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Chronic Toxoplasma infection modifies the structure and the risk of host behavior.

Afonso C, Paixão VB, Costa RM - PLoS ONE (2012)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Champalimaud Neuroscience Programme, Instituto Gulbenkian de Ciência, Oeiras, Portugal.

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.

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Altered behavior in the elevated plus maze in mice with chronic Toxoplasma infection.(A) Infected animals exhibited an increase in the distance travelled in the apparatus relative to controls. (B) Cyst-containing animals covered longer distances than control groups in the open arms. (C) Overall average speed remained unaffected across all experimental groups. (D) In contrast to control groups, infected animals displayed higher speed in closed arms than in open arms. (A–D) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
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pone-0032489-g005: Altered behavior in the elevated plus maze in mice with chronic Toxoplasma infection.(A) Infected animals exhibited an increase in the distance travelled in the apparatus relative to controls. (B) Cyst-containing animals covered longer distances than control groups in the open arms. (C) Overall average speed remained unaffected across all experimental groups. (D) In contrast to control groups, infected animals displayed higher speed in closed arms than in open arms. (A–D) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.

Mentions: The behavioral alterations reported above in animals with brain cysts suggested that these animals behaved differently in exposed versus non-exposed areas when compared to controls. To further characterize this behavior, we used the elevated plus maze test which can reliably assess unconditioned fear-related responses in rodents (reviewed in [18]). This apparatus consisted of four arms (two open and two closed) arranged in a plus shape and elevated from the floor. The test relies upon the innate preference for dark, enclosed spaces and the unconditioned fear of heights/open spaces exhibited by mice; closed arms constitute safe zones whereas open arms represent unsafe areas. Consistent with the results obtained in the open field, animals with brain cysts showed an increase in the overall distance travelled during the 5 min test (Figure 5A, F(2,45) = 9.18, p<0.05), when compared to control groups. Further analysis revealed that this difference in locomotion between groups emerged primarily because animals with brain cysts displayed increased locomotion in open arms compared to controls (Figure 5B, Fw(2,21.8) = 5.08, p<0.05, post hoc tests for cyst-containing mice versus controls, p<0.05; Video S5 and Video S6). Moreover, even though no striking differences were detected in overall speed between groups (Figure 5C, p>0.05), cyst-containing animals moved faster in the closed arms than in the open arms (Figure 5D, F(2,45) = 3.56, p<0.05, post hoc tests p<0.05).


Chronic Toxoplasma infection modifies the structure and the risk of host behavior.

Afonso C, Paixão VB, Costa RM - PLoS ONE (2012)

Altered behavior in the elevated plus maze in mice with chronic Toxoplasma infection.(A) Infected animals exhibited an increase in the distance travelled in the apparatus relative to controls. (B) Cyst-containing animals covered longer distances than control groups in the open arms. (C) Overall average speed remained unaffected across all experimental groups. (D) In contrast to control groups, infected animals displayed higher speed in closed arms than in open arms. (A–D) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3303785&req=5

pone-0032489-g005: Altered behavior in the elevated plus maze in mice with chronic Toxoplasma infection.(A) Infected animals exhibited an increase in the distance travelled in the apparatus relative to controls. (B) Cyst-containing animals covered longer distances than control groups in the open arms. (C) Overall average speed remained unaffected across all experimental groups. (D) In contrast to control groups, infected animals displayed higher speed in closed arms than in open arms. (A–D) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
Mentions: The behavioral alterations reported above in animals with brain cysts suggested that these animals behaved differently in exposed versus non-exposed areas when compared to controls. To further characterize this behavior, we used the elevated plus maze test which can reliably assess unconditioned fear-related responses in rodents (reviewed in [18]). This apparatus consisted of four arms (two open and two closed) arranged in a plus shape and elevated from the floor. The test relies upon the innate preference for dark, enclosed spaces and the unconditioned fear of heights/open spaces exhibited by mice; closed arms constitute safe zones whereas open arms represent unsafe areas. Consistent with the results obtained in the open field, animals with brain cysts showed an increase in the overall distance travelled during the 5 min test (Figure 5A, F(2,45) = 9.18, p<0.05), when compared to control groups. Further analysis revealed that this difference in locomotion between groups emerged primarily because animals with brain cysts displayed increased locomotion in open arms compared to controls (Figure 5B, Fw(2,21.8) = 5.08, p<0.05, post hoc tests for cyst-containing mice versus controls, p<0.05; Video S5 and Video S6). Moreover, even though no striking differences were detected in overall speed between groups (Figure 5C, p>0.05), cyst-containing animals moved faster in the closed arms than in the open arms (Figure 5D, F(2,45) = 3.56, p<0.05, post hoc tests p<0.05).

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Champalimaud Neuroscience Programme, Instituto Gulbenkian de Ciência, Oeiras, Portugal.

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.

Show MeSH
Related in: MedlinePlus