Zaiss, M. M. & Harris, N. L. Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol. 38, 5–11 (2016).
Google Scholar
Jhan, K. Y. et al. Angiostrongylus cantonensis causes cognitive impairments in heavily infected BALB/c and C57BL/6 mice. Parasites Vectors. 13, 405. https://doi.org/10.1186/s13071-020-04230-y (2020).
Google Scholar
Boillat, M. et al. Neuroinflammation-associated aspecific manipulation of mouse predator fear by Toxoplasma gondii. Cell Rep. 30, 320–334 (2020).
Google Scholar
Brombacher, T. M. et al. Nippostrongylus brasiliensis infection leads to impaired reference memory and myeloid cell interference. Sci. Rep. 8, 2958. https://doi.org/10.1038/s41598-018-20770-x (2018).
Google Scholar
Kavaliers, M. & Colwell, D. D. Reduced spatial learning in mice infected with the nematode Heligmosomoides polygyrus. Parasitology 110(Pt 5), 591–597 (1995).
Google Scholar
Pan, S. C. et al. Cognitive and microbiome impacts of experimental Ancylostoma ceylanicum hookworm infections in hamsters. Sci. Rep. 9, 7868. https://doi.org/10.1038/s41598-019-44301-4 (2019).
Google Scholar
Blecharz-Klin, K. et al. Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters. PLoS Pathog. 18, e1010330–e1010330. https://doi.org/10.1371/journal.ppat.1010330 (2022).
Google Scholar
Braithwaite, V. et al. Spatial and discrimination learning in rodents infected with the nematode Strongyloides ratti. Parasitology 117(Pt 2), 145–154 (1998).
Google Scholar
Sharma, S., Rakoczy, S. & Brown-Borg, H. Assessment of spatial memory in mice. Life Sci. 87, 521–536 (2010).
Google Scholar
Vorhees, C. V. & Williams, M. T. Assessing spatial learning and memory in rodents. ILAR J. 55, 310–332 (2014).
Google Scholar
Pelletier, F., Page, K. A., Ostiguy, T. & Festa-Bianchet, M. Fecal counts of lungworm larvae and reproductive effort in bighorn sheep. Ovis canadensis. Oikos. 110, 473–480 (2005).
Google Scholar
Odiere, M. R., Koski, K. G., Weiler, H. A. & Scott, M. E. Concurrent nematode infection and pregnancy induce physiological responses that impair linear growth in the murine foetus. Parasitology 137, 991–1002 (2010).
Google Scholar
Fitzgerald, E., Hor, K. & Drake, A. J. Maternal influences on fetal brain development: The role of nutrition, infection and stress, and the potential for intergenerational consequences. Early Hum. Dev. 150, 105190. https://doi.org/10.1016/j.earlhumdev.2020.105190 (2020).
Google Scholar
Boksa, P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24, 881–897 (2010).
Google Scholar
Akitake, Y. et al. Moderate maternal food restriction in mice impairs physical growth, behavior, and neurodevelopment of offspring. Nutr. Res. 35, 76–87 (2015).
Google Scholar
Hammelrath, L. et al. Morphological maturation of the mouse brain: An in vivo MRI and histology investigation. Neuroimage 125, 144–152 (2016).
Google Scholar
Wills, T., Muessig, L. & Cacucci, F. The development of spatial behaviour and the hippocampal neural representation of space. Philos. Trans. R. Soc. B: Biol. Sci. 369, 20130409. https://doi.org/10.1098/rstb.2013.0409 (2014).
Google Scholar
Travaglia, A., Steinmetz, A. B., Miranda, J. M. & Alberini, C. M. Mechanisms of critical period in the hippocampus underlie object location learning and memory in infant rats. Learn Mem. 25, 176–182 (2018).
Google Scholar
McHail, D. G., Valibeigi, N. & Dumas, T. C. A Barnes maze for juvenile rats delineates the emergence of spatial navigation ability. Learn Mem. 25, 138–146 (2018).
