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Reduced spatial learning in mice infected with the nematode, Heligmosomoides polygyrus

Published online by Cambridge University Press:  06 April 2009

M. Kavaliers  and
D. D. Colwell
M. Kavaliers
Affiliation:
Division of Oral Biology, Faculty of Dentistry and Neuroscience Program, University of Western Ontario, London, Ontario, CanadaN6A 5C1
D. D. Colwell
Affiliation:
Agriculture Canada Research Station, Box 3000, Main, Lethbridge, Alberta, CanadaT1J 4B1
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Summary

Parasite modification of host behaviour influences a number of critical responses, but little is known about the effects on host spatial abilities. This study examined the effects of infection with the intestinal trichostrongylid nematode, Heligmosomoides polygyrus, on spatial water maze learning by male laboratory mice, Mus musculus. In this task individual mice had to learn the spatial location of a submerged hidden platform using extramaze visual cues. Determinations of spatial performance were made on day 19 post-infection with mice that had been administered either 50 or 200 infective larvae of H. polygyrus. The infected mice displayed over 1 day of testing (6 blocks of 4 trials) significantly poorer acquisition and retention of the water maze task than either sham-infected or control mice, with mice that had received 200 infective larvae displaying significantly poorer spatial performance than individuals receiving 50 larvae. The decrease in spatial learning occurred in the absence of either any symptoms of illness and malaise, or any evident motor, visual and motivational impairments. It is suggested that in this single host system the parasitic infection-induced decrease in spatial learning arises as a side-effect of the host's immunological and neuromodulatory responses and represents a fitness cost of response to infection.

Keywords

spatial learningmemoryspatial abilitiesspatial navigationHeligmosomoides polygyrusbehaviour
Type
Research Article
Information
Parasitology , Volume 110 , Issue 5 , June 1995 , pp. 591 - 597
Copyright
Copyright © Cambridge University Press 1995

