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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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Different behavioral alterations in exposed versus non-exposed areas of the open field.(A) Infected animals did not show an altered preference for center area occupancy. (B) Animals with brain cysts displayed increased locomotion in both zones of the arena when compared with control groups. (C) In contrast to Saline animals, cyst-containing mice engaged in locomotion preferentially in the center zone. (D,E) Chronically infected animals showed a smaller number and percentage of non-locomoting periods in the center zone (F) Infected animals displayed a reduction in percent time freezing exclusively in the center zone. (G) The number of rearings against the arena walls was higher in animals with brain cysts than in control groups. (A–G) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
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pone-0032489-g004: Different behavioral alterations in exposed versus non-exposed areas of the open field.(A) Infected animals did not show an altered preference for center area occupancy. (B) Animals with brain cysts displayed increased locomotion in both zones of the arena when compared with control groups. (C) In contrast to Saline animals, cyst-containing mice engaged in locomotion preferentially in the center zone. (D,E) Chronically infected animals showed a smaller number and percentage of non-locomoting periods in the center zone (F) Infected animals displayed a reduction in percent time freezing exclusively in the center zone. (G) The number of rearings against the arena walls was higher in animals with brain cysts than in control groups. (A–G) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.

Mentions: The longer bouts of movement described above could reflect periods of uninterrupted movement spanning both the center and border zones of the open field. We therefore analyzed in more detail the structure of behavior in the center and border zones. Mice will normally avoid the more exposed area (center zone) in favor of the protected one (border zone, close to arena walls, reviewed in [16], [17]). We found that, for all groups, animals spent more time in the border area, with no significant differences in center occupancy (Figure 4A, FR(2,46)R = 0.83, ns). Furthermore, chronically infected animals showed increased locomotion both in the center (Figure 4B, FwR(2,25.3)R = 6.13, p<0.05) and border zones (Fig. 4B, FwR(2,25)R = 4.98, p<0.05) of the arena. We then investigated if the different experimental groups showed distinct patterns of behavior during the time spent in the different zones of the open field. In fact, Saline control mice spent less time engaged in locomotion in the center when compared with the border zone (Figure 4C, t(9) = −5.40, p<0.05), while no such difference was found in the No-cysts group. In contrast, cyst-containing animals showed a reversal of this preference, spending more time engaged in locomotion in the center when compared to the border zone (Figure 4C, t(18) = 4.50, p<0.05).


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

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

Different behavioral alterations in exposed versus non-exposed areas of the open field.(A) Infected animals did not show an altered preference for center area occupancy. (B) Animals with brain cysts displayed increased locomotion in both zones of the arena when compared with control groups. (C) In contrast to Saline animals, cyst-containing mice engaged in locomotion preferentially in the center zone. (D,E) Chronically infected animals showed a smaller number and percentage of non-locomoting periods in the center zone (F) Infected animals displayed a reduction in percent time freezing exclusively in the center zone. (G) The number of rearings against the arena walls was higher in animals with brain cysts than in control groups. (A–G) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3303785&req=5

pone-0032489-g004: Different behavioral alterations in exposed versus non-exposed areas of the open field.(A) Infected animals did not show an altered preference for center area occupancy. (B) Animals with brain cysts displayed increased locomotion in both zones of the arena when compared with control groups. (C) In contrast to Saline animals, cyst-containing mice engaged in locomotion preferentially in the center zone. (D,E) Chronically infected animals showed a smaller number and percentage of non-locomoting periods in the center zone (F) Infected animals displayed a reduction in percent time freezing exclusively in the center zone. (G) The number of rearings against the arena walls was higher in animals with brain cysts than in control groups. (A–G) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.
Mentions: The longer bouts of movement described above could reflect periods of uninterrupted movement spanning both the center and border zones of the open field. We therefore analyzed in more detail the structure of behavior in the center and border zones. Mice will normally avoid the more exposed area (center zone) in favor of the protected one (border zone, close to arena walls, reviewed in [16], [17]). We found that, for all groups, animals spent more time in the border area, with no significant differences in center occupancy (Figure 4A, FR(2,46)R = 0.83, ns). Furthermore, chronically infected animals showed increased locomotion both in the center (Figure 4B, FwR(2,25.3)R = 6.13, p<0.05) and border zones (Fig. 4B, FwR(2,25)R = 4.98, p<0.05) of the arena. We then investigated if the different experimental groups showed distinct patterns of behavior during the time spent in the different zones of the open field. In fact, Saline control mice spent less time engaged in locomotion in the center when compared with the border zone (Figure 4C, t(9) = −5.40, p<0.05), while no such difference was found in the No-cysts group. In contrast, cyst-containing animals showed a reversal of this preference, spending more time engaged in locomotion in the center when compared to the border zone (Figure 4C, t(18) = 4.50, 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