» Articles » PMID: 35286352

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.

Citing Articles

In vitro anthelmintic efficacy of Ferulic and Sinapic acid against zoonotic cestode (Rudolphi, 1819).

Saha S, Mondal C, Mandal S, Ray M, Lyndem L J Parasit Dis. 2024; 48(3):501-513.

PMID: 39145371 PMC: 11319579. DOI: 10.1007/s12639-024-01689-9.


Reevaluating Biota Alteration: Reframing Environmental Influences on Chronic Immune Disorders and Exploring Novel Therapeutic Opportunities.

Parker W, Jirku K, Patel E, Williamson L, Anderson L, Laman J Yale J Biol Med. 2024; 97(2):253-263.

PMID: 38947109 PMC: 11202117. DOI: 10.59249/VUNF1315.


: A Mysterious Member of the Gut Microbiome.

Aykur M, Malatyali E, Demirel F, Comert-Kocak B, Gentekaki E, Tsaousis A Microorganisms. 2024; 12(3).

PMID: 38543512 PMC: 10972062. DOI: 10.3390/microorganisms12030461.


Gallic acid and Catechin induce morphological alterations on the zoonotic parasite Hymenolepis diminuta.

Mondal C, Mandal S, Saha S, Ray M, Lyndem L Parasitol Res. 2023; 122(10):2287-2299.

PMID: 37507540 DOI: 10.1007/s00436-023-07929-w.


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

Wencel P, Blecharz-Klin K, Piechal A, Pyrzanowska J, Mirowska-Guzel D, Strosznajder R Neurotherapeutics. 2023; 20(5):1388-1404.

PMID: 37432552 PMC: 10480137. DOI: 10.1007/s13311-023-01403-2.


References
1.
Bialuk I, Taranta A, Winnicka M . IL-6 deficiency alters spatial memory in 4- and 24-month-old mice. Neurobiol Learn Mem. 2018; 155:21-29. DOI: 10.1016/j.nlm.2018.06.006. View

2.
Pan S, Ward D, Yin Y, Hu Y, Elfawal M, Clark R . Cognitive and Microbiome Impacts of Experimental Ancylostoma ceylanicum Hookworm Infections in Hamsters. Sci Rep. 2019; 9(1):7868. PMC: 6536493. DOI: 10.1038/s41598-019-44301-4. View

3.
Swain M, Blennerhassett P, Collins S . Impaired sympathetic nerve function in the inflamed rat intestine. Gastroenterology. 1991; 100(3):675-82. DOI: 10.1016/0016-5085(91)80011-w. View

4.
Zhang J, Terreni L, De Simoni MG , Dunn A . Peripheral interleukin-6 administration increases extracellular concentrations of serotonin and the evoked release of serotonin in the rat striatum. Neurochem Int. 2001; 38(4):303-8. DOI: 10.1016/s0197-0186(00)00099-1. View

5.
Jones L, Sun E, Martin A, Keating D . The ever-changing roles of serotonin. Int J Biochem Cell Biol. 2020; 125:105776. DOI: 10.1016/j.biocel.2020.105776. View