Google Scholar
Bliss, T. V. P., Collingridge, G. L., Morris, R. G. M. & Reymann, K. G. Long-term potentiation in the hippocampus: Discovery, mechanisms and function. Neuroforum 24, A103–A120 (2018).
Google Scholar
Schiller, D. et al. Memory and space: Towards an understanding of the cognitive map. J. Neurosci. 35, 13904–13911 (2015).
Google Scholar
Kim, J. J. & Diamond, D. M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3, 453–462 (2002).
Google Scholar
Jiang, P. et al. The persistent effects of maternal infection on the offspring’s cognitive performance and rates of hippocampal neurogenesis. Prog. Neuropsychopharmacol. Biol. Psychiatry. 44, 279–289 (2013).
Google Scholar
Wallace, K. L. et al. Interleukin-10/Ceftriaxone prevents E. coli-induced delays in sensorimotor task learning and spatial memory in neonatal and adult Sprague-Dawley rats. Brain. Res. Bull. 81, 141–148 (2010).
Shi, L., Fatemi, S. H., Sidwell, R. W. & Patterson, P. H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23, 297–302 (2003).
Google Scholar
Denenberg, V. H. Open-field behavior in the rat: what does it mean?. Ann. N. Y. Acad. Sci. 159, 852–859 (1969).
Google Scholar
Vogel-Ciernia, A. & Wood, M. A. Examining object location and object recognition memory in mice. Curr. Protoc. Neurosci. 69, 8.31.1–17 (2014).
Denninger, J. K., Smith, B. M. & Kirby, E. D. Novel object recognition and object location behavioral testing in mice on a budget. J. Vis. Exp. https://doi.org/10.3791/58593 (2018).
Google Scholar
Krüger, H.-S., Brockmann, M. D., Salamon, J., Ittrich, H. & Hanganu-Opatz, I. L. Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats. Neurobiol. Learn. Mem. 97, 470–481 (2012).
Google Scholar
Cruz-Sanchez, A. et al. Developmental onset distinguishes three types of spontaneous recognition memory in mice. Sci. Rep. 10, 10612. https://doi.org/10.1038/s41598-020-67619-w (2020).
Google Scholar
Sunyer, B., Patil, S., Hoger, H. & Lubec, G. Barnes maze, a useful task to assess spatial reference memory in the mice. Nat. Protoc. https://doi.org/10.1038/nprot.2007.390 (2007).
Google Scholar
Schenk, F. Development of place navigation in rats from weaning to puberty. Behav. Neural Biol. 43, 69–85 (1985).
Google Scholar
Brown, R. W. & Kraemer, P. J. Ontogenetic differences in retention of spatial learning tested with the Morris water maze. Dev. Psychobiol. 30, 329–341 (1997).
Google Scholar
Batinić, B. et al. Lipopolysaccharide exposure during late embryogenesis results in diminished locomotor activity and amphetamine response in females and spatial cognition impairment in males in adult, but not adolescent rat offspring. Behav. Brain Res. 299, 72–80 (2016).
Google Scholar
Lante, F. et al. Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain. Free Radic. Biol. Med. 42, 1231–1245 (2007).
Google Scholar
Wang, H. et al. Age- and gender-dependent impairments of neurobehaviors in mice whose mothers were exposed to lipopolysaccharide during pregnancy. Toxicol. Lett. 192, 245–251 (2010).
Google Scholar
Yagi, S. & Galea, L. A. M. Sex differences in hippocampal cognition and neurogenesis. Neuropsychopharmacology 44, 200–213 (2019).
Google Scholar
Vuoksimaa, E. et al. Brain structure mediates the association between height and cognitive ability. Brain Struct. Func. 223, 3487–3494 (2018).
Google Scholar
Harris, M. A., Brett, C. E., Deary, I. J. & Starr, J. M. Associations among height, body mass index and intelligence from age 11 to age 78 years. BMC Geriatr. 16, 167. https://doi.org/10.1186/s12877-016-0340-0 (2016).
