The effects of toxoplasma infection on rodent behavior are dependent on dose of the stimulus

Abstract

Parasite Toxoplasma gondii blocks the innate aversion of rats for cat urine, putatively increasing the likelihood of a cat predating a rat. This is thought to reflect an adaptive behavioral manipulation, because toxoplasma can reproduce only in cat intestines. While it will be adaptive for the parasite to cause an absolute behavioral change, fitness costs associated with the manipulation itself suggest that the change is optimized and not maximized. We investigate these conflicting suggestions in the present report. Furthermore, exposure to cat odor causes long-lasting acquisition of learnt fear in the rodents. If toxoplasma manipulates emotional valence of cat odor rather than just sensory response, infection should affect learning driven by the aversive properties of the odor. As a second aim of the present study, we investigate this assertion. We demonstrate that behavioral changes in rodents induced by toxoplasma infection do not represent absolute all-or-none effects. Rather, these effects follow a non-monotonous function dependent on strength of stimulus, roughly resembling an inverted-U curve. Furthermore, infection affects conditioning to cat odor in a manner dependent upon strength of unconditioned stimulus employed. Non-monotonous relationship between behavioral manipulation and strength of cat odor agrees with the suggestion that a dynamic balance exists between benefit obtained and costs incurred by the parasite during the manipulation. This report also demonstrates that toxoplasma affects emotional valence of the cat odor as indicated by altered learned fear induced by cat odor.

Figure 1

Infection increased the relative occupancy in the bisect containing the urine in a dose-dependent manner. A. The ordinate depicts relative occupancy in bobcat bisect relative to occupancy in the same bisect during the habituation plus that during trial containing bobcat urine. Dotted line represents chance level. Abscissa depicts varying doses of the bobcat urine. *, p < 0.05; **, p < 0.01; planned comparison; MW test. B. Intermediate dose of bobcat urine produced a bigger magnitude of difference between control and infected animals. Ordinate depicts difference between control and infected animals in terms of relative occupancy in bisect containing bobcat urine. Data presented in this panel are derived from that in panel B. *, p < 0.05; **, p < 0.01; one-sample student’s t-test, compared to chance level (depicted with dotted line).

Figure 2

Effect of infection on aversion to cat towel was dependent on size of the towel. A. Infection significantly increased relative occupancy in towel bisect at an intermediate dose. *, p < 0.05. B. Magnitude of difference because of infection was dependent on size of towel. Intermediate dose produced the biggest effect. Data presented in this panel are derived from that in panel B. *, p < 0.05.

Figure 3

Effects Effect of infection on conditioned fear was dependent on size of the unconditioned stimulus, the cat towel A. Infection significantly increased relative occupancy in conditioned bisect at an intermediate dose, but decreased relative occupancy at the highest dose. *, p < 0.05. B. Magnitude of difference because of infection was dependent on size of towel. Data presented in this panel are derived from that in panel B. *, p < 0.05.