Chronic Toxoplasma Infection Modifies the Structure and the Risk of Host Behavior
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{"title"=>"Chronic toxoplasma infection modifies the structure and the risk of host behavior", "type"=>"journal", "authors"=>[{"first_name"=>"Cristina", "last_name"=>"Afonso", "scopus_author_id"=>"55085721000"}, {"first_name"=>"Vitor B.", "last_name"=>"Paixão", "scopus_author_id"=>"25648393600"}, {"first_name"=>"Rui M.", "last_name"=>"Costa", "scopus_author_id"=>"7203063633"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84858173209", "sgr"=>"84858173209", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0032489", "pmid"=>"22431975", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "pui"=>"364433919"}, "id"=>"d0f4c643-b8c4-3491-ac45-7b9bf120a732", "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.", "link"=>"http://www.mendeley.com/research/chronic-toxoplasma-infection-modifies-structure-risk-host-behavior", "reader_count"=>73, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>19, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>10, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>19, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>10, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>5, "Mathematics"=>1, "Agricultural and Biological Sciences"=>41, "Medicine and Dentistry"=>10, "Arts and Humanities"=>2, "Neuroscience"=>6, "Veterinary Science and Veterinary Medicine"=>1, "Psychology"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Neuroscience"=>{"Neuroscience"=>6}, "Psychology"=>{"Psychology"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>41}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>3}, "Arts and Humanities"=>{"Arts and Humanities"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "United States"=>2, "Japan"=>1, "Brazil"=>2, "Mexico"=>1, "Portugal"=>3}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/667510"], "description"=>"<p>(A) Movement bouts were reduced in animals with brain cysts, relative to control groups. (B) Chronically infected animals moved for longer periods at a time, as evidenced by the increased bout duration. (C,D) Movement structure was changed in cyst-containing mice compared with controls, with a reduction in the number of shorter bouts, and an increase in the frequency of long and very long bouts. (A–D) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.</p>", "links"=>[], "tags"=>["mice", "changes", "exploratory"], "article_id"=>338000, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Toxoplasma_infected_mice_show_changes_in_the_structure_of_exploratory_movement_/338000", "title"=>"<i>Toxoplasma</i>-infected mice show changes in the structure of exploratory movement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:13:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/667824"], "description"=>"<p>(A) Chronically infected mice did not show the bias for closed arm <i>versus</i> open arm occupancy displayed by control groups. Occupancy of the center of the maze was the same across groups and is not represented. (B) The longer visits to closed arms observed in control groups were not detected in animals with brain cysts (ln s – natural logarithm transformation of visit duration in seconds). (C) In contrast with controls, infected animals showed a higher number of visits to the distal-most point of the open arms. (A–C) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19. (D) The control group for parasite injection (n = 20) displayed a bias for closed arm entry, which increased with injected parasite load. Individual animals are represented as closed circles (black) whereas open circles (red) indicate the average values of closed arm entries (above chance) for each parasite load.</p>", "links"=>[], "tags"=>["behaviors", "elevated", "maze", "mice"], "article_id"=>338316, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g006", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Alterations_in_fear_risk_related_behaviors_in_the_elevated_plus_maze_in_mice_with_brain_cysts_/338316", "title"=>"Alterations in fear/risk related behaviors in the elevated plus maze in mice with brain cysts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:18:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/667997"], "description"=>"<p>(A) Cyst frequency and distribution in different mouse brain areas (n = 23). (B) Lorenz curve of cumulative cyst presence in relation to relative brain volume of specific areas. Cyst distribution deviated from perfect equality and was therefore not random. (C) Representation of the quadrant intersection [C1(+) C2(+)] of the cyst localization PCA space (shaded area). Animals with loadings in this quadrant (red dots) were not different from the rest of the animals with brain cysts, for behavioral component F4. (D) Infected animals which co-clustered in the [C1(+) C2(+)] quadrant of the cyst localization PCA space (n = 3) did not show significantly higher factor loadings for behavioral component 4 (F4) than animals that did not cluster in this quadrant (n = 16). (E) Representation of the quadrant intersection [C1(−) C3(−)] of the cyst localization PCA space (shaded area). Animals with high loading values for behavioral