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Cited by 88Traumatic Brain Injury and Neurovascular DisturbancesAcute Ischemic Stroke ManagementNeuroinflammation and Neurodegeneration Mechanisms

Persistent astroglial swelling accompanies rapid reversible dendritic injury during stroke-induced spreading depolarizations

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Risher, W. Christopher, Croom, Deborah, Kirov, Sergei A.·2012·Glia
DOI 10.1002/glia.22390PMC PMC3435464
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Abstract

Spreading depolarizations are a key event in the pathophysiology of stroke, resulting in rapid dendritic beading, which represents acute damage to synaptic circuitry. The impact of spreading depolarizations on the real‐time injury of astrocytes during ischemia is less clear. We used simultaneous in vivo 2‐photon imaging and electrophysiological recordings in adult mouse somatosensory cortex to examine spreading depolarization‐induced astroglial structural changes concurrently with signs of neuronal injury in the early periods of focal and global ischemia. Astrocytes in the metabolically compromised ischemic penumbra‐like area showed a long lasting swelling response to spontaneous spreading depolarizations despite rapid dendritic recovery in a photothrombotic occlusion model of focal stroke. Astroglial swelling was often facilitated by recurrent depolarizations and the magnitude of swelling strongly correlated with the total duration of depolarization. In contrast, spreading depolarization‐induced astroglial swelling was transient in normoxic healthy tissue. In a model of transient global ischemia, the occurrence of a single spreading depolarization elicited by a bilateral common carotid artery occlusion coincided with astroglial swelling alongside dendritic beading. With immediate reperfusion, dendritic beading subsides. Astroglial swelling was either transient during short ischemic periods distinguished by a short‐lasting spreading depolarization, or persistent during severe ischemia characterized by a long‐lasting depolarization with the ultraslow negative voltage component. We propose that persistent astroglial swelling is initiated and exacerbated during spreading depolarization in brain tissue with moderate to severe energy deficits, disrupting astroglial maintenance of normal homeostatic function thus contributing to the negative outcome of ischemic stroke as astrocytes fail to provide neuronal support. © 2012 Wiley Periodicals, Inc.

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  • Persistent astroglial swelling by ~28% was observed between 30-60 min of severe episode of global ischaemia induced by bilateral common carotid artery occlusion.

    “Likewise in another study (Risher et al., 2012), we observed persistent astroglial swelling by $28% between 30-60 min of severe episode of global ischaemia induced by a bilateral common carotid artery occlusion.”

    From Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging (2013) · cites this paper as Risher et al., 2012

    The Results (Fig. 5C; page unavailable) report persistent astroglial swelling after BCCAO-induced spreading depolarization under severe metabolic compromise. They report 29.8 ± 4.3% swelling at about 88 minutes after depolarization onset, not approximately 28% between 30 and 60 minutes. The 30–60-minute measurement in the Results (Fig. 1E) concerns a different experimental condition. (LLM, conf=0.86)

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  • In the early minutes to hours following stroke, astrocytes swell and remain swollen in the ischaemic neocortex with moderate to severe energy deficits.

    “Recently we have shown that in the early minutes to hours following stroke, astrocytes swell and remain swollen in the ischaemic neocortex with moderate to severe energy deficits (Risher et al., 2012).”

    From Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging (2013) · cites this paper as Risher et al., 2012

  • Astrocytes in the metabolically compromised ischaemic penumbra showed a persistent swelling of ~31% between 30-60 min following photothrombotic occlusion.

    “Furthermore, astrocytes in the metabolically compromised ischaemic penumbra showed a persistent swelling of $31% between 30-60 min following photothrombotic occlusion (Risher et al., 2012).”

    From Evolution of neuronal and astroglial disruption in the peri-contusional cortex of mice revealed by in vivo two-photon imaging (2013) · cites this paper as Risher et al., 2012

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Research works printed but not linked: 1

  1. Mongin AA Kimelberg HK Kettenmann H Ransom BR Astrocytic swelling in neuropathology Neuroglia 2005 Oxford/New York Oxford University Press 550 562

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Authors
Risher, W. C., Croom, D., & Kirov, S. A.
Affiliations
Augusta University Health (US)
Corresponding author
Kirov, Sergei A.
ORCID
Venue
Glia
Publisher
Wiley
Published
2012-07-20
Volume
60
Issue
11
Pages
1709-1720
ISSN
  • 0894-1491 (ISSN-L)
  • 1098-1136
DOI
10.1002/glia.22390
PMC
PMC3435464
OpenAlex
W2026613673
Semantic Scholar
8878bf488baf7f31739826f7e43a1fca6c6804c0
Cited by
88
References
46
Citations by year
2026: 2 · 2025: 4 · 2024: 4 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 8 · 2019: 6 · 2018: 8 · 2017: 8 · 2016: 9 · 2015: 6 · 2014: 10 · 2013: 4 · 2012: 1
FWCI
4.39
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Glia (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Neurological Disorders and Stroke (R01NS057113, F31NS064753, NS057113, NS064753)
Topics
  • Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
  • Health Sciences › Medicine › Epidemiology › Acute Ischemic Stroke Management
  • Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords
spreading depolarization, ischemic stroke, focal cerebral ischemia, global cerebral ischemia, photothrombotic stroke, somatosensory cortex, ischemic penumbra, astrocyte energy metabolism, reperfusion
MeSH terms
Animals, Astrocytes, Brain, Brain Ischemia, Dendrites, Female, Male, Mice, Transgenic, Cortical Spreading Depression, Stroke, Cell Enlargement, Mice

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