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Poorer results of mice with latent toxoplasmosis in learning tests: impaired learning processes or the novelty discrimination mechanism?

Published online by Cambridge University Press:  20 April 2007

H. HODKOVA ,
P. KODYM  and
J. FLEGR
H. HODKOVA
Affiliation:
Department of Parasitology, 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 10042, Czech Republic
J. FLEGR*
Affiliation:
Department of Parasitology, Charles University, Viničná 7, Prague 128 44, Czech Republic
*
*Corresponding author: Department of Parasitology, Charles University, Viničná 7, Prague 128 44, Czech Republic. Tel: +420-221951821. Fax: +420-224919704. E-mail: [email protected]
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Summary

The heteroxenous protozoan parasite Toxoplasma gondii is transmitted from the intermediate host (any warm-blooded animal) to the definitive host (members of the felidae) by carnivory. The infected intermediate hosts develop several specific behavioural changes that are usually considered products of manipulative activity of the parasite aimed to increase the probability of its transmission to the definitive host. Among other changes, the infected rodents were shown to have impaired learning capability. All previous studies were done 2–6 weeks after the infection. Therefore, it was difficult to resolve whether the observed impairment of learning processes was a result of acute or latent toxoplasmosis, i.e. whether it was a side-effect of the disease or a product of manipulation activity. Here we studied the learning capability of Toxoplasma-infected mice in the static rod test and 8-arm radial maze test and their spontaneous activity in the wheel running test 10 weeks after the infection. The infected mice achieved worse scores in the learning tests but showed higher spontaneous activity in the wheel running test. However, a detailed study of the obtained results as well as of the data reported by other authors suggested that the differences between infected and control mice were a result of impaired ability to recognize novel stimuli rather than of impaired learning capacity in animals with latent toxoplasmosis.