Google Scholar
Pereira, V. H. et al. Adult body height is a good predictor of different dimensions of cognitive function in aged individuals: A cross-sectional study. Front. Aging Neurosci. 8, 1. https://doi.org/10.3389/fnagi.2016.00217 (2016).
Case, A. & Paxson, C. Stature and status: Height, ability, and labor market outcomes. J. Polit. Econ. 116, 499–532 (2008).
Google Scholar
Frick, K. M., Kim, J., Tuscher, J. J. & Fortress, A. M. Sex steroid hormones matter for learning and memory: estrogenic regulation of hippocampal function in male and female rodents. Learn Mem. 22, 472–493 (2015).
Google Scholar
Qiu, L. R. et al. Mouse MRI shows brain areas relatively larger in males emerge before those larger in females. Nat. Commun. 9, 2615. https://doi.org/10.1038/s41467-018-04921-2 (2018).
Google Scholar
Towe, A. L. & Mann, M. D. Brain size/body length relations among myomorph rodents. Brain Behav. Evol. 39, 17–23 (1992).
Google Scholar
Perepelkina, O. V., Tarasova, A. Y., Ogienko, N. A., Lil’p, I. G. & Poletaeva, I. I. Brain weight and cognitive abilities of laboratory mice. Biol. Bull. Rev. 10, 91–101 (2020).
Odiere, M. R., Scott, M. E., Weiler, H. A. & Koski, K. G. Protein deficiency and nematode infection during pregnancy and lactation reduce maternal bone mineralization and neonatal linear growth in mice. J. Nutr. 140, 1638–1645 (2010).
Google Scholar
Sánchez, M. B. et al. Leishmania amazonensis infection impairs reproductive and fetal parameters in female mice. Rev. Argent. Microbiol. 53, 194–201 (2021).
Google Scholar
Haque, M., Koski, K. G. & Scott, M. E. Maternal gastrointestinal nematode infection up-regulates expression of genes associated with long-term potentiation in perinatal brains of uninfected developing pups. Sci. Rep. 9, 4165. https://doi.org/10.1038/s41598-019-40729-w (2019).
Google Scholar
Gregory, R. D., Montgomery, S. S. J. & Montgomery, W. I. Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. J. Anim. Ecol. 61, 749–757 (1992).
Google Scholar
Reynolds, L. A., Filbey, K. J. & Maizels, R. M. Immunity to the model intestinal helminth parasite Heligmosomoides polygyrus. Semin. Immunopathol. 34, 829–846 (2012).
Google Scholar
Maizels, R. M. et al. Immune modulation and modulators in Heligmosomoides polygyrus infection. Exp. Parasitol. 132, 76–89 (2012).
Google Scholar
Haque, M., Starr, L. M., Koski, K. G. & Scott, M. E. Differential expression of genes in fetal brain as a consequence of maternal protein deficiency and nematode infection. Int. J. Parasitol. 48, 51–58 (2018).
Google Scholar
Hsueh, P.-T. et al. Immune imbalance of global gene expression, and cytokine, chemokine and selectin levels in the brains of offspring with social deficits via maternal immune activation. Genes Brain Behav. 17, e12479. https://doi.org/10.1111/gbb.12479 (2018).
Steimer, T. The biology of fear- and anxiety-related behaviors. Dialogues Clin. Neurosci. 4, 231–249 (2002).
Google Scholar
Ricceri, L., Colozza, C. & Calamandrei, G. Ontogeny of spatial discrimination in mice: A longitudinal analysis in the modified open-field with objects. Dev. Psychobiol. 37, 109–118 (2000).
Google Scholar
Howland, J. G., Cazakoff, B. N. & Zhang, Y. Altered object-in-place recognition memory, prepulse inhibition, and locomotor activity in the offspring of rats exposed to a viral mimetic during pregnancy. Neuroscience 201, 184–198 (2012).
