Abstract
The intracellular parasite Toxoplasma has an indirect life cycle, in which felids are the definitive host. It has been suggested that this parasite developed mechanisms for enhancing its transmission rate to felids by inducing behavioral modifications in the intermediate rodent host. For example, Toxoplasma-infected rodents display a reduction in the innate fear of predator odor. However, animals with Toxoplasma infection acquired in the wild are more often caught in traps, suggesting that there are manipulations of intermediate host behavior beyond those that increase predation by felids. We investigated the behavioral modifications of Toxoplasma-infected mice in environments with exposed versus non-exposed areas, and found that chronically infected mice with brain cysts display a plethora of behavioral alterations. Using principal component analysis, we discovered that most of the behavioral differences observed in cyst-containing animals reflected changes in the microstructure of exploratory behavior and risk/unconditioned fear. We next examined whether these behavioral changes were related to the presence and distribution of parasitic cysts in the brain of chronically infected mice. We found no strong cyst tropism for any particular brain area but found that the distribution of Toxoplasma cysts in the brain of infected animals was not random, and that particular combinations of cyst localizations changed risk/unconditioned fear in the host. These results suggest that brain cysts in animals chronically infected with Toxoplasma alter the fine structure of exploratory behavior and risk/unconditioned fear, which may result in greater capture probability of infected rodents. These data also raise the possibility that selective pressures acted on Toxoplasma to broaden its transmission between intermediate predator hosts, in addition to felid definitive hosts.
Highlights
IntroductionToxoplasma gondii (from here on referred to as Toxoplasma) is an obligate intracellular parasite [1], capable of infecting all mammals, with an indirect life cycle where cats and other felids constitute the definitive hosts
Toxoplasma gondii is an obligate intracellular parasite [1], capable of infecting all mammals, with an indirect life cycle where cats and other felids constitute the definitive hosts
Our results demonstrate that chronic infection by Toxoplasma changes the microstructure of exploratory behaviors and risk/ unconditioned fear, and that these changes are related to cyst presence and cyst localization
Summary
Toxoplasma gondii (from here on referred to as Toxoplasma) is an obligate intracellular parasite [1], capable of infecting all mammals, with an indirect life cycle where cats and other felids constitute the definitive hosts. Parasites will invade the epithelial cells of the intestine, where they undergo both sexual and asexual reproduction. Felids are the only mammals known to shed Toxoplasma oocysts with their feces [2], which will contaminate the surrounding environment. When oocysts are ingested by a mammal other than a cat, such as a wild rodent (intermediate host), an extra-intestinal cycle is initiated, where asexual (clonal) reproduction occurs and small cysts form in various tissues, most notably in the brain. If a non-infected cat consumes an infected intermediate host, the Toxoplasma life cycle is completed [3]
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