Interneuron Development Is Disrupted in Preterm Brains With Diffuse White Matter Injury: Observations in Mouse and Human
Open accessAbstract
Preterm brain injury, occurring in approximately 30% of infants born <32 weeks gestational age, is associated with an increased risk of neurodevelopmental disorders, such as autism spectrum disorder (ASD) and attention deficit hyperactivity disorder (ADHD). The mechanism of grey matter injury in preterm born children is unclear and likely to be multifactorial, however inflammation, a high predictor of poor outcome in preterm infants, has been associated with disrupted interneuron maturation in a number of animal models. Interneurons are important for regulating normal brain development, and disruption in interneuron development, and the downstream effects of this, has been implicated in the aetiology of neurodevelopmental disorders. Here we utilise post-mortem tissue from human preterm cases with) or without diffuse white matter injury (WMI; PMA range: 23+2 to 28+1 for non-WMI group, 26+6 to 30+0 for WMI group, p=0.002), and a model of inflammation-induced preterm diffuse white matter injury (i.p. IL-1β, b.d., 10µg/kg/injection in male CD1 mice from P1-5). Data from human preterm infants show deficits in interneuron numbers in the cortex and delayed development of neuronal arbours at this early stage of development. In the mouse, significant reduction in the number of parvalbumin positive interneurons was observed from postnatal day (P) 10. This decrease in parvalbumin neuron number was largely rectified by P40, though there was a significantly smaller number of parvalbumin positive cells associated with perineuronal nets in the upper cortical layers. Together, these data suggest that inflammation in the preterm brain may be a contributor to injury of specific interneuron in the cortical grey matter. This may represent a potential target for postnatal therapy to reduce the incidence and/or severity of neurodevelopmental disorders in preterm infants.
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PNN has an indirect role over principal neurons via regulating synaptic plasticity and dendritic arborization of the interneuron.
“PNN has an indirect role over principal neurons via regulating synaptic plasticity (Sigal et al., 2019) and dendritic arborization (Stolp et al., 2019) of the interneuron.”
From Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis (2020) · cites this paper as Stolp et al., 2019
The Discussion suggests that changes involving perineuronal nets and parvalbumin interneurons may affect pyramidal-neuron function indirectly. But Stolp et al. do not show that perineuronal nets regulate interneuron dendritic arborization; the Results report no significant difference in the dendritic arborization of the cortical neurons examined at P40. The Stolp citation is attached specifically to the arborization part of the citing sentence. (LLM, conf=0.86)
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- Vontell R. Supramaniam V. Thornton C. Wyatt-Ashmead J. Mallard C. Gressens P.. (2013). Toll-like receptor 3 expression in glia and neurons alters in response to white matter injury in preterm infants. Dev. Neurosci. 35, 130– 139. 10.1159/000346158, PMID: 23548575 PMC3826123 · DOI
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- Wood N. S. Costeloe K. Gibson A. T. Hennessy E. M. Marlow N. Wilkinson A. R.. (2005). The EPICure study: associations and antecedents of neurological and developmental disability at 30 months of age following extremely preterm birth. Arch. Dis. Child. Fetal Neonatal Ed. 90, F134– F140. 10.1136/adc.2004.052407, PMID: 15724037 PMC1721849 · DOI
Cited by
Sorted by citations
Disrupted structural connectivity in ArcAβ mouse model of Aβ amyloidosis
Al-Amin, M. M., Grandjean, J., Klohs, J., & Kim, J. (2020) · doi:10.1101/2020.04.27.064634 · Cited by 2 · see citing works
“PNN has an indirect role over principal neurons via regulating synaptic plasticity (Sigal et al., 2019) and dendritic arborization (Stolp et al., 2019) of the interneuron.”
Background
- Authors
- Stolp, H. B., Fleiss, B., Arai, Y., Supramaniam, V., Vontell, R., Birtles, S., Yates, A. G., Baburamani, A. A., Thornton, C., Rutherford, M., Edwards, A. D., & Gressens, P.
- Affiliations
- Royal Veterinary College (GB)
- Inserm (FR)
- King's College London (GB)
- University of Miami (US)
- Corresponding author
- Stolp, Helen B.
- ORCID
- Venue
- Frontiers in Physiology
- Publisher
- Frontiers Media SA
- Published
- 2019-07-30
- Volume
- 10
- Pages
- 955-955
- ISSN
- 1664-042X (ISSN-L)
- PMC
- PMC6683859
- OpenAlex
- W2956435356
- Cited by
- 85
- References
- 12
- Citations by year
- 2026: 13 · 2025: 9 · 2024: 12 · 2023: 11 · 2022: 10 · 2021: 16 · 2020: 12 · 2019: 2
- FWCI
- 10.40
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Physiology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RVC Research Online (Royal Veterinary College) (submittedVersion, cc-by)
- RMIT Research Repository (RMIT University Library) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Research Portal (King's College London) (submittedVersion, cc-by)
- Funders
- Medical Research Council (MR/K006355/1)
- Fondation Roger de Spoelberch
- National Institute for Health Research (NIHR)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Development and Preterm Care
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- preterm brain injury, interneuron development, parvalbumin interneurons, neuroinflammation, IL-1β, cortical gray matter, perineuronal nets, neurodevelopmental disorders, autism spectrum disorder, attention deficit hyperactivity disorder
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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