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Initiation site of experimentally-evoked spreading depolarizations influence tissue outcomes in a murine stroke model.

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Τίτλος: Initiation site of experimentally-evoked spreading depolarizations influence tissue outcomes in a murine stroke model.
Συγγραφείς: Bennett MC; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: michael.bennett@umontreal.ca., Morton RA; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: ramorton@salud.unm.edu., Carlson AP; Department of Neurosurgery, University of Virginia, Charlottesville, VA 22903, USA. Electronic address: EQB2TS@uvahealth.org., Shuttleworth CW; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: bshuttleworth@salud.unm.edu.
Πηγή: Experimental neurology [Exp Neurol] 2026 May; Vol. 399, pp. 115671. Date of Electronic Publication: 2026 Jan 27.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Academic Press Country of Publication: United States NLM ID: 0370712 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1090-2430 (Electronic) Linking ISSN: 00144886 NLM ISO Abbreviation: Exp Neurol Subsets: MEDLINE
Imprint Name(s): Publication: Orlando Fl : Academic Press
Original Publication: New York.
Ιατρικοί όροι (MeSH): Cortical Spreading Depression*/physiology , Stroke*/physiopathology , Stroke*/pathology , Infarction, Middle Cerebral Artery*/physiopathology , Infarction, Middle Cerebral Artery*/pathology, Potassium Chloride/toxicity ; Animals ; Male ; Mice ; Disease Models, Animal ; Mice, Inbred C57BL ; Optogenetics
Περίληψη: Spreading depolarization waves (SDs) are implicated in secondary expansion of brain injuries and are the target for initial clinical intervention trials. However, the assumption that SD directly causes neuronal injury has been challenged by recent findings with experimentally-induced SD in stroke models. The current study addressed this controversy by examining whether stroke consequences are confounded by the precise location of experimental SD initiation. Focal ischemic lesions were generated by transient distal middle cerebral artery occlusion in male mice. Clusters of SDs (6 at 10-min intervals) were induced by either focal KCl application or optogenetic stimulation during occlusion. SDs were initiated either in regions close to the infarct core (penumbral-SD; <50% perfusion) or in less compromised tissue in the same hemisphere (remote-SD; >70% perfusion). Despite the fact that all SDs fully invaded stroke expansion areas, the location of experimental SD induction had significant effects on stroke outcomes measured 48 h after reperfusion. Penumbral-SDs resulted in larger infarct expansion than seen in control stroke mice lacking experimentally-imposed SD. Conversely, remote-SDs led to significantly smaller infarcts than stroke alone. Laser speckle contrast imaging of blood flow in injury expansion areas showed enhanced hypoperfusion responses after penumbral-SDs and larger hyperemic responses after remote-SDs, suggesting that differential vascular responses could contribute to stroke outcomes. Overall, this study helps to reconcile different prior reports by showing that experimentally-induced SDs can either exacerbate or reduce stroke-induced injury depending on the SD initiation site and further strengthens evidence for injurious roles of SDs initiating in vulnerable brain tissue.
(Copyright © 2026 The Authors. Published by Elsevier Inc. All rights reserved.)
Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Σχόλια: Update of: bioRxiv. 2025 Oct 06:2025.10.03.680372. doi: 10.1101/2025.10.03.680372.. (PMID: 41279059)
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J Neurosci. 2003 Dec 17;23(37):11602-10. (PMID: 14684862)
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Neurology. 2013 Mar 19;80(12):1095-102. (PMID: 23446683)
J Neurophysiol. 2007 Jun;97(6):4143-51. (PMID: 17329631)
J Biomed Opt. 2011 Jan-Feb;16(1):016009. (PMID: 21280915)
Brain. 2010 Jul;133(Pt 7):1994-2006. (PMID: 20504874)
Stroke. 1986 Nov-Dec;17(6):1304-8. (PMID: 2433817)
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J Cereb Blood Flow Metab. 1996 Mar;16(2):202-13. (PMID: 8594051)
J Cereb Blood Flow Metab. 1996 Nov;16(6):1090-9. (PMID: 8898680)
Eur J Neurosci. 2014 Nov;40(9):3413-21. (PMID: 25216240)
J Cereb Blood Flow Metab. 1994 Jan;14(1):12-9. (PMID: 8263047)
Exp Neurol. 2015 May;267:243-53. (PMID: 25819105)
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Grant Information: P30 GM159568 United States GM NIGMS NIH HHS; P20 GM109089 United States GM NIGMS NIH HHS; F31 NS129351 United States NS NINDS NIH HHS; R01 NS106901 United States NS NINDS NIH HHS; R01 NS128006 United States NS NINDS NIH HHS
Contributed Indexing: Keywords: Cortical spreading depression; Ischemic stroke; MCAo; Neuronal injury; Optogenetic
Substance Nomenclature: 660YQ98I10 (Potassium Chloride)
Entry Date(s): Date Created: 20260129 Date Completed: 20260701 Latest Revision: 20260920
Update Code: 20260920
PubMed Central ID: PMC12910855
DOI: 10.1016/j.expneurol.2026.115671
PMID: 41611073
Βάση Δεδομένων: MEDLINE
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  Data: Initiation site of experimentally-evoked spreading depolarizations influence tissue outcomes in a murine stroke model.
