Extracellular Matrix Modulation Is Driven by Experience-Dependent Plasticity During Stroke Recovery

Quattromani, Miriana Jlenia; Pruvost, Mathilde; Guerreiro, Carla; Backlund, Fredrik; Englund, Elisabet; Aspberg, Anders; Jaworski, Tomasz; Hakon, Jakob; Ruscher, Karsten; Kaczmarek, Leszek; Vivien, Denis; Wieloch, Tadeusz

doi:10.1007/s12035-017-0461-2

Cited by 35 publications

(36 citation statements)

References 76 publications

(90 reference statements)

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“…In terms of the significance of PNN net integrity as an effector of SWR event frequency, expression and/or integrity of PNN components can be influenced by age, enrichment or disease (Berretta, 2012;Matuszko, Curreli, Kaushik, Becker, & Dityatev, 2017;Quattromani et al, 2017;Slaker, Barnes, Sorg, & Grimm, 2016;Wiegand et al, 2016). Glial cells express critical components of the PNN, and expression of components is regulated by factors including neuronal activity (Howell and Gottschall, 2012;Matthews et al, 2002;McRae et al, 2007;Song and Dityatev, 2017).…”

Section: Discussionmentioning

confidence: 99%

Disruption of perineuronal nets increases the frequency of sharp wave ripple events

et al. 2017

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Hippocampal sharp wave ripples (SWRs) represent irregularly occurring synchronous neuronal population events that are observed during phases of rest and slow wave sleep. SWR activity that follows learning involves sequential replay of training-associated neuronal assemblies and is critical for systems level memory consolidation. SWRs are initiated by CA2 or CA3 pyramidal cells (PCs) and require initial excitation of CA1 PCs as well as participation of parvalbumin (PV) expressing fast spiking (FS) inhibitory interneurons. These interneurons are relatively unique in that they represent the major neuronal cell type known to be surrounded by perineuronal nets (PNNs), lattice like structures composed of a hyaluronin backbone that surround the cell soma and proximal dendrites. Though the function of the PNN is not completely understood, previous studies suggest it may serve to localize glutamatergic input to synaptic contacts and thus influence the activity of ensheathed cells. Noting that FS PV interneurons impact the activity of PCs thought to initiate SWRs, and that their activity is critical to ripple expression, we examine the effects of PNN integrity on SWR activity in the hippocampus. Extracellular recordings from the stratum radiatum of horizontal murine hippocampal hemisections demonstrate SWRs that occur spontaneously in CA1.As compared with vehicle, pre-treatment (120 min) of paired hemislices with hyaluronidase, which cleaves the hyaluronin backbone of the PNN, decreases PNN integrity and increases SWR frequency. Pre-treatment with chondroitinase, which cleaves PNN side chains, also increases SWR frequency. Together, these data contribute to an emerging appreciation of extracellular matrix as a regulator of neuronal plasticity and suggest that one function of mature perineuronal nets could be to modulate the frequency of SWR events. K E Y W O R D Schondrotinase, hippocampus, hyaluronidase, protease, PV interneuron

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Section: Discussionmentioning

confidence: 99%

Disruption of perineuronal nets increases the frequency of sharp wave ripple events

et al. 2017

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“…In a similar manner, induced focal ischaemia into the rat motor cortex has been found to increase the activity of the ECM proteases tPA and matrix metalloproteinase (MMP)‐9 and to promote ECM remodelling by reducing the number of perineuronal nets (PNN) in the ipsilesional somatosensory cortex (Quattromani et al., ). Furthermore, multisensory stimulation through environmental enrichment at the early stages after stroke was found to increase proteolytic tPA and MMP‐9 activity and promote ECM remodelling and PNN degradation, resulting in improved functional outcomes suggestive of experience‐dependent plasticity (Quattromani et al., ). Analysis of postmortem brain tissue obtained from stroke patients has revealed equivalent tPA, MMP‐9, MMP‐2 and PNN expression profiles in brain regions proximal but also distal to the infarct (Quattromani et al., ).…”

Section: Introductionmentioning

confidence: 93%

“…Furthermore, multisensory stimulation through environmental enrichment at the early stages after stroke was found to increase proteolytic tPA and MMP‐9 activity and promote ECM remodelling and PNN degradation, resulting in improved functional outcomes suggestive of experience‐dependent plasticity (Quattromani et al., ). Analysis of postmortem brain tissue obtained from stroke patients has revealed equivalent tPA, MMP‐9, MMP‐2 and PNN expression profiles in brain regions proximal but also distal to the infarct (Quattromani et al., ).…”

