Cited by 218Tryptophan and brain disordersStress Responses and CortisolNeuropeptides and Animal Physiology

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Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation

Lyte, Mark, Varcoe, Jeffrey J., Bailey, Michael T.·1998·Physiology & Behavior

Abstract

Challenge of animals with infectious microorganisms is well documented to affect a number of behavioral measures through activation of immune-neural mechanisms. In the present study, the ability of an infectious microorganism to directly alter behavioral responses in the absence of an overt immunologic response was examined. Eight-week-old CF-1 male mice were infected orally with the Gram-negative pathogen Campylobacter jejuni in order to establish a subclinical infection that did not result in immune activation. Microbiological examination of cecal contents revealed the presence of C. jejuni in all infected, but not control, animals 1 and 2 days post-oral challenge. Measurement of interleukin-6 (IL-6) levels and peripheral blood leukocyte populations did not reveal the activation of an overt immune response in 1 or 2 day infected animals as compared to controls. Infected mice demonstrated altered levels of anxiety-like behaviors on the elevated plus-maze as compared to controls on Day 2, but not Day 1, as reflected by a significant decrease in exploratory and an increase in nonexploratory behaviors. The anxiogenic effect of a subclinical infection in the absence of an overt immunologic response suggests that the direct activation of neural pathways by microorganisms may play a role in behavior.

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Research works printed but not linked: 36

  1. Archer, 1973, Tests for emotionality in rats and mice: A review, Anim. Behav., 21, 205, 10.1016/S0003-3472(73)80065-X · DOI · Paper page
  2. Bradfield, 1992, Behavioral and physiologic effects of inapparent wound infection in rats, Lab. Anim. Sci., 42, 572
  3. Buck, 1994, Interleukin-6: a sensitive parameter for the early diagnosis of neonatal bacterial infection, Pediatrics, 93, 54, 10.1542/peds.93.1.54 · DOI
  4. Butzler, 1991, Campylobacter: Pathogenicity and significance in foods, Int. J. Food Microbiol., 12, 1, 10.1016/0168-1605(91)90043-O · DOI
  5. Cao, 1997, Anxiolytic-like profile of p-MPPI, a novel 5HT1A receptor antagonist, in the murine elevated plus-maze, Psychopharmacology, 129, 365, 10.1007/s002130050202 · DOI
  6. Cruz, 1994, Ethopharmacological analysis of rat behavior on the elevated plus-maze, Pharmacol. Biochem. Behav., 49, 171, 10.1016/0091-3057(94)90472-3 · DOI
  7. Donovick, 1987, The consequences of parasitic infection for the behavior of the mammalian host, Environ. Health Perspect., 73, 247, 10.1289/ehp.8773247 · DOI
  8. Ebadi, 1997, Neurotrophins and their receptors in nerve injury and repair, Neurochem. Int., 30, 347, 10.1016/S0197-0186(96)00071-X · DOI
  9. Fernandez Espejo, 1997, Structure of the mouse behaviour on the elevated plus-maze test of anxiety, Behav. Brain Res., 86, 105, 10.1016/S0166-4328(96)02245-0 · DOI
  10. Fiore, 1996, Schistosoma mansoni: Influence of infection on mouse behavior, Exp. Parasitol., 83, 46, 10.1006/expr.1996.0047 · DOI
  11. Gibertini, 1995, Spatial learning impairment in mice infected with Legionalla pneumophila or administered exogenous interleukin-1-beta, Brain Behav. Immun., 9, 113, 10.1006/brbi.1995.1012 · DOI
  12. Hotchin, 1977, Virus-induced behavioral alteration of mice, Science, 196, 671, 10.1126/science.854742 · DOI
  13. Hsu, 1986, The bacterial flora of the intestine of Ascaris suum and 5-hydroxytryptamine production, J. Parasit., 72, 545, 10.2307/3281505 · DOI
  14. Kavaliers, 1995, Decreased predator avoidance in parasitized mice: Neuromodulatory correlates, Parasitology, 111, 257, 10.1017/S0031182000081816 · DOI
  15. Kavaliers, 1995, Reduced spatial learning in mice infected with the nematode, Heligmosomoides polygyrus, Parasitology, 110, 591, 10.1017/S0031182000065318 · DOI
  16. Kulkarni, 1991, Elevated plus-maze: A novel psychobehavioral tool to measure anxiety in rodents, Methods Find. Exp. Clin. Pharmacol., 13, 573
  17. Lapin, 1995, Only controls: Effect of handling, sham injection, and intraperitoneal injection of saline on behavior of mice in an elevated plus-maze, J. Pharmacol. Toxicol. Methods., 34, 73, 10.1016/1056-8719(95)00025-D · DOI
  18. Lenard, 1992, Mammalian hormones in microbial cells, Trends Biochem. Sci., 17, 147, 10.1016/0968-0004(92)90323-2 · DOI
  19. Lister, 1987, The use of a plus-maze to measure anxiety in the mouse, Psychopharmacology, 92, 180, 10.1007/BF00177912 · DOI
  20. Lister, 1990, Ethologically-based animal models of anxiety disorders, Pharmacol. Ther., 46, 321, 10.1016/0163-7258(90)90021-S · DOI
  21. Lyte, 1990, Examination of the neuroendocrine basis for the social conflict-induced enhancement of immunity in mice, Physiol. Behav., 48, 685, 10.1016/0031-9384(90)90212-M · DOI
  22. McCardell, 1986, A mouse model for the measurement of virulence of species of Campylobacter, J. Infect. Dis., 153, 177, 10.1093/infdis/153.1.177 · DOI
  23. Minuk, 1986, Gamma-aminobutyric acid (GABA) production by eight common bacterial pathogens, Scand. J. Infect. Dis., 18, 465, 10.3109/00365548609032366 · DOI
  24. Moon, 1997, Comparative histopathology of intestinal infections, Adv. Exp. Med. Biol., 412, 1, 10.1007/978-1-4899-1828-4_1 · DOI
  25. Rodgers, 1993, Anxiety enhancement in the murine elevated plus-maze by immediate prior exposure to social stressors, Physiol. Behav., 53, 383, 10.1016/0031-9384(93)90222-2 · DOI
  26. Rodgers, 1995, Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety, Pharmacol. Biochem. Behav., 52, 297, 10.1016/0091-3057(95)00138-M · DOI
  27. Savage, 1986, Gastrointestinal microflora in mammalian nutrition, Ann. Rev. Nutr, 6, 155, 10.1146/annurev.nu.06.070186.001103 · DOI
  28. Schrott, 1996, Increased anxiety behaviors in autoimmune mice, Behav. Neurosci., 110, 492, 10.1037/0735-7044.110.3.492 · DOI
  29. Sullivan, 1992, Correlation of plasma cytokine elevations with mortality rate in children with sepsis, J. Pediatr., 120, 510, 10.1016/S0022-3476(05)82476-X · DOI
  30. Swiergiel, 1997, Influenza virus infection of mice induces anorexia: Comparison with endotoxin and interleukin-1 and the effects of indomethacin, Pharmacol. Biochem. Behav., 57, 389, 10.1016/S0091-3057(96)00335-8 · DOI
  31. Tabor, 1985, Polyamines in microorganisms, Microbiol. Rev., 49, 81, 10.1128/MR.49.1.81-99.1985 · DOI
  32. Watkins, 1994, Blockade of interleukin-1 induced hypothermia by subdiaphragmatic vagotomy: Evidence for vagal mediation of immune-brain communication, Neurosci. Lett., 183, 1
  33. Watkins, 1995, Cytokine-to-brain communication: A review and analysis of alternative mechanisms, Life Sci., 57, 1011, 10.1016/0024-3205(95)02047-M · DOI · Paper page
  34. Winder, 1988, gamma-aminobutyric acid (GABA) and sepsis-related encephalopathy, Can. J. Neurol. Sci., 15, 23, 10.1017/S0317167100027128 · DOI
  35. Yirmiya, 1997, Intracerebral administration of Mycoplasma fermentans produces sickness behavior: Role of prostaglandins, Brain Res., 749, 71, 10.1016/S0006-8993(96)01295-4 · DOI
  36. Yurdaydin, 1995, Gut bacteria provide precursors of benzodiazepine receptor ligands in a rat model of hepatic encephalopathy, Brain Res., 679, 42, 10.1016/0006-8993(95)00241-H · DOI