Keywords

Toxoplasmalatent toxoplasmosisnovelty seekingdopaminemanipulation hypothesisparasite
Type
Research Article
Information
Parasitology , Volume 134 , Issue 10 , September 2007 , pp. 1329 - 1337
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Alonso, R., Chaudieu, I., Diorio, J., Krishnamurthy, A., Quirion, R. and Boksa, P. (1993). Interleukin-2 modulates evoked release of [3H]dopamine in rat cultured mesencephalic cells. Journal of Neurochemistry 61, 1284–1290.CrossRefGoogle ScholarPubMed
Bachmann, S., Schroder, J., Bottmer, C., Torrey, E. F. and Yolken, R. H. (2005). Psychopathology in first-episode schizophrenia and antibodies to Toxoplasma gondii. Psychopathology 38, 87–90.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Creese, I., Burt, D. R. and Snyder, S. H. (1976). Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 192, 481–483.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Flegr, J. (2007). Effects of Toxoplasma on human behavior. Schizophrenia Bulletin PMID: 17218612.Google Scholar
Flegr, J., Hruskova, M., Hodny, Z., Novotna, M. and Hanusova, J. (2005). Body height, body mass index, waist-hip ratio, fluctuating asymmetry and second to fourth digit ratio in subjects with latent toxoplasmosis. Parasitology 130, 621–628.CrossRefGoogle ScholarPubMed
Flegr, J., Preiss, M., Klose, J., Havliček, 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. Dopamine, a missing link between schizophrenia and toxoplasmosis? Biological Psychology 63, 253–268.CrossRefGoogle ScholarPubMed
Gross, U. (1996). Toxoplasma gondii research in Europe. Parasitology Today 12, 1–4.CrossRefGoogle Scholar
Hay, J., Aitken, P. P. and Arnott, M. A. (1985). The influence of Toxoplasma infection on the spontaneous running activity of mice. Zeitschrift für Parasitenkunde 71, 459–462.CrossRefGoogle ScholarPubMed
Hay, J., Aitken, P. P. and Graham, D. I. (1984). Toxoplasma infection and response to novelty in mice. Zeitschrift für Parasitenkunde 70, 575–588.CrossRefGoogle ScholarPubMed
Hay, J., Hutchison, W. M., Aitken, P. P. and Graham, D. I. (1983). The effect of congenital and adult-acquired Toxoplasma infections on activity and responsiveness to novel stimulation in mice. Annals of Tropical Medicine and Parasitology 77, 483–495.CrossRefGoogle ScholarPubMed
Holliman, R. E. (1997). Toxoplasmosis, behaviour and personality. Journal of Infection 35, 105–110.CrossRefGoogle ScholarPubMed
Holmes, J. 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.Google Scholar
Hrdá, S., Votypka, J., Kodym, P. and Flegr, J. (2000). Transient nature of Toxoplasma gondii-induced behavioral changes in mice. Journal of Parasitology 86, 657–663.CrossRefGoogle ScholarPubMed
Hubscher, C. H., Brooks, D. L. and Johnson, J. R. (2005). A quantitative method for assessing stages of the rat estrous cycle. Biotechnic and Histochemistry 80, 79–87.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Aitken, P. P. and Wells, B. W. P. (1980 a). Chronic Toxoplasma infection and familiarity-novelty discrimination in the mouse. Annals of Tropical Medicine and Parasitology 74, 145–150.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Aitken, P. P. and Wells, B. W. P. (1980 b). Chronic Toxoplasma infections and motor performance in the mouse. Annals of Tropical Medicine and Parasitology 74, 505–510.Google ScholarPubMed
Hutchison, W. M., Bradley, M., Cheyne, W. M., Wells, B. W. P. and Hay, J. (1980 c). Behavioural abnormalities in Toxoplasma-infected mice. Annals of Tropical Medicine and Parasitology 74, 337–345.CrossRefGoogle Scholar
Hutchison, W. M. and Work, K. (1969). Toxoplasma – A versatile parasite. New Scientist 29, 464–466.Google 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 Behavior 59, 361–367.CrossRefGoogle ScholarPubMed
Kabbaj, M. and Akil, H. (2001). Individual differences in novelty-seeking behavior in rats: A c-fos study. Neuroscience 106, 535–545.CrossRefGoogle ScholarPubMed
Kaňková, S., Sulc, J., Nouzová, K., Fajfrlik, K., Frynta, D. and Flegr, J. (2007). Women infected with parasite Toxoplasma have more sons. Naturwissenschaften 94, 122–127.CrossRefGoogle ScholarPubMed
Kodym, P., Blažek, K., Malý, M. and Hrdá, S. (2002). Pathogenesis of experimental toxoplasmosis in mice with strains differing in virulence. Acta Parasitologica 47, 239–248.Google Scholar
Kramer, W. (1966). Frontiers of neurological diagnosis in acquired toxoplasmosis. Psychiatria, Neurologia, Neurochirurgia 69, 43–64.Google ScholarPubMed
Ladee, G. A., Scholten, J. M. and Meyes, F. E. P. (1966). Diagnostic problems in psychiatry with regard to acquired toxoplasmosis. Psychiatria, Neurologia, Neurochirurgia 69, 65–82.Google ScholarPubMed
Minto, A. and Roberts, F. J. (1959). The psychiatric complications of toxoplasmosis. Lancet 1, 1180–1182.CrossRefGoogle ScholarPubMed
Nieoullon, A. (2002). Dopamine and the regulation of cognition and attention. Progress in Neurobiology 67, 53–83.CrossRefGoogle ScholarPubMed
Novotná, M., Hanušová, J., Klose, J., Preiss, M., Havlíček, J., Roubalová, K. and Flegr, J. (2005). Probable neuroimmunological link between Toxoplasma and cytomegalovirus infections and personality changes in the human host. BMC Infectious Diseases 54, 1–10.Google Scholar
Petitto, J. M., McCarthy, D. B., Rinker, C. M., Huang, Z. and Getty, T. (1997). Modulation of behavioral and neurochemical measures of forebrain dopamine function in mice by species-specific interleukin-2. Journal of Neuroimmunology 73, 183–190.CrossRefGoogle ScholarPubMed
Piekarski, G., Zippelius, H. M. and Witting, P. A. (1978). Auswirkungen einer latenten Toxoplasma-Infektion auf das Lernvermogen von weissen Laboratoriumsratten und Mausen. Zeitschrift für Parasitenkunde 57, 1–15.CrossRefGoogle Scholar
Sawa, A. and Snyder, S. H. (2002). Schizophrenia: diverse approaches to a complex disease. Science 296, 692–695.CrossRefGoogle ScholarPubMed
Skallová, A., Frynta, D., Kodym, P. and Flegr, J. (2006). The role of dopamine in Toxoplasma-induced behavioural alterations in mice: an ethological and ethopharmacological study. Parasitology 133, 525–535.CrossRefGoogle ScholarPubMed
Skallová, A., Novotná, M., Kolbeková, P., Gasová, Z., Veselý, V. and Flegr, J. (2005). Decreased level of novelty seeking in blood donors infected with Toxoplasma. Neuroendocrinology Letters 26, 480–486.Google ScholarPubMed
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 ScholarPubMed
Tarr, B. A., Kellaway, L. A., Gibson, A. S. and Russell, V. A. (2004). Voluntary running distance is negatively correlated with striatal dopamine release in untrained rats. Behavioural Brain Research 154, 493–499.CrossRefGoogle ScholarPubMed
Torrey, E. F. and Yolken, R. H. (2003). Toxoplasma gondii and schizophrenia. Emerging Infectious Diseases 9, 1375–1380.CrossRefGoogle ScholarPubMed
Viggiano, D., Vallone, D., Ruocco, L. A. and Sadile, A. G. (2003). Behavioural, pharmacological, morpho-functional molecular studies reveal a hyperfunctioning mesocortical dopamine system 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 ScholarPubMed
Witting, P. A. (1979). Learning capacity and memory of normal and Toxoplasma-infected laboratory rats and mice. Zeitschrift für Parasitenkunde 61, 29–51.CrossRefGoogle ScholarPubMed