Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-19T02:10:15.777Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study

Published online by Cambridge University Press:  02 August 2006

A. SKALLOVÁ ,
P. KODYM ,
D. FRYNTA  and
J. FLEGR
A. SKALLOVÁ
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Viničná 7, Prague 128 44, Czech Republic
P. KODYM
Affiliation:
National Reference Laboratory for Toxoplasmosis, National Institute of Public Health, šrobárova 48, Prague 100 42, Czech Republic
D. FRYNTA
Affiliation:
Department of Zoology, Faculty of Science, Charles University, Viničná 7, Prague 128 44, Czech Republic
J. FLEGR
Affiliation:
Department of Parasitology, Faculty of Science, Charles University, Viničná 7, Prague 128 44, Czech Republic
Get access Rights & Permissions [Opens in a new window]

Abstract

Toxoplasma gondii, a cosmopolitan protozoan parasite, is known to induce behavioural alterations in rodents and may exert an effect on human personality and behaviour. The mechanism of parasite-induced alterations in host behaviour has not been described, but it was hypothesized that development of Toxoplasma tissue cysts in the brain could affect the dopaminergic neuromodulatory system. In this study, we tested the effect of latent Toxoplasma infection on mouse behaviour associated with activity of the dopaminergic system, i.e. locomotion in a novel environment and exploration test. Additionally, we examined the behavioural response of Toxoplasma-infected mice to a selective dopamine uptake inhibitor, GBR 12909. In both genders, Toxoplasma infection decreased locomotion in the open field. Infected females displayed an increased level of exploration in the holeboard test. GBR 12909 induced suppression in holeboard-exploration in the infected males, but had an opposite effect on the controls. These results suggest an association between Toxoplasma gondii infection and changes in the dopaminergic neuromodulatory system.

