Physical Enrichment Triggers Brain Plasticity and Influences Blood Plasma Circulating miRNA in Rainbow Trout (Oncorhynchus mykiss)

SIMPLE SUMMARY: Overall, this study has reported that environmental enrichment significantly displayed a series of differentially expressed genes and pathways related to cerebral activity, neural plasticity (neurotrophic markers), neurogenesis, and synaptogenesis, essentially in telencephalon, which may underpin the beneficial effects of a complex environment on rainbow trout’s adaptive behaviors. In addition, environmental enrichment significantly influenced circulating miRNAs (c-miRNAs) profiles of plasma in rainbow trout, which reveals the high potential of c-miRNAs, as physiologically relevant biomarker candidates of fish behavioral plasticity. ABSTRACT: Physical enrichment is known to improve living conditions of fish held in farming systems and has been shown to promote behavioral plasticity in captive fish. However, the brain’s regulatory-mechanism systems underlying its behavioral effects remain poorly studied. The present study investigated the impact of a three-month exposure to an enriched environment (EE vs. barren environment, BE) on the modulation of brain function in rainbow trout (Oncorhynchus mykiss) juveniles. Using high-throughput RT-qPCR, we assessed mRNA genes related to brain function in several areas of the trout brain. These included markers of cerebral activity and plasticity, neurogenesis, synaptogenesis, or selected neurotransmitters pathways (dopamine, glutamate, GABA, and serotonin). Overall, the fish from EE displayed a series of differentially expressed genes (neurotrophic, neurogenesis, and synaptogenesis markers) essentially localized in the telencephalon, which could underpin the beneficial effects of complexifying the environment on fish brain plasticity. In addition, EE significantly affected blood plasma c-miRNA signatures, as revealed by the upregulation of four c-miRNAs (miR-200b/c-3p, miR-203a-3p, miR-205-1a-5p, miR-218a-5p) in fish blood plasma after 185 days of EE exposure. Overall, we concluded that complexifying the environment through the addition of physical structures that stimulate and encourage fish to explore promotes the trout’s brain function in farming conditions.