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Metadata

Authors
Lyte, M., Varcoe, J. J., & Bailey, M. T.
Affiliations
Minnesota State University, Mankato (US)
Corresponding author
Lyte, Mark
Venue
Physiology & Behavior
Publisher
Elsevier BV
Published
1998-08
Volume
65
Issue
1
Pages
63-68
ISSN
0031-9384 (ISSN-L)
OpenAlex
W2012109410
Cited by
218
References
0
Citations by year
2026: 3 · 2025: 8 · 2024: 14 · 2023: 9 · 2022: 17 · 2021: 12 · 2020: 17 · 2019: 11 · 2018: 12 · 2017: 20 · 2016: 19 · 2015: 13 · 2014: 14 · 2013: 14 · 2012: 6
FWCI
0.29
Type
journal article
Language
en
Open access
closed
Locations
  • Physiology & Behavior (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5k02mh001371-02)
  • National Institute of Mental Health (MH-50431, MH01371, R01MH050431)
Topics
  • Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Keywords
Campylobacter jejuni, anxiety-like behavior, anxiogenic effects, neuroimmune interactions, interleukin-6, peripheral blood leukocytes, elevated plus maze, exploratory behavior, oral infection, Gram-negative bacteria
MeSH terms
Animals, Anxiety, Behavior, Animal, Campylobacter Infections, Leukocyte Count, Male, Interleukin-6, Campylobacter jejuni, Lymphocyte Count, Mice, Rats

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