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Anxiogenic effect of subclinical bacterial infection in mice in the absence of overt immune activation
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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“Landmark studies in the 1990s were the first and demonstrate that bacteria respond to host neuroendocrine signaling molecules (Lyte andErnst, 1992, 1993), including norepinephrine and epinephrine, and that the microbiota can affect host behavior via the gut-brain axis (Lyte et al., 1998).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Lyte et al., 1998
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“Campylobacter jejuni administration had previously been shown to induce anxiety-related behavior without initiating a systemic immune response (Lyte et al., 1998).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Lyte et al., 1998
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“These findings were also echoed in animal studies where low-level infections altered behavior even in the absence of immune activation (Lyte et al., 1998).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Lyte et al., 1998
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Maier, S. F., & Watkins, L. R. (1998) · Psychological Review · doi:10.1037/0033-295x.105.1.83 · Cited by 1,130
Research works printed but not linked: 36
- 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
- Bradfield, 1992, Behavioral and physiologic effects of inapparent wound infection in rats, Lab. Anim. Sci., 42, 572
- 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
- Butzler, 1991, Campylobacter: Pathogenicity and significance in foods, Int. J. Food Microbiol., 12, 1, 10.1016/0168-1605(91)90043-O · DOI
- 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
- 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
- Donovick, 1987, The consequences of parasitic infection for the behavior of the mammalian host, Environ. Health Perspect., 73, 247, 10.1289/ehp.8773247 · DOI
- Ebadi, 1997, Neurotrophins and their receptors in nerve injury and repair, Neurochem. Int., 30, 347, 10.1016/S0197-0186(96)00071-X · DOI
- 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
- Fiore, 1996, Schistosoma mansoni: Influence of infection on mouse behavior, Exp. Parasitol., 83, 46, 10.1006/expr.1996.0047 · DOI
- 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
- Hotchin, 1977, Virus-induced behavioral alteration of mice, Science, 196, 671, 10.1126/science.854742 · DOI
- Hsu, 1986, The bacterial flora of the intestine of Ascaris suum and 5-hydroxytryptamine production, J. Parasit., 72, 545, 10.2307/3281505 · DOI
- Kavaliers, 1995, Decreased predator avoidance in parasitized mice: Neuromodulatory correlates, Parasitology, 111, 257, 10.1017/S0031182000081816 · DOI
- Kavaliers, 1995, Reduced spatial learning in mice infected with the nematode, Heligmosomoides polygyrus, Parasitology, 110, 591, 10.1017/S0031182000065318 · DOI
- Kulkarni, 1991, Elevated plus-maze: A novel psychobehavioral tool to measure anxiety in rodents, Methods Find. Exp. Clin. Pharmacol., 13, 573
- 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
- Lenard, 1992, Mammalian hormones in microbial cells, Trends Biochem. Sci., 17, 147, 10.1016/0968-0004(92)90323-2 · DOI
- Lister, 1987, The use of a plus-maze to measure anxiety in the mouse, Psychopharmacology, 92, 180, 10.1007/BF00177912 · DOI
- Lister, 1990, Ethologically-based animal models of anxiety disorders, Pharmacol. Ther., 46, 321, 10.1016/0163-7258(90)90021-S · DOI
- 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
- 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
- Minuk, 1986, Gamma-aminobutyric acid (GABA) production by eight common bacterial pathogens, Scand. J. Infect. Dis., 18, 465, 10.3109/00365548609032366 · DOI
- Moon, 1997, Comparative histopathology of intestinal infections, Adv. Exp. Med. Biol., 412, 1, 10.1007/978-1-4899-1828-4_1 · DOI
- 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
- 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
- Savage, 1986, Gastrointestinal microflora in mammalian nutrition, Ann. Rev. Nutr, 6, 155, 10.1146/annurev.nu.06.070186.001103 · DOI
- Schrott, 1996, Increased anxiety behaviors in autoimmune mice, Behav. Neurosci., 110, 492, 10.1037/0735-7044.110.3.492 · DOI
- 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
- 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
- Tabor, 1985, Polyamines in microorganisms, Microbiol. Rev., 49, 81, 10.1128/MR.49.1.81-99.1985 · DOI
