The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats
Early life stress negatively impacts brain development and affects structure and function of parvalbumin immunopositive (PV+) inhibitory neurons. Main regulators of PV+ interneurons activity and plasticity are perineuronal nets (PNNs), an extracellular matrix formation that enwraps PV+ interneurons...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-11-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2022.982663/full |
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| author | Ana Jakovljevic Gorana Agatonovic Dubravka Aleksic Milan Aksic Gebhard Reiss Eckart Förster Antonios Stamatakis Igor Jakovcevski Joko Poleksic |
| author_facet | Ana Jakovljevic Gorana Agatonovic Dubravka Aleksic Milan Aksic Gebhard Reiss Eckart Förster Antonios Stamatakis Igor Jakovcevski Joko Poleksic |
| author_sort | Ana Jakovljevic |
| collection | DOAJ |
| description | Early life stress negatively impacts brain development and affects structure and function of parvalbumin immunopositive (PV+) inhibitory neurons. Main regulators of PV+ interneurons activity and plasticity are perineuronal nets (PNNs), an extracellular matrix formation that enwraps PV+ interneurons mainly in the neocortex and hippocampus. To experimentally address the impact of early life stress on the PNNs and PV+ interneurons in the medial prefrontal cortex and dorsal hippocampus in rats, we employed a 24 h maternal deprivation protocol. We show that maternal deprivation in the medial prefrontal cortex of adult rats caused a decrease in density of overall PNNs and PNNs that enwrap PV+ interneurons in the rostral cingulate cortex. Furthermore, a staining intensity decrease of overall PNNs and PNN+/PV+ cells was found in the prelimbic cortex. Finally, a decrease in both intensity and density of overall PNNs and PNNs surrounding PV+ cells was observed in the infralimbic cortex, together with increase in the intensity of VGAT inhibitory puncta. Surprisingly, maternal deprivation did not cause any changes in the density of PV+ interneurons in the mPFC, neither had it affected PNNs and PV+ interneurons in the hippocampus. Taken together, our findings indicate that PNNs, specifically the ones enwrapping PV+ interneurons in the medial prefrontal cortex, are affected by early life stress. |
| first_indexed | 2024-04-12T05:05:36Z |
| format | Article |
| id | doaj.art-0a5beb41bdf64c2fbd88e2cab0650b39 |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-04-12T05:05:36Z |
| publishDate | 2022-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-0a5beb41bdf64c2fbd88e2cab0650b392022-12-22T03:46:53ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-11-011010.3389/fcell.2022.982663982663The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult ratsAna Jakovljevic0Gorana Agatonovic1Dubravka Aleksic2Milan Aksic3Gebhard Reiss4Eckart Förster5Antonios Stamatakis6Igor Jakovcevski7Joko Poleksic8Center for Laser Microscopy, Institute for Physiology and Biochemistry “Jean Giaja”, Faculty of Biology, University of Belgrade, Belgrade, SerbiaSchool of Medicine, Institute of Anatomy “Niko Miljanic”, University of Belgrade, Belgrade, SerbiaSchool of Medicine, Institute of Anatomy “Niko Miljanic”, University of Belgrade, Belgrade, SerbiaSchool of Medicine, Institute of Anatomy “Niko Miljanic”, University of Belgrade, Belgrade, SerbiaInstitut für Anatomie und Klinische Morphologie, Universität Witten/Herdecke, Witten, GermanyDepartment of Neuroanatomy and Molecular Brain Research, Institute of Anatomy, Ruhr-Universität Bochum, Bochum, GermanyBiology-Biochemistry Lab, School of Health Sciences, Faculty of Nursing, National and Kapodistrian University of Athens, Athens, GreeceInstitut für Anatomie und Klinische Morphologie, Universität Witten/Herdecke, Witten, GermanySchool of Medicine, Institute of Anatomy “Niko Miljanic”, University of Belgrade, Belgrade, SerbiaEarly life stress negatively impacts brain development and affects structure and function of parvalbumin immunopositive (PV+) inhibitory neurons. Main regulators of PV+ interneurons activity and plasticity are perineuronal nets (PNNs), an extracellular matrix formation that enwraps PV+ interneurons mainly in the neocortex and hippocampus. To experimentally address the impact of early life stress on the PNNs and PV+ interneurons in the medial prefrontal cortex and dorsal hippocampus in rats, we employed a 24 h maternal deprivation protocol. We show that maternal deprivation in the medial prefrontal cortex of adult rats caused a decrease in density of overall PNNs and PNNs that enwrap PV+ interneurons in the rostral cingulate cortex. Furthermore, a staining intensity decrease of overall PNNs and PNN+/PV+ cells was found in the prelimbic cortex. Finally, a decrease in both intensity and density of overall PNNs and PNNs surrounding PV+ cells was observed in the infralimbic cortex, together with increase in the intensity of VGAT inhibitory puncta. Surprisingly, maternal deprivation did not cause any changes in the density of PV+ interneurons in the mPFC, neither had it affected PNNs and PV+ interneurons in the hippocampus. Taken together, our findings indicate that PNNs, specifically the ones enwrapping PV+ interneurons in the medial prefrontal cortex, are affected by early life stress.https://www.frontiersin.org/articles/10.3389/fcell.2022.982663/fullperineuronal netsinterneuronsmaternal deprivationearly life stressprefrontal cortexhippocampus |
| spellingShingle | Ana Jakovljevic Gorana Agatonovic Dubravka Aleksic Milan Aksic Gebhard Reiss Eckart Förster Antonios Stamatakis Igor Jakovcevski Joko Poleksic The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats Frontiers in Cell and Developmental Biology perineuronal nets interneurons maternal deprivation early life stress prefrontal cortex hippocampus |
| title | The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| title_full | The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| title_fullStr | The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| title_full_unstemmed | The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| title_short | The impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| title_sort | impact of early life maternal deprivation on the perineuronal nets in the prefrontal cortex and hippocampus of young adult rats |
| topic | perineuronal nets interneurons maternal deprivation early life stress prefrontal cortex hippocampus |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2022.982663/full |
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