Google Scholar
Ito, H. T., Smith, S. E. P., Hsiao, E. & Patterson, P. H. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav. Immun. 24, 930–941 (2010).
Google Scholar
Meyer, U. et al. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 26, 4752–4762 (2006).
Google Scholar
Meyer, U. et al. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol. Psychiatry. 13, 208–221 (2008).
Google Scholar
Chapillon, P. & Roullet, P. Use of proximal and distal cues in place navigation by mice changes during ontogeny. Dev. Psychobiol. 29, 529–545 (1996).
Google Scholar
Variyam, E. P. & Banwell, J. G. Hookworm disease: Nutritional implications. Rev. Infect. Dis. 4, 830–835 (1982).
Google Scholar
Bansemir, A. D. & Sukhdeo, M. V. The food resource of adult Heligmosomoides polygyrus in the small intestine. J. Parasitol. 80, 24–28 (1994).
Google Scholar
Starr, L. M., Scott, M. E. & Koski, K. G. Protein deficiency and intestinal nematode infection in pregnant mice differentially impact fetal growth through specific stress hormones, growth factors, and cytokines. J. Nutr. 145, 41–50 (2015).
Google Scholar
Herring, C. M., Bazer, F. W., Johnson, G. A. & Wu, G. Impacts of maternal dietary protein intake on fetal survival, growth, and development. Exp. Biol. Med. (Maywood). 243, 525–533 (2018).
Google Scholar
Starr, L. M., Odiere, M. R., Koski, K. G. & Scott, M. E. Protein deficiency alters impact of intestinal nematode infection on intestinal, visceral and lymphoid organ histopathology in lactating mice. Parasitology 141, 801–813 (2014).
Google Scholar
Bastian, T. W., von Hohenberg, W. C., Mickelson, D. J., Lanier, L. M. & Georgieff, M. K. Iron deficiency impairs developing hippocampal neuron gene expression, energy metabolism, and dendrite complexity. Dev. Neurosci. 38, 264–276 (2016).
Google Scholar
Bastian, T. W., Rao, R., Tran, P. V. & Georgieff, M. K. The effects of early-life iron deficiency on brain energy metabolism. Neurosci. Insights. 15, 2633105520935104. https://doi.org/10.1177/2633105520935104 (2020).
Google Scholar
Gould, J. M. et al. Mouse maternal protein restriction during preimplantation alone permanently alters brain neuron proportion and adult short-term memory. Proc. Natl. Acad. Sci. 115, E7398–E7407. https://doi.org/10.1073/pnas.1721876115 (2018).
Google Scholar
Radlowski, E. & Johnson, R. Perinatal iron deficiency and neurocognitive development. Front. Hum. Neurosci. 7, 585 (2013).
Google Scholar
Rytych, J. L. et al. Early life iron deficiency impairs spatial cognition in neonatal piglets. J. Nutr. 142, 2050–2056 (2012).
Google Scholar
Snyder, J. S., Hong, N. S., McDonald, R. J. & Wojtowicz, J. M. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843–852 (2005).
Google Scholar
Brązert, M. et al. Expression of genes involved in neurogenesis, and neuronal precursor cell proliferation and development: Novel pathways of human ovarian granulosa cell differentiation and transdifferentiation capability in vitro. Mol. Med. Rep. 21, 1749–1760 (2020).
Google Scholar
van Praag, H., Christie, B. R., Sejnowski, T. J. & Gage, F. H. Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 13427–13431 (1999).
Google Scholar
Li, H. et al. Regular treadmill running improves spatial learning and memory performance in young mice through increased hippocampal neurogenesis and decreased stress. Brain. Res. 1531, 1–8 (2013).
Google Scholar
Odiere, M. R., Scott, M. E., Leroux, L. P., Dzierszinski, F. S. & Koski, K. G. Maternal protein deficiency during a gastrointestinal nematode infection alters developmental profile of lymphocyte populations and selected cytokines in neonatal mice. J. Nutr. 143, 100–107 (2013).