- Watkins, 1994, Blockade of interleukin-1 induced hypothermia by subdiaphragmatic vagotomy: Evidence for vagal mediation of immune-brain communication, Neurosci. Lett., 183, 1
- 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
- Winder, 1988, gamma-aminobutyric acid (GABA) and sepsis-related encephalopathy, Can. J. Neurol. Sci., 15, 23, 10.1017/S0317167100027128 · DOI
- 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
- 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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BackgroundHagerty, S. L., Ellingson, J. M., Helmuth, T. B., Bidwell, L. C., Hutchison, K. E., & Bryan, A. D. (2019) · Perspectives on Psychological Science · doi:10.1177/1745691619827010 · Cited by 12
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Asbjornsdottir, B., Miranda-Ribera, A., Fiorentino, M. R., Konno, T., Çetinbaş, M., Lan, J., Sadreyev, R. I., Gudmundsson, L. S., Gottfreðsson, M., Lauth, B., et al. (2022) · Biomedicines · doi:10.3390/biomedicines11010091 · Cited by 7
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“There is also clear evidence that GI colonization with potential enteropathogens can alter the behavior of the infected animals.(32) For example, in 1 study, mice were inoculated with Campylobacter jejuni, leading to mild subclinical infection that did not lead to measurable activation of the immune system (ie, no alt…”
Influentialvan Tilburg, M. A. L. (2012) · Humana Press eBooks · doi:10.1007/978-1-60761-709-9_6 · Cited by 4
Silva, O. N., Franco, O. L., Neves, B. J., Morais, Á. C. B., Neto, J. R. D. O., da Cunha, L. C., Naves, L. M., Pedrino, G. R., Costa, É. A., & Fajemiroye, J. O. (2020) · Neuropeptides · doi:10.1016/j.npep.2020.102027 · Cited by 8
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Goehler, L., & Gaykema, R. (2009) · Springer eBooks · doi:10.1007/978-0-387-84851-8_3 · Cited by 6
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BackgroundSelf-citationChen, Y., Wang, D., Liao, Y., Zuo, G., & Lu, X. (2024) · Discover Medicine · doi:10.1007/s44337-024-00135-2 · Cited by 5
Gómez-Chavarín, M. (2017) · Archivos de Neurociencias · doi:10.31157/archneurosciencesmex.v22i2.153 · Cited by 3
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Domínguez-Roldan, R., Hallal-Calleros, C., Sciutto, E., Hernández, M., Aguirre-Flores, V., García-Jiménez, S., Báez-Saldaña, A., & Flores-Pérez, F. I. (2016) · Experimental parasitology · doi:10.1016/j.exppara.2016.04.013 · Cited by 3
“It was performed in an elevated plus-maze, the device was constructed with twowooden corridors of 45 cm long 9 cmwide, intersected in half perpendicularly, and with walls of 38 cm in height mounted on supports at a height of 34 cm from the floor (Lyte et al., 1998; Moise et al., 2008).”
MethodDorsey, A., & Miller, E. M. (2023) · Evolutionary Anthropology (print) · doi:10.1002/evan.22004 · Cited by 2
“72 The effects of commensal proinflammatory bacteria, such as Enterobacteriaceae, on the vagus nerve are not well ‐ characterized; however there is a well ‐ established relationship between gut cytokines and vagus nerve function.”
BackgroundSuchodolski, J. S. (2020) · Advances in Small Animal Care · doi:10.1016/j.yasa.2020.07.008 · Cited by 3
Gastrointestinal Microbiota and the Neural System
Philip, V., & Berčík, P. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-804024-9.00027-6 · Cited by 2
Castelli, L., García-Amado, M., Rudolf, C. A., Contreras, M., Espinosa-Blanco, A. S., & Godoy-Vitorino, F. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1697111 · Cited by 1
“Studies in mice have shown that C. jejuni infection induces anxiety-like behavior even in the absence of overt gastrointestinal illness (Lyte et al., 1998).”
Nankova, B. B., Hu, F., & LaGamma, E. F. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1504513 · Cited by 1
“…that redundant overlapping neuronal processes emerged through evolution to enhance survival responses as a reasonable teleologic interpretation to explain these observations (Goehler et al., 2005; Lyte et al., 1998; Bravo et al., 2011; Sgritta et al., 2019; Bercik et al., 2011; Han et al., 2022).”
The relationship of depression, gut microbiota and colorectal cancer: A negative cycle
Sun, X., Li, Y., Li, W., Koeban, S., Zhang, L., Zhang, W., Li, X., Zhang, Y., Li, L., Chen, H., et al. (2025) · Well-Being Sciences Review · doi:10.54844/wsr.2025.0910 · Cited by 1
“Research on mice has demonstrated that intestinal infections or chemically induced colitis can lead to behaviors typically associated with anxiety, such as reduced exploration (Lyte et al ., 2006) and significant behavioral inhibition (Bercik et al ., 2010; Lyte et al ., 1998).”