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  Data: &lt;searchLink fieldCode=&quot;AU&quot; term=&quot;%22Bennett+MC%22&quot;&gt;Bennett MC&lt;/searchLink&gt;; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: michael.bennett@umontreal.ca.&lt;br /&gt;&lt;searchLink fieldCode=&quot;AU&quot; term=&quot;%22Morton+RA%22&quot;&gt;Morton RA&lt;/searchLink&gt;; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: ramorton@salud.unm.edu.&lt;br /&gt;&lt;searchLink fieldCode=&quot;AU&quot; term=&quot;%22Carlson+AP%22&quot;&gt;Carlson AP&lt;/searchLink&gt;; Department of Neurosurgery, University of Virginia, Charlottesville, VA 22903, USA. Electronic address: EQB2TS@uvahealth.org.&lt;br /&gt;&lt;searchLink fieldCode=&quot;AU&quot; term=&quot;%22Shuttleworth+CW%22&quot;&gt;Shuttleworth CW&lt;/searchLink&gt;; Department of Neurosciences, University of New Mexico, Albuquerque, NM 87131, USA. Electronic address: bshuttleworth@salud.unm.edu.
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  Data: &lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Cortical+Spreading+Depression%22&quot;&gt;Cortical Spreading Depression*&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Cortical+Spreading+Depression+physiology%22&quot;&gt;physiology&lt;/searchLink&gt; &lt;br /&gt;&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Stroke%22&quot;&gt;Stroke*&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Stroke+physiopathology%22&quot;&gt;physiopathology&lt;/searchLink&gt; &lt;br /&gt;&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Stroke%22&quot;&gt;Stroke*&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Stroke+pathology%22&quot;&gt;pathology&lt;/searchLink&gt; &lt;br /&gt;&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Infarction%2C+Middle+Cerebral+Artery%22&quot;&gt;Infarction, Middle Cerebral Artery*&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Infarction%2C+Middle+Cerebral+Artery+physiopathology%22&quot;&gt;physiopathology&lt;/searchLink&gt; &lt;br /&gt;&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Infarction%2C+Middle+Cerebral+Artery%22&quot;&gt;Infarction, Middle Cerebral Artery*&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MM&quot; term=&quot;%22Infarction%2C+Middle+Cerebral+Artery+pathology%22&quot;&gt;pathology&lt;/searchLink&gt;&lt;br /&gt;&lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Potassium+Chloride%22&quot;&gt;Potassium Chloride&lt;/searchLink&gt;/&lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Potassium+Chloride+toxicity%22&quot;&gt;toxicity&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Animals%22&quot;&gt;Animals&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Male%22&quot;&gt;Male&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Mice%22&quot;&gt;Mice&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Disease+Models%2C+Animal%22&quot;&gt;Disease Models, Animal&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Mice%2C+Inbred+C57BL%22&quot;&gt;Mice, Inbred C57BL&lt;/searchLink&gt; ; &lt;searchLink fieldCode=&quot;MH&quot; term=&quot;%22Optogenetics%22&quot;&gt;Optogenetics&lt;/searchLink&gt;
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  Data: Spreading depolarization waves (SDs) are implicated in secondary expansion of brain injuries and are the target for initial clinical intervention trials. However, the assumption that SD directly causes neuronal injury has been challenged by recent findings with experimentally-induced SD in stroke models. The current study addressed this controversy by examining whether stroke consequences are confounded by the precise location of experimental SD initiation. Focal ischemic lesions were generated by transient distal middle cerebral artery occlusion in male mice. Clusters of SDs (6 at 10-min intervals) were induced by either focal KCl application or optogenetic stimulation during occlusion. SDs were initiated either in regions close to the infarct core (penumbral-SD; &amp;lt;50% perfusion) or in less compromised tissue in the same hemisphere (remote-SD; &amp;gt;70% perfusion). Despite the fact that all SDs fully invaded stroke expansion areas, the location of experimental SD induction had significant effects on stroke outcomes measured 48&#160;h after reperfusion. Penumbral-SDs resulted in larger infarct expansion than seen in control stroke mice lacking experimentally-imposed SD. Conversely, remote-SDs led to significantly smaller infarcts than stroke alone. Laser speckle contrast imaging of blood flow in injury expansion areas showed enhanced hypoperfusion responses after penumbral-SDs and larger hyperemic responses after remote-SDs, suggesting that differential vascular responses could contribute to stroke outcomes. Overall, this study helps to reconcile different prior reports by showing that experimentally-induced SDs can either exacerbate or reduce stroke-induced injury depending on the SD initiation site and further strengthens evidence for injurious roles of SDs initiating in vulnerable brain tissue.