Keywords

parasitedopamineexplorationholeboardGBR 12909
Type
Research Article
Information
Parasitology , Volume 133 , Issue 5 , November 2006 , pp. 525 - 535
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Berdoy, M., Webster, J. P. and Macdonald, D. W. ( 1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology 111, 403–409.Google Scholar
Berdoy, M., Webster J. P. and Macdonald, D. W. ( 2000). Fatal attraction in rats infected with Toxoplasma gondii. Proceedings of the Royal Society of London, B 267, 1591–1594.CrossRefGoogle Scholar
Cloninger, C. R., Svrakic D. M. and Przybeck T. R. ( 1993). A psychobiological model of temperament and character. Archives of General Psychiatry 50, 975–990.CrossRefGoogle Scholar
Contet, C., Rawlins, N. and Deacon, R. M. J. ( 2001). A comparison of 129S2/SvHsd and C57BL/6JOlaHsd mice on a test battery assessing sensorimotor, affective and cognitive behaviours, implications for the study of genetically modified mice. Behavioural Brain Research 124, 33–46.CrossRefGoogle Scholar
Corr, P. J. and Kumari, V. ( 2000). Individual differences in mood reactions to d-amphetamine, a test of three personality factors. Journal of Psychopharmacology 14, 371–377.CrossRefGoogle Scholar
Crawley, J. N., Belknap, J. K., Collins, A., Crabbe, J. C., Frankel, W., Henderson, N., Hitzemann, R. J., Maxson, S. C., Miner, L. L., Silva, A., Wehner, J., Wynshaw-Boris, A. and Paylor, R. ( 1997). Behavioral phenotypes of inbred mouse strains, implication and recommendations for molecular studies. Psychopharmacology 132, 107–124.CrossRefGoogle Scholar
Darcy, F. and Santoro, F. ( 1994). Toxoplasmosis. In Parasitic Infections and the Immune System ( ed. Kierszenbaum, F.), pp. 163–201. Academic Press, San Diego.CrossRef
Deacon, R. M. J., Croucher, A. and Rawlins, J. N. ( 2002). Hippocampal cytotoxic lesion effects on species-typical behaviours in mice. Behavioural Brain Research 132, 203–213.CrossRefGoogle Scholar
Dellu, F., Piazza, P. V., Mayo, W., LeMoal, M. and Simon, H. ( 1996). Novelty-seeking in rats – biobehavioral characteristics and possible relationship with the sensatin-seeking trait in man. Neuropsychobiology 34, 136–145.CrossRefGoogle Scholar
Denkers, E. Y. and Gazzelini, R. T. ( 1998). Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection. Clinical Microbiology Reviews 11, 569–588.Google Scholar
Dow-Edwards, D. L. and Busidan, Y. ( 2001). Behavioral responses to dopamine agonists in adult rats exposed to cocaine during preweaning period. Pharmacology, Biochemistry, and Behavior 70, 23–30.CrossRefGoogle Scholar
Fernandes, C., González, M. L., Wilson, C. A. and File, S. E. ( 1999). Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacology Biochemistry and Behavior 64, 731–738.CrossRefGoogle Scholar
File, S. E. ( 2001). Factors controlling measures of anxiety and responses to novelty in the mouse. Behavioural Brain Research 125, 151–157.CrossRefGoogle Scholar
Flegr, J., Preiss, M., Klose, J., Havlíček, J., Vitáková, M. and Kodym, P. ( 2003). Decreased level of psychobiological factor novelty seeking and lower intelligence in men latently infected with the protozoan parasite Toxoplasma gondii. Biological Psychology 63, 253–268.CrossRefGoogle Scholar
Frenkel, J. K. ( 1988). Patophysiology of Toxoplasmosis. Parasitology Today 4, 273–278.CrossRefGoogle Scholar
Gebhardt, Ch., Leisch, F., Schüssler, P., Fuchs, K., Stompe, T., Sieghart, W., Hornik, K., Kasper, S. and Aschauer, H. N. ( 2000). Non-association of dopamine D4 and D2 receptor genes with personality in healthy individuals. Psychiatric Genetics 10, 1–7.CrossRefGoogle Scholar
Hansenne, M., Pinto, E., Pitchot, W., Reggers, J., Scantamburlo, G., Moor, M. and Ansseau, M. ( 2002). Further evidence on the relationship between dopamine and novelty seeking, a neuroendocrine study. Personality and Individual Differences 33, 967–977.CrossRefGoogle Scholar
Hay, J., Hutchison, W. M., Aitken, P. P. and Graham, D. I. ( 1983). The effect of congenital and adult-aquired Toxoplasma infections on activity and responsiveness to novel stimulation in mice. Annals of Tropical Medicine and Parasitology 77, 483–495.CrossRefGoogle Scholar
Hay, J., Aitken, P. P., Hair, D. M., Hutchison, W. M. and Graham, D. I. ( 1984 a). The effect of congenital Toxoplasma infection on mouse activity and relative preference for exposed areas over a series of trials. Annals of Tropical Medicine and Parasitology 78, 611–618.Google Scholar
Hay, J., Aitken, P. P. and Graham, D. I. ( 1984 b). Toxoplasma infection and response to novelty in mice. Zeitschrift für Parasitenkunde 70, 575–587.Google Scholar
Hay, J., Aitken, P. P. and Arnott, M. A. ( 1985). The influence of congenital Toxoplasma infection on the spontaneous running activity of mice. Zeitschrift für Parasitenkunde 71, 459–462.CrossRefGoogle Scholar
Holmes, J. C. and Bethel, W. M. ( 1972). Modification of intermidiate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission ( ed. Canning, E. U. and Wright, C. A.), pp. 123–149. Academic Press, London.
Hrdá, š., Votýpka, J., Kodym, P. and Flegr, J. ( 2000). Transient nature of Toxoplasma gondii-induced behavioral changes in mice. Journal of Parasitology 86, 657–663.CrossRefGoogle Scholar
Hutchison, W. M., Bradley, M., Cheyne, W. M., Wells, B. W. P. and Hay, J. ( 1980 a). Behavioural abnormalities in Toxoplasma-infected mice. Annals of Tropical Medicine and Parasitology 74, 337–345.Google Scholar