Exploring the role of nutrition in mental health: A narrative review
Bhat, N., Dahal, A., Shakya, Y., & Dhungana, N. (2023) · Journal of Psychiatrists Association of Nepal · doi:10.3126/jpan.v12i1.59429 · Cited by 1
Bouharati (2019) · Pacific International Journal · doi:10.55014/pij.v4i1.28 · Cited by 1
“accompanied by variations in biological parameters including action on mediators of systemic stress ([21]).”
BackgroundThe Human Microbiome: Composition and Change Reflecting Health and Disease
Cooper, S., Mathews, R., Bushar, L., Paddock, B., Wood, J., & Tammara, R. (2019) · HAPS Educator · doi:10.21692/haps.2019.020 · Cited by 1
“The first methods of DNA sequencing involved chemical cleavage and electrophoresis (Maxam and Gilbert 1977) or primer directed synthesis and chain termination (Sanger et al. 1977).”
MethodGuest Editorial: anxiety and the immune system: the modulation of benzodiazepines
Song, C. (2001) · Stress and Health · doi:10.1002/smi.899 · Cited by 1
Molecular Signaling in the Gut–Brain Axis in Stress
Page, A. J., & Li, H. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813156-5.00012-1 · Cited by 1
The Role of the Microbiota and Potential for Dietary Intervention in Chronic Fatigue Syndrome
Kirchgessner, A. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802304-4.00021-9 · Cited by 4
Immunosensory Signaling: Role of Cytokines
Goehler, L. (2003) · Neurobiological foundation of aberrant behaviors · doi:10.1007/978-1-4615-0323-1_2 · Cited by 1
“Cytokines released from immune cells can interact with the nervous system at the level of (1) meninges, ( 2 ) choroid plexus present in the brain's ventricular space, (3) brain endothelium, (4) the circumventricular organs, (5) the ependyma lining the ventricular space, and (6) primary afferents of the peripheral nerv…”
BackgroundOke, O. E., Eletu, T. A., Uyanga, V. A., & Onagbesan, O. M. (2026) · Annals of Animal Science · doi:10.2478/aoas-2027-0015
“Approximately 80% of vagal fi bres are a ff erent, transmitting sensory information from the gastrointestinal tract to the brain, including signals derived from microbial metabolites, in fl ammatory mediators, and gut hormones (Lyte et al., 1998).”
L’axe intestin–cerveau : les pistes actuelles
Piguet, P. (2021) · Douleur et Analgésie · doi:10.3166/dea-2021-0167
Bharwani, A., Bienenstock, J., & Forsythe, P. (2017) · Wageningen Academic Publishers eBooks · doi:10.3920/978-90-8686-839-1_8 · Cited by 1
The gut microbiota and the CNS
Bharwani, A., & Forsythe, P. (2016) · Wiley eBooks · doi:10.1002/9781118982907.ch27
The Future of Prebiotics and Probiotics
Brunser, O., Bravo, J., & Gotteland, M. (2013) · CRC Press eBooks · doi:10.1201/b15561-24
Challenges and solutions: pandemic 2009 H1N1 influenza A in a pediatric emergency department.
Graham, J. C., Shirm, S., Storm, E., Lyle, K., Linam, W., & Romero, J. (2011) · American Journal of Disaster Medicine · doi:10.5055/ajdm.2011.0060
Beneficial microbes from human and animal intestines
Fernández-Ciganda, S., Fraga, M., & Zunino, P. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85170-1.00008-7
Gut microbiota and brain function and pathophysiology
Duttaroy, A. K. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822405-2.00014-1
Hoffman, J. D. (2018) · doi:10.13023/etd.2018.405
“jejuni increased anxiety-like behavioral measure in the EPM two days after infection [303].”
BackgroundThe Role of the Indigenous Gut Microbiota in Human Health and Disease
Vunk, T. R., & Burkholder, K. M. (2017) · Advances in environmental microbiology · doi:10.1007/978-3-319-60616-3_4 · Cited by 1
Luczynski, P., Neufeld, K. M., Clarke, G. A., Dinan, T. G., & Cryan, J. F. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802304-4.00007-4 · Cited by 3
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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