Decreased predator avoidance in parasitized mice: neuromodulatory correlates

Abstract

Although parasites are reported to alter host responses to predators, little is known about the neurochemical mechanisms involved. Using an odour preference test, we examined the effects of an acute, subclinical infection with the naturally occurring, single host, enteric protozoan parasite, Eimeria vermiformis, on the responses of male laboratory mice, Mus musculus, to a predator. Uninfected mice avoided the odour of a predatory cat, spending a minimal amount of time in a Y-maze in the vicinity of the cat odour. In contrast, mice infected with E. vermiformis, spent a significantly greater amount of time in the proximity of the cat odour, showing a reduced avoidance of the cat odour and a reduction in predator-induced fear or anxiety. This was not related to augmented opioid activity and decreased pain sensitivity in the infected mice, as neither treatment with the exogenous opiate, morphine, nor restraint stress-induced augmentation of endogenous opioid activity, had any significant effects on the responses of uninfected mice to cat odour. The altered responses of the infected mice to the cat odour were reduced by peripheral administration of the gamma-aminobutyric A (GABAA) antagonists, bicuculline and picrotoxin, but were not significantly affected by either the benzodiazepine antagonist, Ro 15-1788, the opiate antagonist, naloxone, or the excitatory amino acid, N-methyl-D-aspartate (NMDA) antagonist, MK-801. These results indicate that infection with E. vermiformis in mice reduces the avoidance of predator odour through neurochemical systems associated with anxiety involving, at least in part, GABAA receptor mechanisms.

Adaptive host manipulation by Toxoplasma gondii: fact or fiction?

“…Mice infected with E. vermiformis show a similar decrease in avoidance of cat odour as T. gondii-infected rodents [8]. In the case of E. vermiformis, this cannot be argued to benefit the parasite -if the parasitised mouse is caught by a cat the parasite will die too.…”

“…Instead, the decrease in cat-odour avoidance is interpreted as a coincidental side effect of a general reduction in anxiety and fearfulness [8]. If this behavioural change can be induced by E. vermiformis without being of benefit to the parasite, the same may be true for T. gondii -the decreased fear of cat odour may be co-incidental, rather than an adaptation to enhance transmission to cats.…”

An overview of parasite-induced behavioral alterations – and some lessons from bats

“…Thünken et al, 2010;Perrot-Minnot, 2007;Benesh et al, 2008;Baldauf et al, 2007); there are terrestrial examples of this fearlessness, and even attraction to predators, as well (Kavaliers and Colwell, 1995; The Journal of Experimental Biology 216 (1) THE JOURNAL OF EXPERIMENTAL BIOLOGY Berdoy et al, 2000). This is not, however, the same phenomenon as one involving parasites that alter host odor itself.…”

Parasite dissemination and the pathogenesis of toxoplasmosis

“…The accumulation of infected red blood cells at the placenta allows the transport of infected red blood cells or Plasmodium antigens across the placenta, leading to severe complications that affect fetal development, as reviewed elsewhere (see [40]). For congenital CMV infection, which is considered the most frequent congenital infection in humans, transmission to the fetus is thought to occur by the direct infection of placental tissue, [4] the extracellular migration of the tachyzoite in blood or lymph, [5] intracellular migration, and/or [6] cell-dependent migration with adhesion to the host cell membrane. In order to penetrate tissues sites, such as the placenta, brain or eye, T. gondii may [7] infect the epithelial/endothelial or trophoblast cells that make up the tissue barrier, [8] employ a Trojan horse, and/or [9] enter the tissue via a paracellular or transcellular means.…”

“…The basis for this tropism is uncertain -but could be a consequence of the immune privileged nature of these sites. Alternatively, there are multiple instances of parasites that affect the nervous system of their hosts to alter behaviour and promote predation of intermediate hosts [5][6][7]. For example, Dicrocoelium dendriticum, a flatworm, alters the behaviour of its intermediate host, the ant, to improve the chances of parasite transmission to herbivores (for an entertaining review on parasites and behaviour see [8]).…”