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References

REFERENCES

Behnke, J. M., Barnard, C. J. & Wakelin, D. (1992). Understanding chronic infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.Google Scholar
Bellinger, F. P., Madamba, S. & Siggins, G. R. (1993). Interleukin 1B inhibits synaptic strength and long-term potentiation in the rat CA1 hippocampus. Brain Research 628, 227–34.CrossRefGoogle Scholar
Colwell, D. D. & Kavaliers, M. (1993). Altered nociceptive responses of mice infected with Eimeria vermiformis: evidence for involvement of endogenous opioid systems. Journal of Parasitology 79, 751–6.Google Scholar
Cypess, R. H., Lucia, H. I., Zidian, J. L. & Rivera-Ortiz, C. I. (1977). Heligmosomoides polygyrus: temporal, spatial and morphological population characteristics in LAF/J mice. Experimental Parasitology 42, 34–43.CrossRefGoogle Scholar
Dobson, C. & Tang, J.-M. (1991). Genetic variation and host-parasite relations: Nematospiroides dubius in mice. Journal of Parasitology 77, 884–9.CrossRefGoogle ScholarPubMed
Dolinsky, Z. S., Burright, R. G., Donovick, P. J., Glickman, L. T., Babish, J., Summers, B. & Cypess, R. H. (1981). Behavioral effects of lead and Toxocaris canis in mice. Science 213, 1142–4.CrossRefGoogle Scholar
Freeland, W. J. (1981). Parasitism and behavioural dominance among male mice. Science 213, 461–2.CrossRefGoogle ScholarPubMed
Galea, L. A. M., Kavaliers, M., Ossenkopp, K.-P., Innes, D. & Hargreaves, E. L. (1994). Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Research 635, 18–26.CrossRefGoogle ScholarPubMed
Gaulin, S. J. C. & Fitzgerald, R. W. (1989). Sexual selection for spatial-learning ability. Animal Behaviour 37, 322–31.Google Scholar
Holmes, J. C. & Zohar, S. (1990). Pathology and host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 34–63. London: Taylor and Francis.Google Scholar
Kavaliers, M. & Colwell, D. D. (1992). Parasitism, opioid systems and host behaviour. Advances in Neuroimmunology 2, 287–95.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1993). Multiple opioid system involvement in the mediation of parasitic-infection induced analgesia. Brain Research 623, 316–20.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1995). Exposure to stable flies reduces spatial learning in mice: involvement of endogenous opioid systems. Medical and Veterinary Entomology (in the Press.)CrossRefGoogle ScholarPubMed
Kavaliers, M., Colwell, D. D. & Galea, L. A. M. (1995). Parasitic infection impairs spatial learning in mice. Animal Behaviour (In the Press).Google Scholar
Kavaliers, M. & Galea, L. A. M. (1994). Spatial water maze learning using celestial cues by the meadow vole, Microtus pennsylvanicus. Behavioural Brain Research 61, 97–100.CrossRefGoogle ScholarPubMed
Kershaw, W. E., Leytham, G. W. H. & Dickerson, G. (1950). The effect of schistosomiasis on animal intelligence. Annals of Tropical Medicine and Parasitology 53, 504–6.CrossRefGoogle Scholar
Krebs, J. R. & Horn, G. (1991). Behavioural and Neural Aspects of Learning and Memory. Oxford: Clarendon Press.Google Scholar
Krebs, J. R. & Inman, A. J. (1992). Learning and foraging: individuals groups and populations. American Naturalist 140, S63–S84.CrossRefGoogle ScholarPubMed
Kvalsvig, J. D. (1988). The effects of parasitic infection on cognitive performance. Parasitology Today 4, 206–8.CrossRefGoogle ScholarPubMed
Kvalsvig, J. D., Coopan, R. M. & Connolly, K. J. (1991). The effects of parasite infections on cognitive processes in children. Annals of Tropical Medicine and Parasitology 85, 551–68.CrossRefGoogle ScholarPubMed
McGaugh, J. L., Introini-Collison, I. B. & Castellano, C. (1993). Involvement of opioid peptides in learning and memory. In Opioids II (ed. Herz, A.), pp. 429–448. New York: Springer-Verlag.Google Scholar
McNamara, R. K. & Skeleton, R. W. (1993). The neuropharmacological and neurochemical basis of place learning in the Morris water maze. Brain Research Reviews 18, 33–49.Google Scholar
Milinski, M. (1990). Parasites and host decision-making. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, M.), pp. 95–116. London: Taylor and Francis.Google Scholar
Moller, A. P., Dufva, R. & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behaviour 23, 65–102.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1990). A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, M.), pp. 193–223. London: Taylor and Francis.Google Scholar
Morris, R. G. M. (1984). Development of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 11, 47–60.CrossRefGoogle ScholarPubMed
Nokes, C., Granttham-McGregor, S. M., Sawyer, A. W., Cooper, E. S., Robinson, B. A. & Bundy, D. A. (1992). Moderate to heavy infections of Trichuris trichiura affect cognitive function in Jamaican school children. Parasitology 104, 539–47.CrossRefGoogle ScholarPubMed
Oitzl, M. S., Oers Van, H., Schobitz, B. & De Kloet, E. R. (1993). Interleukin-1B, but not interleukin-6, impairs spatial navigation learning. Brain Research 613, 160–3.CrossRefGoogle Scholar
Olson, L. J. & Rose, J. E. (1966). Effect of Toxocara canis infection on the ability of white rats to solve maze problems. Experimental Parasitology 19, 77–84.CrossRefGoogle ScholarPubMed
Olton, D. S., Becker, J. T. & Handelman, G. E. (1979). Hippocampus, space and memory. Behavioral Brain Sciences 2, 313–65.CrossRefGoogle Scholar
Poulin, R. (1994). Meta-analysis of parasite-induced behavioural changes. Animal Behaviour 48, 137–46.CrossRefGoogle Scholar
Real, L. A. (1993). Toward a cognitive ecology. Trends in Ecology and Evolution 8, 413–17.CrossRefGoogle Scholar
Robinson, M., Wahid, F. N., Behnke, J. M. & Gilbert, F. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98, 115–24.CrossRefGoogle ScholarPubMed
Scott, M. E. (1990). An experimental and theoretical study of the dynamics of a mouse-nematode (Heligmosomoides polygyrus) interaction. Parasitology 101, 75–92.CrossRefGoogle ScholarPubMed
Sei, Y., Arora, P. K., Skilnick, P. & Paul, I. A. (1992). Spatial learning impairment in a murine model of AIDS. FASEB Journal 6, 3008–13.CrossRefGoogle Scholar
Sherry, D. F., Jacobs, L. F. & Gaulin, J. C. (1992). Spatial memory and adaptive specialization of the hippocampus. Trends in Neurosciences 15, 298–303.CrossRefGoogle ScholarPubMed
Stewart, C. A. & Morris, G. M. (1993). The watermaze. In Behavioural Neuroscience, A Practical Approach, Vol. 1. (ed. Shaga, A.), pp. 107–122. New York: IRL Press.Google Scholar
Stretch, R. G. A., Leytham, G. W. H. & Kershaw, W. E. (1960). The effect of acute schistosomiasis upon learning in rats under different levels of motivation. Annals of Tropical Medicine and Parasitology 54, 487–92.CrossRefGoogle Scholar
Thompson, S. N. & Kavaliers, M. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109, 5119–38.CrossRefGoogle ScholarPubMed
Vanderwolf, C. H. & Cain, D. P. (1994). The behavioral neurobiology of learning and memory: a conceptual reorientation. Brain Research Reviews 19, 264–97.Google Scholar
Wahid, F. N. & Behnke, J. M. (1992). Stimuli for acquired resistance to Heligmosomoides polygyrus from intestinal tissue resident L3 and L4 larvae. International Journal for Parasitology 22, 699–710.CrossRefGoogle ScholarPubMed
Wahid, F. N., Robinson, M. & Behnke, J. M. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): expulsion of adult worms from fast responder syngenic and hybrid strains of mice. Parasitology 98, 459–69.Google Scholar
Williams, C. L. & Meck, W. H. (1991). The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 16, 155–76.CrossRefGoogle ScholarPubMed
Zuk, M. (1992). The role of parasites in sexual selection: current evidence and future directions. Advances in the Study of behavior 21, 39–68.Google Scholar