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 be 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.

Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

“…In male human volunteers, T. gondii infection is associated with a statistically non-significant increase in salivary testosterone levels (Flegr et al, 2008). In parallel, female volunteers rate portraits of infected males as being more dominant and masculine compared with uninfected males (Hodková et al, 2007b) [see review by Flegr (Flegr, 2013) for a detailed discussion of toxoplasmosis in humans].Apart from manipulating host mate choice, T. gondii also alters host response to predator odors (Berdoy et al, 2000;Vyas et al, 2007a;Vyas et al, 2007b;Webster and McConkey, 2010). Rats infected with T. gondii loose their natural aversion to cat odor and instead develop an attraction.…”

Manipulation of host behaviour by Toxoplasma gondii: what is the minimum a proposed proximate mechanism should explain?

“…While infected rats show a deficit in conditioned fear when foot shock is used an unconditioned stimulus, T. gondii affects learned fear expressed after conditioning to the cat odour (Vyas et al 2007b). in uninfected rodents, exposure to cat odour causes acquired changes in the behaviour related to learning.…”

“…infected rats retain the aversion to odours of predators that do not serve as definitive host of T. gondii, like mink (lamberton et al 2008). c) The response of infected rats to cat odour is linked to the dose of cat odour in a subtle and non-monotonic way (Vyas et al 2007b). infected animals do not differ from control animals when cat odour is presented in very high or very low ranges of concentration; instead, the behavioural manipulation is restricted to middle ranges of cat odour strength.…”

Toxoplasma gondii-altered host behaviour: clues as to mechanism of action

“…the apparent subtle ability of these rats to distinguish between (a) a predatory cat and a non-predatory mammal such as rabbit odours (Berdoy et al 2000, Webster et al 2006, Vyas et al 2007a, and (b) even between contrasting potential predator host species odours, where infected rats have been shown to be attracted to/differentiate between a cat definitive host odour from that of a non-definitive host predator such as mink (lamberton et al 2008) or dog (Kannan et al 2010, this volume), (c) that the specificity of the response appears to be restricted to the middle ranges of cat odour strength (Vyas et al 2007b), and finally (d) that the observed effects appear to represent an apparent change in the cognitive perception of the host to such cat odour, a 'fatal feline attraction', rather than a destruction of that behavioural trait (Berdoy et al 2000), all suggests this is not a simple disruption or reduction of, for example, olfaction in general, nor likely to indicate any sweeping changes in the neural substrates involved in bringing about these effects (lamberton et al 2008). one could thus speculate, therefore, that T. gondii could induce the inactivation of a few olfactory receptors important specifically for cat, but not other species.…”

“…one could thus speculate, therefore, that T. gondii could induce the inactivation of a few olfactory receptors important specifically for cat, but not other species. Indeed, recent studies have shown that, for example, cat odour but not fox odour (trimethylthiazoline) activates accessory specific olfactory and defence-related brain regions in rats (staples et al 2008), although the apparent dose sensitivity of the cat odour response may mitigate against this potential explanation (Vyas et al 2007b). Alternatively one may speculate some form of T. gondii-induced alteration to the emotional 'valence' (how negative or positive an emotional response) of cat odour by brain rewiring (lamberton et al 2008).…”