Hypoxia-Induced Developmental Delays of Inhibitory Interneurons Are Reversed by Environmental Enrichment in the Postnatal Mouse Forebrain
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Infants born premature experience hypoxic episodes due to immaturity of their respiratory and central nervous systems. This profoundly affects brain development and results in cognitive impairments. We used a mouse model to examine the impact of hypoxic rearing (9.5–10.5% O 2) from postnatal day 3 to 11 (P3–P11) on GABAergic interneurons and the potential for environmental enrichment to ameliorate these developmental abnormalities. At P15 the numbers of cortical interneurons expressing immunohistochemically detectable levels of parvalbumin (PV), somatostatin (SST), and vasoactive intestinal peptide were decreased in hypoxic-reared mice by 59%, 32%, and 38%, respectively, compared with normoxic controls. Hypoxia also decreased total GABA content in frontal neocortex by 31%. However, GAD67-EGFP knock-in mice reared under hypoxic conditions showed no changes in total number of GAD67-EGFP+cells and no evidence of increased interneuron death, suggesting that the total number of interneurons was not decreased, but rather, that hypoxic-rearing decreased interneuron marker expression in these cells. In adulthood, PV and SST expression levels were decreased in hypoxic-reared mice. In contrast, intensity of reelin (RLN) expression was significantly increased in adult hypoxic-reared mice compared with normoxic controls. Housing mice in an enriched environment from P21 until adulthood normalized phenotypic interneuron marker expression without affecting total interneuron numbers or leading to increased neurogenesis. Our data show that (1) hypoxia decreases PV and SST and increases RLN expression in cortical interneurons during postnatal cortical development and (2) enriched environment has the capacity to normalize the interneuron abnormalities in cortex.
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Multiple fetuses per pregnancy, intrauterine growth restriction (IUGR), X-ray, UV, nuclear or cosmic radiation, (ultra)sound as well as high temperature, preterm birth or hypoxia whether or not by traumatic causes can pose serious threats to proper corticogenesis.
“Multiple fetuses per pregnancy, intrauterine growth restriction (IUGR, due to placental failure other than by causes described above), X-ray, UV, nuclear or cosmic radiation, (ultra)sound as well as high temperature, preterm birth or hypoxia whether or not by traumatic causes can pose serious threats to proper corticogenesis as well [349–356].”
From Development of prefrontal cortex (2022) · cites this paper as [350]
The Introduction and Discussion (page numbers unavailable) link premature birth and postnatal hypoxia to disrupted cortical development, including lasting changes in inhibitory interneurons in a mouse model. The paper does not address the sentence’s other proposed threats, such as multiple fetuses, IUGR, radiation, ultrasound, or high temperature; nor does it establish effects of traumatic causes of hypoxia. (LLM, conf=0.87)
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- Authors
- Komitova, M., Xenos, D., Salmaso, N., May Tran, K., Brand, T., Schwartz, M. L., Ment, L., & Vaccarino, F. M.
- Affiliations
- Yale University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-08-14
- Volume
- 33
- Issue
- 33
- Pages
- 13375-13387
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3742925
- OpenAlex
- W2107713038
- Cited by
- 88
- References
- 63
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 1 · 2023: 4 · 2022: 4 · 2021: 8 · 2020: 8 · 2019: 3 · 2018: 7 · 2017: 10 · 2016: 6 · 2015: 18 · 2014: 6 · 2013: 1
- FWCI
- 9.62
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research
- National Institute of Neurological Disorders and Stroke (P01NS062686, R01NS060750, P01NS035476)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- hypoxia, developmental delay, inhibitory interneurons, environmental enrichment, GABAergic interneurons, parvalbumin, somatostatin, vasoactive intestinal peptide, reelin, GABA levels, GAD67, cortical development, preterm birth, postnatal development, mouse model
- MeSH terms
- Reelin Protein, Animals, Hypoxia, Cerebral Cortex, Chromatography, High Pressure Liquid, Disease Models, Animal, Housing, Animal, Immunohistochemistry, Interneurons, Mice, Inbred C57BL, Mice, Transgenic, Nerve Tissue Proteins, Parvalbumins, Serine Endopeptidases, Somatostatin, Cell Adhesion Molecules, Neuronal, Extracellular Matrix Proteins, Prosencephalon, Mice, Gene Knock-In Techniques
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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