&lt;br /&gt; (Copyright &#169; 2026 The Authors. Published by Elsevier Inc. All rights reserved.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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  Label: Comments
  Group: Commnt
  Data: Update of: bioRxiv. 2025 Oct 06:2025.10.03.680372. doi: 10.1101/2025.10.03.680372.. (PMID: &lt;searchLink fieldCode=&quot;PM&quot; term=&quot;%2241279059%22&quot;&gt;41279059)&lt;/searchLink&gt;
– Name: Ref
  Label: References
  Group: RefInfo
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– Name: GrantInfo
  Label: Grant Information
  Group: Grant
  Data: P30 GM159568 United States GM NIGMS NIH HHS; P20 GM109089 United States GM NIGMS NIH HHS; F31 NS129351 United States NS NINDS NIH HHS; R01 NS106901 United States NS NINDS NIH HHS; R01 NS128006 United States NS NINDS NIH HHS
– Name: SubjectMinor
  Label: Contributed Indexing
  Group:
  Data: &lt;i&gt;Keywords: &lt;/i&gt;Cortical spreading depression; Ischemic stroke; MCAo; Neuronal injury; Optogenetic
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  Data: 660YQ98I10 (Potassium Chloride)
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  Data: &lt;i&gt;Date Created: &lt;/i&gt;20260129 &lt;i&gt;Date Completed: &lt;/i&gt;20260701 &lt;i&gt;Latest Revision: &lt;/i&gt;20260920
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  Data: 20260920
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  Label: PubMed Central ID
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  Data: PMC12910855
– Name: DOI
  Label: DOI
  Group: ID
  Data: 10.1016/j.expneurol.2026.115671
– Name: AN
  Label: PMID
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  Data: 41611073
PLink https://search.ebscohost.com/login.aspx?direct=true&site=eds-live&db=cmedm&AN=41611073
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      – Type: doi
        Value: 10.1016/j.expneurol.2026.115671
    Languages:
      – Code: eng
        Text: English
    PhysicalDescription:
      Pagination:
        StartPage: 115671
    Subjects:
      – SubjectFull: Potassium Chloride toxicity
        Type: general
      – SubjectFull: Animals
        Type: general
      – SubjectFull: Male
        Type: general
      – SubjectFull: Mice
        Type: general
      – SubjectFull: Disease Models, Animal
        Type: general
      – SubjectFull: Mice, Inbred C57BL
        Type: general
      – SubjectFull: Optogenetics
        Type: general
      – SubjectFull: Cortical Spreading Depression physiology
        Type: general
      – SubjectFull: Stroke physiopathology
        Type: general
      – SubjectFull: Stroke pathology
        Type: general
      – SubjectFull: Infarction, Middle Cerebral Artery physiopathology
        Type: general
      – SubjectFull: Infarction, Middle Cerebral Artery pathology
        Type: general
    Titles:
      – TitleFull: Initiation site of experimentally-evoked spreading depolarizations influence tissue outcomes in a murine stroke model.
        Type: main
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            NameFull: Bennett MC
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            NameFull: Morton RA
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            NameFull: Carlson AP
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            NameFull: Shuttleworth CW
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          Dates:
            – D: 01
              M: 05
              Text: 2026 May
              Type: published
              Y: 2026
          Identifiers:
            – Type: issn-electronic
              Value: 1090-2430
          Numbering:
            – Type: volume
              Value: 399
          Titles:
            – TitleFull: Experimental neurology
              Type: main
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