component F5 cluster in this quadrant (red dots). (F) Infected animals which co-clustered in the C1(−) C3(−) quadrant of the cyst localization PCA space (n = 7) showed significantly higher factor loadings for behavioral component 5 (F5) than animals that did not cluster in this quadrant (n = 12). Hippoc, hippocampus; Amyg, amygdala; Motor cx, motor cortex; Cpu, caudate putamen; Acc Ncl, accumbens nucleus; VTA, ventral tegmental area; Pirif cx, piriform cortex; Olfac tract, olfactory tract; Somats cx, somatosensory cortex; Aud cx, auditory cortex; Vis cx, visual cortex; Orbital cx, orbital cortex; Thalam, thalamus; Lat sep nucl, lateral septal nucleus; Agrn insl cx, agranular insular cortex; Retrospl dysg cx, retrosplenial dysgranular cortex; Prelimb cx, prelimbic cortex; Periaqued gray, periaqueductal gray; Cg cx, cingulate cortex; Hypothal, hypothalamus; Assoc cx, association cortex.</p>", "links"=>[], "tags"=>["cysts"], "article_id"=>338490, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g008", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Non_random_distribution_of_Toxoplasma_cysts_in_mouse_brains_/338490", "title"=>"Non-random distribution of <i>Toxoplasma</i> cysts in mouse brains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:21:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/668193"], "description"=>"<p>List of brain areas considered in the Lorenz curve analysis and respective brain volumes in mice, according to reference <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032489#pone.0032489-Ma1\" target=\"_blank\">[38]</a>.</p>", "links"=>[], "tags"=>["areas", "considered", "lorenz", "respective", "volumes"], "article_id"=>338677, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.t003", "stats"=>{"downloads"=>1, "page_views"=>35, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_brain_areas_considered_in_the_Lorenz_curve_analysis_and_respective_brain_volumes_in_mice_according_to_reference_38_/338677", "title"=>"List of brain areas considered in the Lorenz curve analysis and respective brain volumes in mice, according to reference [38].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-14 02:24:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/341898", "https://ndownloader.figshare.com/files/341915", "https://ndownloader.figshare.com/files/341932", "https://ndownloader.figshare.com/files/341945", "https://ndownloader.figshare.com/files/341955", "https://ndownloader.figshare.com/files/341973"], "description"=>"<div><p>The intracellular parasite <em>Toxoplasma</em> 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, <em>Toxoplasma</em>-infected rodents display a reduction in the innate fear of predator odor. However, animals with <em>Toxoplasma</em> 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 <em>Toxoplasma</em>-infected mice in environments with exposed <em>versus</em> 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 <em>Toxoplasma</em> 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 <em>Toxoplasma</em> 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 <em>Toxoplasma</em> to broaden its transmission between intermediate predator hosts, in addition to felid definitive hosts.</p> </div>", "links"=>[], "tags"=>["modifies"], "article_id"=>127601, "categories"=>["Cancer", "Neuroscience", "Microbiology", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0032489.s001", "https://dx.doi.org/10.1371/journal.pone.0032489.s002", "https://dx.doi.org/10.1371/journal.pone.0032489.s003", "https://dx.doi.org/10.1371/journal.pone.0032489.s004", "https://dx.doi.org/10.1371/journal.pone.0032489.s005", "https://dx.doi.org/10.1371/journal.pone.0032489.s006"], "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Chronic_Toxoplasma_Infection_Modifies_the_Structure_and_the_Risk_of_Host_Behavior/127601", "title"=>"Chronic <em>Toxoplasma</em> Infection Modifies the Structure and the Risk of Host Behavior", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-03-14 02:06:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/668119"], "description"=>"<p>Factors obtained from principal component analysis of behavioral variables measured in the open field (OF) and elevated plus maze (EPM).</p>", "links"=>[], "tags"=>["variables", "elevated", "maze"], "article_id"=>338609, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Factors_obtained_from_principal_component_analysis_of_behavioral_variables_measured_in_the_open_field_OF_and_elevated_plus_maze_EPM_/338609", "title"=>"Factors obtained from principal component analysis of behavioral variables measured in the open field (OF) and elevated plus maze (EPM).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-14 02:23:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/667930"], "description"=>"<p>Factor scores were calculated for individual animals in the different experimental groups using loadings derived from PCA. Animals with brain cysts showed different loadings from control groups for Factors 4 (F4) and 5 (F5). Factor 2 (F2) loadings were different in cyst-containing mice compared with saline injected animals, but similar to infection control mice with no cysts.