Hutchison, W. M., Aitken, P. P. and Wells, B. W. P. ( 1980 b). Chronic Toxoplasma infections and familiarity-novelty discrimination in the mouse. Annals of Tropical Medicine and Parasitology 74, 145–150.Google Scholar
Hutchison, W. M., Aitken, P. P. and Wells, B. W. P. ( 1980 c). Chronic Toxoplasma infections and motor performance in the mouse. Annals of Tropical Medicine and Parasitology 74, 507–510.Google Scholar
Irifune, M., Nomoto, M. and Fukuda, T. ( 1995). Effects of GBR 12909 on locomotor activity and dopamine turnover in mice, comparison with apomorphine. European Journal of Pharmacology 272, 79–85.CrossRefGoogle Scholar
Jones, B. C., Hou, X. and Cook, M. N. ( 1996). Effect of exposure to novelty on brain monoamines in C57BL/6 and DBA/2 mice. Physiology and Behaviour 59, 361–367.CrossRefGoogle Scholar
Kabbaj, M. and Akil, H. ( 2001). Individual differences in novelty-seeking behavior in rats, a c-fos study. Neuroscience 106, 535–545.CrossRefGoogle Scholar
Kodym, P., Blažek, K., Malý, M. and Hrdá, š. ( 2002). Pathogenesis of experimental toxoplasmosis in mice with strains differing in virulence. Acta Parasitologica 47, 239–248.Google Scholar
Lee, Y. H., Channon J. Y., Matsuura, T., Schwartzman, J. D., Shin, D. W. and Kasper, L. H. ( 1999). Functional and quantitative analysis of splenic T cell immune responses following oral Toxoplasma gondii infection in mice. Experimental Parasitology 91, 212–221.Google Scholar
Lipp, H. P. and Wolfer, D. P. ( 2003). Genetic background problems in the analysis of cognitive and neuronal changes in genetically modified mice. Clinical Neuroscience Research 3, 223–231.CrossRefGoogle Scholar
Mazei, M. S., Pluto, C. P., Kirkbride, B. and Pehek, E. A. ( 2002). Effects of catecholamine uptake blockers in the caudate-putamen and subregions of the medial prefrontal cortex of the rat. Brain Research 936, 58–67.CrossRefGoogle Scholar
McLeod, R., Eisenhauer, P., Mack, D., Brown, C., Filice, G. and Spitalny, G. ( 1989). Immune responses associated with early survival after peroral infection with Toxoplasma gondii. Journal of Immunology 142, 3247–3255.Google Scholar
Nieoullon, A. ( 2002). Dopamine and regulation of cognition and attention. Progress in Neurobiology 67, 53–83.CrossRefGoogle Scholar
Piekarski, G., Zippelius, H. M. and Witting, P. A. ( 1978). Auswirkungen einer latenten Toxoplasma-Infektion auf das Lernvermogen von weissen Laboratoriumsratten and mausen. Zeitschrift für Parasitenkunde 57, 1–15.Google Scholar
Powell, S. B., Paulus, M. P., Hartman, D. S., Godel, T. and Geyer, M. A. ( 2003). RO-10-5824 is a selective dopamine D4 receptor agonist that increases novel object exploration in C57 mice. Neuropharmacology 44, 473–481.CrossRefGoogle Scholar
Prut, L. and Belzung, C. ( 2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors, a review. European Journal of Pharmacology 463, 3–33.CrossRefGoogle Scholar
Puglisi-Allegra, S. and Cabib, S. ( 1997). Psychopharmacology of dopamine, The contribution of comparative studies in inbred strains of mice. Progress in Neurobiology 51, 637–661.CrossRefGoogle Scholar
Rogers, D. C., Jones, D. N. C., Nelson, P. R., Jones, C. M., Quilter, Ch. A., Robinson, T. L. and Hagan, J. J. ( 1999). Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behavioural Brain Research 105, 207–217.CrossRefGoogle Scholar
Stahle, L. ( 1992). Do autoreceptors mediate dopamine agonist-induced yawning and suppression of exploration? Psychopharmacology 106, 1–13.Google Scholar
Stahle, L. and Ungerstedt, U. ( 1986). Different behavioural patterns induced by the dopamine agonist apomorphine analysed by multivariate statistics. Pharmacology, Biochemistry, and Behavior 24, 291–298.CrossRefGoogle Scholar
Stahle, L. and Ungerstedt, U. ( 1987). On the mode of action of six putative dopamine receptor agonists on suppression of exploratory behaviour in rats. Psychopharmacology 91, 139–146.Google Scholar
Stibbs, H. H. ( 1985). Changes in brain concentrations of catecholamines and indoleamines in Toxoplasma gondii infected mice. Annals of Tropical Medicine and Parasitology 79, 153–157.CrossRefGoogle Scholar
Tang, X. and Sanford, L. D. ( 2005). Home cage activity and activity-based measures of anxiety in 129P3/J, 129X1/SvJ and C57BL/6J mice. Physiology and Behaviour 84, 105–115.CrossRefGoogle Scholar
Thiel, C. M., Muller, C. P., Huston, J. P. and Schwarting, R. K. ( 1999). High versus low reactivity to novel environment, behavioural, pharmacological and neurochemical assassments. Neuroscience 93, 243–251.CrossRefGoogle Scholar
Viggiano, D., Vallone, D., Ruocco, L. A. and Sadile, A. G. ( 2003). Behavioural, pharmacological, morpho-functional molecular studies reveal a hyperfunctioning mesocortical dopamine systém in an animal model of attention deficit and hyperactivity disorder. Neuroscience and Biobehavioral Reviews 27, 683–689.CrossRefGoogle Scholar
Webster, J. P., Brunton, C. F. A. and Macdonald, D. W. ( 1994). Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109, 37–43.CrossRefGoogle Scholar
Webster, J. P. ( 1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583–589.CrossRefGoogle Scholar
Westerink, B. H. C., Damsma, J. B., De Vries, J. B. and Koning, H. ( 1987). Dopamine re-uptake inhibitors show inconsistent effects on the in vivo release of dopamine as measured by intracerebral dialysis in the rat. European Journal of Pharmacology 135, 123–129.CrossRefGoogle Scholar
Witting, P. A. ( 1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Zeitschrift für Parasitenkunde 61, 29–51.CrossRefGoogle Scholar