Google Scholar
El Ahdab, N., Haque, M., Madogwe, E., Koski, K. G. & Scott, M. E. Maternal nematode infection upregulates expression of Th2/Treg and diapedesis related genes in the neonatal brain. Sci. Rep. 11, 22082. https://doi.org/10.1038/s41598-021-01510-0 (2021).
Google Scholar
Hein, A. M. et al. Sustained hippocampal IL-1β overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav. Immun. 24, 243–253 (2010).
Google Scholar
Derecki, N. C. et al. Regulation of learning and memory by meningeal immunity: A key role for IL-4. Exp. Med. 207, 1067–1080 (2010).
Google Scholar
Brombacher, T. M. et al. IL-4R alpha deficiency influences hippocampal-BDNF signaling pathway to impair reference memory. Sci. Rep. 10, 16506. https://doi.org/10.1038/s41598-020-73574-3 (2020).
Google Scholar
Mizuno, M., Yamada, K., Olariu, A., Nawa, H. & Nabeshima, T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 20, 7116–7121 (2000).
Google Scholar
Miranda, M., Morici, J. F., Zanoni, M. B. & Bekinschtein, P. Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Front. Cell. Neurosci. 13. https://doi.org/10.3389/fncel.2019.00363 (2019).
Williamson, L. L. et al. Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection. Brain Behav. Immun. 51, 14–28 (2016).
Google Scholar
McKay, D. M. The immune response to and immunomodulation by Hymenolepis diminuta. Parasitology 137, 385–394 (2010).
Google Scholar
Meyer, U., Feldon, J. & Fatemi, S. H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33, 1061–1079 (2009).
Google Scholar
Johnston, C. J. C. et al. Cultivation of Heligmosomoides polygyrus: an immunomodulatory nematode parasite and its secreted products. J. Vis. Exp. e52412–e52412. https://doi.org/10.3791/52412 (2015).
Valanparambil, R. M. et al. Production and analysis of immunomodulatory excretory-secretory products from the mouse gastrointestinal nematode Heligmosomoides polygyrus bakeri. Nat. Protoc. 9, 2740–2754 (2014).
Google Scholar
Murai, T., Okuda, S., Tanaka, T. & Ohta, H. Characteristics of object location memory in mice: Behavioral and pharmacological studies. Physiol. Behav. 90, 116–124 (2007).
Google Scholar
Patil, S. S., Sunyer, B., Hoger, H. & Lubec, G. Evaluation of spatial memory of C57BL/6J and CD1 mice in the Barnes maze, the Multiple T-maze and in the Morris water maze. Behav. Brain. Res. 198, 58–68 (2009).
Google Scholar
R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2020).
Wickham, H. ggplot2: Elegant graphics for data analysis (Springer-Verlag, 2016).
Google Scholar
Lazic, S. E. The problem of pseudoreplication in neuroscientific studies: Is it affecting your analysis?. BMC Neurosci. 11, 5. https://doi.org/10.1186/1471-2202-11-5 (2010).
Google Scholar
Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. & Smith, G. M. Mixed effects models and extensions in ecology with R. Vol. 1–574 (2009).
Bates, D., Maechler, M., Bolker, B. & Steve, W. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).
Google Scholar
Fox, J. & Sanford, W. An R Companion to Applied Regression. 3 edn, (Sage, 2019).
emmeans: Estimated marginal means, aka least-squares means v. 1.4.8 (R package, 2020).
RVAideMemoire: Testing and plotting procedures for biostatistics. v. 0.9-78 (R package, 2020).
DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models v. 0.3.3.0 (R package, 2020).
Delignette-Muller, M. L. & Dutang, C. fitdistrplus: An R package for fitting distributions. J. Stat. Softw. 64, 1–34 (2015).
Google Scholar
Source: Ecology - nature.com