학술논문

Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters.
Document Type
Article
Source
PLoS Pathogens. 3/14/2022, Vol. 18 Issue 3, p1-25. 25p.
Subject
*HELMINTHS
*HELMINTHIASIS
*CURIOSITY
*INTESTINAL infections
*PARASITES
*TAPEWORM infections
*PARASITIC diseases
*NEUROTRANSMITTERS
Language
ISSN
1553-7366
Abstract
Parasites may significantly affect the functioning of the host organism including immune response and gut-brain-axis ultimately leading to alteration of the host behavior. The impact of intestinal worms on the host central nervous system (CNS) remains unexplored. The aim of this study was to evaluate the effect of intestinal infection by the tapeworm Hymenolepis diminuta on behavior and functions of the CNS in rats. The 3 months old animals were infected, and the effects on anxiety, exploration, sensorimotor skills and learning processes were assessed at 18 months in Open Field (OF), Novel Object Recognition (NOR) and the Water Maze (WM) tests. After completing the behavioral studies, both infected and non-infected rats were sacrificed, and the collected tissues were subjected to biochemical analysis. The levels of neurotransmitters, their metabolites and amino acids in selected structures of the CNS were determined by HPLC. In addition, the gene expression profile of the pro- and anti-inflammatory cytokines (TNF-α, IL-1β, IL-6 and IL-10) was evaluated by Real-Time PCR to determine the immune response within the CNS to the tapeworm infection. The parasites caused significant changes in exploratory behavior, most notably, a reduction of velocity and total distance moved in the OF test; the infected rats exhibited decreased frequency in the central zone, which may indicate a higher level of anxiety. Additionally, parasite infestation improved spatial memory, assessed in the WM test, and recognition of new objects. These changes are related to the identified reduction in noradrenaline level in the CNS structures and less pronounced changes in striatal serotonergic neurotransmission. H. diminuta infestation was also found to cause a significant reduction of hippocampal expression of IL-6. Our results provide new data for further research on brain function during parasitic infections especially in relation to helminths and diseases in which noradrenergic system may play an important role. Author summary: Recent advances in the research on parasitic manipulation and/or control of the nervous system of their host resulted in the development of neuro-parasitology, a new and emerging branch of science. There have been advances in this area in relation to parasite-insect interactions or parasites directly invading central nervous system (CNS). However, the neuro-parasitology of parasitic infections in vertebrate hosts remains unexplored. In our study the effect of intestinal infection by the tapeworm on the behavior, neurotransmission and functions of the CNS in rats was evaluated. This infection positively influenced spatial memory and new object recognition. At the same time, the infected animals developed a greater level of anxiety and move more slowly. Behavioral changes were related to the reduction in noradrenaline level in the CNS structures, and less pronounced changes in striatal serotonergic neurotransmission. The results provide important data for the further progress in neuro-parasitology and our understanding of parasite-host interactions. In our opinion in the near future may turn out that the role of the intestinal host macrobiome in the CNS functioning may be just as significant as that of the microbiome. Presented neuro-immunological data provide a new perspectives for further studies on the CNS under intestinal parasite infection. The data of behavioral changes induced by active parasitic infection may be valid for explanations of the host-parasite relationship at the evolutionary level and their molecular adjustment. [ABSTRACT FROM AUTHOR]