</p>", "links"=>[], "tags"=>["scores", "derived", "elevated", "maze"], "article_id"=>338416, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g007", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Factorial_scores_derived_from_principal_component_analysis_of_open_field_and_elevated_plus_maze_variables_/338416", "title"=>"Factorial scores derived from principal component analysis of open field and elevated plus maze variables.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:20:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/668157"], "description"=>"<p>Factors obtained from principal component analysis of cyst distribution across brain areas.</p>", "links"=>[], "tags"=>["cyst"], "article_id"=>338652, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.t002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Factors_obtained_from_principal_component_analysis_of_cyst_distribution_across_brain_areas_/338652", "title"=>"Factors obtained from principal component analysis of cyst distribution across brain areas.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-03-14 02:24:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/667741"], "description"=>"<p>(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.</p>", "links"=>[], "tags"=>["elevated", "maze", "mice"], "article_id"=>338233, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Altered_behavior_in_the_elevated_plus_maze_in_mice_with_chronic_Toxoplasma_infection_/338233", "title"=>"Altered behavior in the elevated plus maze in mice with chronic <i>Toxoplasma</i> infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:17:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/667588"], "description"=>"<p>(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.</p>", "links"=>[], "tags"=>["alterations", "exposed", "non-exposed", "areas"], "article_id"=>338076, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Different_behavioral_alterations_in_exposed_versus_non_exposed_areas_of_the_open_field_/338076", "title"=>"Different behavioral alterations in exposed <i>versus</i> non-exposed areas of the open field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:14:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/667285"], "description"=>"<p>(A) Weight variation during infection. Acute infection resulted in severe weight loss in the first two weeks, followed by a recovery phase, with animals returning to initial weight values nine weeks post-injection (dotted line). (B) All animals with acute weight loss (>5%) during the first two weeks post-infection developed brain cysts. (A,B) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19. (C) Immunofluorescence and phase contrast images of GFP-expressing cysts in the mouse brain. DNA was artificially stained in red. (D) Efficiency of chronic infection increased with number of parasites injected (injected animals: 1000 parasites n = 14; 10 000 parasites n = 13; 100 000 parasites n = 21). (E) Average number of cysts formed in the mouse brain did not depend on the number of parasites injected (1000 parasites n = 1 out of 14; 10 000 parasites n = 5 out of 13; 100 000 parasites n = 17 out of 21).</p>", "links"=>[], "tags"=>["Infectious diseases", "microbiology", "neuroscience", "Evolutionary biology"], "article_id"=>337775, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dynamics_of_Toxoplasma_infection_in_C57BL_6J_mice_/337775", "title"=>"Dynamics of <i>Toxoplasma</i> infection in C57BL/6J mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:09:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/667432"], "description"=>"<p>(A) Compared to control animals, infected mice showed an increase in the total distance travelled in the arena. (B) Animals that contain brain cysts moved at higher speeds in the open field than controls. (C) The initial acceleration during a movement bout was higher in animals with brain cysts. Centesimal values indicate line slopes in one second intervals. (D) Infected animals showed no latency to move after being placed in the open field, in contrast to control groups. (E) In contrast to what was observed in control animals, no habituation to the novel environment was observed in infected animals, as shown by the absence of the reduction in locomotion over time. (F) The distance covered was more uniform over time in cyst-containing animals, as indicated by the reduced coefficient of variation when compared to control groups. (A–F) Saline group, n = 10; No cysts group, n = 20; Brain cysts group, n = 19.</p>", "links"=>[], "tags"=>["infected", "mice", "alterations", "exploratory"], "article_id"=>337919, "categories"=>["Microbiology", "Neuroscience", "Infectious Diseases", "Evolutionary Biology"], "users"=>["Cristina Afonso", "Vitor B. Paixão", "Rui M. Costa"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0032489.g002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chronically_infected_mice_display_alterations_in_exploratory_behavior_in_the_open_field_/337919", "title"=>"Chronically infected mice display alterations in exploratory behavior in the open field.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-03-14 02:11:59"}

PMC Usage Stats | Further Information

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Relative Metric

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