Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups
Abstract The developing brain is particularly vulnerable to factors including maternal infection during pregnancy. Establishment of neural networks critical for memory and cognition begins during the perinatal period, when Heligmosomoides bakeri, a gastrointestinal (GI) nematode restricted to the ma...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2022-06-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-13971-y |
| _version_ | 1811343400780169216 |
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| author | Sophia C. Noel Liana Fortin-Hamel Manjurul Haque Marilyn E. Scott |
| author_facet | Sophia C. Noel Liana Fortin-Hamel Manjurul Haque Marilyn E. Scott |
| author_sort | Sophia C. Noel |
| collection | DOAJ |
| description | Abstract The developing brain is particularly vulnerable to factors including maternal infection during pregnancy. Establishment of neural networks critical for memory and cognition begins during the perinatal period, when Heligmosomoides bakeri, a gastrointestinal (GI) nematode restricted to the maternal mouse intestine, has been shown to upregulate expression of long-term potentiation genes in the young rodent pup brain. We explored the impact of maternal infection during pregnancy and early lactation on the spatial behavior of uninfected male and female juvenile mice. Pre-weaned pups of H. bakeri infected dams exhibited less exploratory behaviour compared to pups of uninfected dams on postnatal day (PD) 16 but not PD 17, possibly reflecting a transient fear of an unfamiliar environment and/or a brief neurodevelopmental delay. Our two spatial memory tests show for the first time an enhancement of spatial memory in response to maternal nematode infection regardless of pup sex. At PD 17, pups of infected dams expressed object location memories after 3 h in the Object Location Test whereas offspring of uninfected mothers did not. In addition, at PD 34, juveniles of infected mothers retained their ability to find the escape hole in the Barnes Maze Test for one week whereas offspring from uninfected mothers did not. This finding is even more striking given that spatial memory was positively associated with pup length, yet this maternal infection impaired linear growth of pups. Thus, the positive impact of maternal infection on spatial memory countered any impairment associated with the shorter length of the pups. Overall, these novel findings indicate that a maternal GI nematode infection during pregnancy and lactation positively influences the spatial memory of uninfected juvenile offspring with potential fitness implications for the next generation. |
| first_indexed | 2024-04-13T19:28:45Z |
| format | Article |
| id | doaj.art-285b7858cc1b4471939825c68cf00d70 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-13T19:28:45Z |
| publishDate | 2022-06-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-285b7858cc1b4471939825c68cf00d702022-12-22T02:33:14ZengNature PortfolioScientific Reports2045-23222022-06-0112111410.1038/s41598-022-13971-yMaternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pupsSophia C. Noel0Liana Fortin-Hamel1Manjurul Haque2Marilyn E. Scott3Institute of Parasitology, McGill University (Macdonald Campus)Institute of Parasitology, McGill University (Macdonald Campus)Institute of Parasitology, McGill University (Macdonald Campus)Institute of Parasitology, McGill University (Macdonald Campus)Abstract The developing brain is particularly vulnerable to factors including maternal infection during pregnancy. Establishment of neural networks critical for memory and cognition begins during the perinatal period, when Heligmosomoides bakeri, a gastrointestinal (GI) nematode restricted to the maternal mouse intestine, has been shown to upregulate expression of long-term potentiation genes in the young rodent pup brain. We explored the impact of maternal infection during pregnancy and early lactation on the spatial behavior of uninfected male and female juvenile mice. Pre-weaned pups of H. bakeri infected dams exhibited less exploratory behaviour compared to pups of uninfected dams on postnatal day (PD) 16 but not PD 17, possibly reflecting a transient fear of an unfamiliar environment and/or a brief neurodevelopmental delay. Our two spatial memory tests show for the first time an enhancement of spatial memory in response to maternal nematode infection regardless of pup sex. At PD 17, pups of infected dams expressed object location memories after 3 h in the Object Location Test whereas offspring of uninfected mothers did not. In addition, at PD 34, juveniles of infected mothers retained their ability to find the escape hole in the Barnes Maze Test for one week whereas offspring from uninfected mothers did not. This finding is even more striking given that spatial memory was positively associated with pup length, yet this maternal infection impaired linear growth of pups. Thus, the positive impact of maternal infection on spatial memory countered any impairment associated with the shorter length of the pups. Overall, these novel findings indicate that a maternal GI nematode infection during pregnancy and lactation positively influences the spatial memory of uninfected juvenile offspring with potential fitness implications for the next generation.https://doi.org/10.1038/s41598-022-13971-y |
| spellingShingle | Sophia C. Noel Liana Fortin-Hamel Manjurul Haque Marilyn E. Scott Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups Scientific Reports |
| title | Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| title_full | Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| title_fullStr | Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| title_full_unstemmed | Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| title_short | Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| title_sort | maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups |
| url | https://doi.org/10.1038/s41598-022-13971-y |
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