Cited by 82Stroke Rehabilitation and RecoveryNeurogenesis and neuroplasticity mechanismsSpinal Cord Injury Research

Enriched housing enhances recovery of limb placement ability and reduces aggrecan-containing perineuronal nets in the rat somatosensory cortex after experimental stroke.

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Madinier, Alexandre, Quattromani, Miriana Jlenia, Sjölund, Carin, Ruscher, Karsten, Wieloch, Tadeusz·2014·PLoS ONE

Abstract

Stroke causes life long disabilities where few therapeutic options are available. Using electrical and magnetic stimulation of the brain and physical rehabilitation, recovery of brain function can be enhanced even late after stroke. Animal models support this notion, and housing rodents in an enriched environment (EE) several days after experimental stroke stimulates lost brain function by multisensory mechanisms. We studied the dynamics of functional recovery of rats with a lesion to the fore and hind limb motor areas induced by photothrombosis (PT), and with subsequent housing in either standard (STD) or EE. In this model, skilled motor function is not significantly enhanced by enriched housing, while the speed of recovery of sensori-motor function substantially improves over the 9-week study period. In particular, this stroke lesion completely obliterates the fore and hind limb placing ability when visual and whisker guidance is prevented, a deficit that persists for up to 9 weeks of recovery, but that is markedly restored within 2 weeks by enriched housing. Enriched housing after stroke also leads to a significant loss of perineuronal net (PNN) immunoreactivity; detection of aggrecan protein backbone with AB1031 antibody was decreased by 13-22%, and labelling of a glycan moiety of aggrecan with Cat-315 antibody was reduced by 25-30% in the peri-infarct area and in the somatosensory cortex, respectively. The majority of these cells are parvalbumin/GABA inhibitory interneurons that are important in sensori-information processing. We conclude that damage to the fore and hind limb motor areas provides a model of loss of limb placing response without visual guidance, a deficit also seen in more than 50% of stroke patients. This loss is amenable to recovery induced by multiple sensory stimulation and correlates with a decrease in aggrecan-containing PNNs around inhibitory interneurons. Modulating the PNN structure after ischemic damage may provide new therapies enhancing tactile/proprioceptive function after stroke.

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Crossref · 10.1371/journal.pone.0093121

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  • Rats housed in enriched environments following ischemic damage exhibited faster neurological recovery compared to rats placed in standard housing.

    “recent findings in rodent stroke models indicate that rats housed in enriched environments following ischemic damage exhibited faster neurological recovery compared to rats placed in standard housing (Madinier et al., 2014; Quattromani et al., 2018).”
  • Ischemia-induced damage of PNs in rat neocortices was analyzed by Bidmon et al. (1998) and by Wieloch's research group using a similar animal model.

    “Using a similar animal model, ischemia-induced damage of PNs in rat neocortices was analyzed by Bidmon et al. (1998) and by Wieloch’s research group (Madinier et al., 2014; Quattromani et al., 2017).”
  • Abolished and decomposed PNs were reported for other animal models of experimentally induced stroke in neocortices of rats.

    “Based on WFA staining, abolished and decomposed PNs were also reported for other animal models of experimentally induced stroke in neocortices of rats (Hobohm et al., 2005; Karetko-Sysa et al., 2011; Madinier et al., 2014; Quattromani et al., 2017).”
  • Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced perineuronal nets.

    “Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced PNs, modulated activity and mRNA expression of ECM proteases and their inhibitors, accompanied by enhanced recovery of limb placement ability (Madinier et al., 2014; Quattromani et al., 2017).”
  • Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction modulated activity and mRNA expression of extracellular matrix proteases and their inhibitors.

    “Following cortical photothrombotic stroke in rats, enriched housing after ischemia induction reduced PNs, modulated activity and mRNA expression of ECM proteases and their inhibitors, accompanied by enhanced recovery of limb placement ability (Madinier et al., 2014; Quattromani et al., 2017).”

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Authors
Madinier, A., Quattromani, M. J., Sjölund, C., Ruscher, K., & Wieloch, T.
Affiliations
Lund University (SE)
Corresponding author
Wieloch, Tadeusz
Venue
PLoS ONE
Published
2014-03-24
Volume
9
Issue
3
Pages
e93121
ISSN
1932-6203 (ISSN-L)
OpenAlex
W1973274270
Cited by
82
References
93
Citations by year
2026: 6 · 2025: 7 · 2024: 2 · 2023: 8 · 2022: 8 · 2021: 7 · 2020: 3 · 2019: 7 · 2018: 13 · 2017: 7 · 2016: 7 · 2015: 3 · 2014: 3
FWCI
6.47
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Lund University Publications (Lund University) (submittedVersion, other-oa)
Funders
  • Crafoordska Stiftelsen
  • Vetenskapsrådet (201024, 2011-02684, 2011-02652)
  • Greta och Johan Kocks stiftelser
Topics
  • Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
Keywords
environmental enrichment, stroke recovery, perineuronal nets, aggrecan, somatosensory cortex, sensorimotor function, parvalbumin interneurons, photothrombosis, stroke rehabilitation, multisensory stimulation
MeSH terms
Animals, Hindlimb, Male, Nerve Net, Proprioception, Somatosensory Cortex, Rats, Sprague-Dawley, Stroke, Rats, Aggrecans, Touch Perception

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