Section: Introductionmentioning

confidence: 99%

Neuroplasticity in stroke recovery. The role of microglia in engaging and modifying synapses and networks

Sandvig

Augestad

Håberg

et al. 2018

Eur J of Neuroscience

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Neuroplasticity after ischaemic injury involves both spontaneous rewiring of neural networks and circuits as well as functional responses in neurogenic niches. These events involve complex interactions with activated microglia, which evolve in a dynamic manner over time. Although the exact mechanisms underlying these interactions remain poorly understood, increasing experimental evidence suggests a determining role of pro- and anti-inflammatory microglial activation profiles in shaping both synaptogenesis and neurogenesis. While the inflammatory response of microglia was thought to be detrimental, a more complex profile of the role of microglia in tissue remodelling is emerging. Experimental evidence suggests that microglia in response to injury can rapidly modify neuronal activity and modulate synaptic function, as well as be beneficial for the proliferation and integration of neural progenitor cells (NPCs) from endogenous neurogenic niches into functional networks thereby supporting stroke recovery. The manner in which microglia contribute towards sculpting neural synapses and networks, both in terms of activity-dependent and homeostatic plasticity, suggests that microglia-mediated pro- and/or anti-inflammatory activity may significantly contribute towards spontaneous neuronal plasticity after ischaemic lesions. In this review, we first introduce some of the key cellular and molecular mechanisms underlying neuroplasticity in stroke and then proceed to discuss the crosstalk between microglia and endogenous neuroplasticity in response to brain ischaemia with special focus on the engagement of synapses and neural networks and their implications for grey matter integrity and function in stroke repair.

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“…In terms of the significance of PNN net integrity as an effector of SWR event frequency, expression and/or integrity of PNN components can be influenced by age, 1 5 enrichment or disease (Berretta, 2012;Matuszko et al, 2017;Quattromani et al, 2017;Slaker et al, 2016a;Wiegand et al, 2016). Glial cells express critical components of the PNN, and expression of components is regulated by factors including neuronal activity (Howell and Gottschall, 2012;Matthews et al, 2002;McRae et al, 2007;Song and Dityatev, 2017).…”

Section: Discussionmentioning

confidence: 99%

Disruption of perineuronal nets increases the frequency of sharp wave ripples

Sun

Bozzelli

Caccavano

et al. 2017

Preprint

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Hippocampal sharp wave ripples (SWRs) represent irregularly occurring synchronous neuronal population events that are observed during phases of rest and slow wave sleep. SWR activity that follows learning involves sequential replay of training-associated neuronal assemblies and is critical for systems level memory consolidation. SWRs are initiated by CA2 or CA3 pyramidal cells and require initial excitation of CA1 pyramidal cells as well as subsequent participation of parvalbumin (PV) expressing fast spiking (FS) inhibitory interneurons. These interneurons are relatively unique in that they represent the major neuronal cell type known to be surrounded by perineuronal nets (PNNs), lattice like structures composed of a hyaluronin backbone that surround the cell soma and proximal dendrites. Though the function of the PNN is not completely understood, previous studies suggest it may serve to localize glutamatergic input to synaptic contacts and thus influence the activity of ensheathed cells. Noting that FS PV interneurons impact the activity of pyramidal cells thought to initiate SWRs, and that their activity is critical to ripple expression, we examine the effects of PNN integrity on SWR activity in the hippocampus. Extracellular recordings from the stratum radiatum of 490 micron horizontal murine hippocampal hemisections demonstrate SWRs that occur spontaneously in CA1. As compared to vehicle, pretreatment (120 min) of paired hemislices with hyaluronidase, which cleaves the hyaluronin backbone of the PNN, decreases PNN integrity and increases SWR frequency. Pretreatment with chondroitinase, which cleaves PNN side chains, also increases SWR frequency.Together, these data contribute to an emerging appreciation of extracellular matrix as a regulator of neuronal plasticity and suggest that one function of mature perineuronal nets could be to modulate the frequency of SWR events. peer-reviewed)

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Extracellular Matrix Modulation Is Driven by Experience-Dependent Plasticity During Stroke Recovery

Cited by 35 publications

References 76 publications

Disruption of perineuronal nets increases the frequency of sharp wave ripple events

Disruption of perineuronal nets increases the frequency of sharp wave ripple events

Neuroplasticity in stroke recovery. The role of microglia in engaging and modifying synapses and networks

Disruption of perineuronal nets increases the frequency of sharp wave ripples

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