainbow trout brain parenchyma and meninges reveals specialized immune niches and region-specific hubs for bacterial immune surveillance

Abstract

Several studies have described immune responses in the teleost brain and meninges during infection, however, fundamental studies that systematically dissect how different regions of the brain maintain immune homeostasis in teleosts are missing. Here we present an in-depth investigation of the immune status of the brain parenchyma and meninges of juvenile rainbow trout (Oncorhynchus mykiss) at the steady state. We dissected four parenchymal brain regions including olfactory bulbs (OB), telencephalon (Tel), optic tectum (OT) and cerebellum (Cer) and its corresponding dorsal meninges. Gene expression analyses revealed higher expression of all studied immune gene markers in the meninges compared to the adjacent parenchymal areas. In the parenchyma, il1b, tnfa, ighd, ighm, ight, c3ra, icam1, and vcam1 expression were highest in the OB compared to other regions. Interestingly, il6 and il10 expression was lowest in the OB and higher in the posterior brain. Nod2a and nod2b expression levels were highest in the OT, a finding that was confirmed by in situ hybridization. cd45 in situ hybridization revealed that most of the cd45^high (immune cells) in the brain are located at the borders of the brain parenchyma (glia limitans superficialis). The present study demonstrates the presence of regional differences in the brain immune system of rainbow trout at homeostasis and identifies previously unknown hubs poised for specialized detection of microbial products.