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Experience-Dependent Plasticity and Modulation of Growth Regulatory Molecules at Central Synapses
Open accessAbstract
Structural remodeling or repair of neural circuits depends on the balance between intrinsic neuronal properties and regulatory cues present in the surrounding microenvironment. These processes are also influenced by experience, but it is still unclear how external stimuli modulate growth-regulatory mechanisms in the central nervous system. We asked whether environmental stimulation promotes neuronal plasticity by modifying the expression of growth-inhibitory molecules, specifically those of the extracellular matrix. We examined the effects of an enriched environment on neuritic remodeling and modulation of perineuronal nets in the deep cerebellar nuclei of adult mice. Perineuronal nets are meshworks of extracellular matrix that enwrap the neuronal perikaryon and restrict plasticity in the adult CNS. We found that exposure to an enriched environment induces significant morphological changes of Purkinje and precerebellar axon terminals in the cerebellar nuclei, accompanied by a conspicuous reduction of perineuronal nets. In the animals reared in an enriched environment, cerebellar nuclear neurons show decreased expression of mRNAs coding for key matrix components (as shown by real time PCR experiments), and enhanced activity of matrix degrading enzymes (matrix metalloproteinases 2 and 9), which was assessed by in situ zymography. Accordingly, we found that in mutant mice lacking a crucial perineuronal net component, cartilage link protein 1, perineuronal nets around cerebellar neurons are disrupted and plasticity of Purkinje cell terminal is enhanced. Moreover, all the effects of environmental stimulation are amplified if the afferent Purkinje axons are endowed with enhanced intrinsic growth capabilities, induced by overexpression of GAP-43. Our observations show that the maintenance and growth-inhibitory function of perineuronal nets are regulated by a dynamic interplay between pre- and postsynaptic neurons. External stimuli act on this interaction and shift the balance between synthesis and removal of matrix components in order to facilitate neuritic growth by locally dampening the activity of inhibitory cues.
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“In this model, decreased synthesis of Hapln1/Crtl1 and other PNN components is observed, suggesting that external stimuli may have a plasticity-permissive role by affecting the synthesis of link proteins (Foscarin et al., 2011).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Foscarin et al., 2011
In the citing paper
“Indeed, structural changes found after enriched environment, such as an enlargement of Purkinje axon boutons, are also observed in Hapln1/Crtl1 mice (Foscarin et al., 2011).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Foscarin et al., 2011
In the citing paper
“In this model, decreased synthesis of Hapln1/Crtl1 and other PNN components is observed, suggesting that external stimuli may have a plasticity-permissive role by affecting the synthesis of link proteins (Foscarin et al., 2011).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Foscarin et al., 2011
In the citing paper
“Enriched environment also promotes structural plasticity in the cerebellum, which is accompanied by a strong PNN reduction and a putative increase in the excitatory/inhibitory ratio.”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Foscarin et al., 2011
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“enriched environment rearing reduces PNNs in the cerebellum (32)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [32]
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Metadata
- Authors
- Foscarin, S., Ponchione, D., Pajaj, E., Leto, K., Gawlak, M., Wilczynski, G. M., Rossi, F., & Carulli, D.
- Affiliations
- Neuroscience Institute Cavalieri Ottolenghi (IT)
- Instytut Biologii Doświadczalnej im. Marcelego Nenckiego (PL)
- Corresponding author
- Rossi, Ferdinando
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-01-31
- Volume
- 6
- Issue
- 1
- Pages
- e16666
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3031615
- OpenAlex
- W2023333383
- Cited by
- 128
- References
- 56
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 15 · 2023: 5 · 2022: 7 · 2021: 10 · 2020: 8 · 2019: 7 · 2018: 8 · 2017: 9 · 2016: 10 · 2015: 9 · 2014: 10 · 2013: 9 · 2012: 7
- FWCI
- 4.10
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- International Foundation for Research in Paraplegia
- Ministero dell’Istruzione, dell’Università e della Ricerca
- Regione Piemonte
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- experience-dependent plasticity, perineuronal nets, extracellular matrix, environmental enrichment, deep cerebellar nuclei, Purkinje cells, matrix metalloproteinases, GAP-43, growth inhibition, neural circuit remodeling, postsynaptic modulation
- MeSH terms
- Animals, Central Nervous System, Cerebellar Nuclei, Extracellular Matrix, Nerve Tissue Proteins, Neuronal Plasticity, Purkinje Cells, Synapses, Neurites, GAP-43 Protein, Mice
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