Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters

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.

Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups

“…Parasites have been found to have profound effects on host behaviour and cognition 2 , 3 , and the impact of GI helminths on cognitive function has been debated for many years 4 . Rodent studies in controlled laboratory settings showed that the GI helminths Nippostrongylus brasiliensis 4 , Heligmosomoides polygyrus 5 and Ancylostoma ceylanicum 6 impaired spatial learning and memory of the infected host, that Hymenolepsis diminuta improved spatial memory of the infected host 7 , and that Strongyloides ratti did not influence spatial learning or memory of the infected host 8 . Spatial memory is an important aspect of cognitive function that is needed both to plan a route to a desired location and to remember where an object is located or where an event occurred 9 .…”

Fingolimod Modulates the Gene Expression of Proteins Engaged in Inflammation and Amyloid-Beta Metabolism and Improves Exploratory and Anxiety-Like Behavior in Obese Mice

“…The GHI allows us to determine the overall level of exploration as well as the side and object preferences [ 33 , 41 ]. A higher GHI usually indicates less interest in the objects in the next trial [ 42 ]. The GHI was higher in mice on a HFD, indicating less interest in the novel object.…”

Blastocystis: A Mysterious Member of the Gut Microbiome

“…Although research has been conducted on the relationship between parasite manipulations and insect parasite interactions with the central nervous system (CNS), there have not been many studies on the interaction of the vertebrate host CNS and parasites [ 131 , 132 ]. The understanding of the interaction of the host CNS and parasites has increased recently with the development of the new and developing field of neuro-parasitology.…”

“…Echinococcus granulosus -derived ESPs (excretory–secretory products) affect cognitive function and the gut microbiome–brain axis as they have been demonstrated to alleviate dysbiosis and ameliorate cognitive decline in obese mice [ 134 ]. Another study revealed that Hymenolepis diminuta positively affected the spatial memory and new object recognition of the infected animal [ 131 ].…”