Depletion of Perineuronal Nets Enhances Recognition Memory and Long-Term Depression in the Perirhinal Cortex
Open accessAbstract
Perineuronal nets (PNNs) are extracellular matrix structures surrounding cortical neuronal cell bodies and proximal dendrites and are involved in the control of brain plasticity and the closure of critical periods. Expression of the link protein Crtl1/Hapln1 in neurons has recently been identified as the key event triggering the formation of PNNs. Here we show that the genetic attenuation of PNNs in adult brain Crtl1 knock-out mice enhances long-term object recognition memory and facilitates long-term depression in the perirhinal cortex, a neural correlate of object recognition memory. Identical prolongation of memory follows localized digestion of PNNs with chondroitinase ABC, an enzyme that degrades the chondroitin sulfate proteoglycan components of PNNs. The memory-enhancing effect of chondroitinase ABC treatment attenuated over time, suggesting that the regeneration of PNNs gradually restored control plasticity levels. Our findings indicate that PNNs regulate both memory and experience-driven synaptic plasticity in adulthood.
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In general, there is an overall increase in network activity when PNNs are depleted or attenuated.
“However, in general, there is an overall increase in network activity when PNNs are depleted or attenuated [53, 59, 68], possibly due to an overall reduction in inhibitory activity.”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [53]
The Introduction reports enhanced basal synaptic transmission after genetic or enzymatic PNN reduction, and the Discussion describes enhanced excitatory transmission in the perirhinal cortex of treated mice. These findings support increased transmission in that setting, but not a general increase in overall network activity. Page numbers are unavailable in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measuredDigestion of CSPGs in PrC or transgenic attenuation of PNNs greatly extends object memory, from 12 to 96 hours.
“Digestion of CSPGs in PrC or transgenic attenuation of PNNs had the effect of greatly extending object memory, from 12 to 96 hours (Romberg et al., 2013).”
From Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity (2016) · cites this paper as Romberg et al., 2013
The Results report that both perirhinal chABC treatment and Crtl1 knockout prolonged object recognition memory in mice. But the Methods list recognition-test delays only up to 48 hours, and the Results report memory at 48 hours in the treated mice while controls showed no memory by 24 hours. The claimed extension from 12 to 96 hours is not supported. (LLM, conf=0.90)
Experimental — accuracy not yet measuredDeletion of link proteins leads to fewer Purkinje synapses, decreases inhibitory transmission in the deep cerebellar nucleus, and facilitates long-term depression in the perirhinal cortex.
“Deletion of link proteins leads to fewer Purkinje synapses, decreases inhibitory transmission in the deep cerebellar nucleus [52], and facilitates long-term depression in the perirhinal cortex [53].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [53]
Long-term depression (LTD) is altered after PNN degradation, with both increases and decreases reported.
“Long-term depression (LTD) is also altered after PNN degradation, with both increases [67] and decreases [53, 60] reported.”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [53]
Genetic or enzymatic attenuation of PNNs can increase synaptic transmission and facilitate long-term depression (LTD) in the perirhinal cortex or CA1 region, and this correlates with enhanced recognition memory.
“Genetic or enzymatic attenuation of PNNs can increase synaptic transmission and facilitate long-term depression (LTD) in the perirhinal cortex [53] or CA1 region [67], and this correlates with enhanced recognition memory.”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [53]
Contrasting effects of PNN ablation on certain memory tasks and measures of plasticity suggest this is not the case for all types of memory, but differences may be partly attributable to the PNN ablation method used.
“Although contrasting effects of PNN ablation on certain (specifically object recognition) memory tasks and measures of plasticity suggest this is not the case for all types of memory [21, 29, 87], such differences may also be at least partly attributable to the PNN ablation method utilized (e.g. enzymatic digestion vs genetic deletion of PNN components) which can produce differential effects on”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [87]
The time course of plasticity induced by LRx may be determined by regrowth of the ECM.
“The time course of the plasticity induced by LRx may be determined by regrowth of the ECM, which mirrors the reformation of the mature ECM observed after enzymatic degradation (Lensjø et al., 2017; Romberg et al., 2013).”
From Light reintroduction after dark exposure reactivates plasticity in adults via perisynaptic activation of MMP-9 (2017) · cites this paper as Romberg et al., 2013
ChABC-induced enhancement of object recognition is reversible; memory gradually returns to control levels over 8 weeks, suggesting reoccurring PNNs restore control plasticity.
“ChABC induced enhancement of object recognition was reversible. Notably, over the course of 8 weeks, memory gradually returned to control levels, suggesting that reoccurring PNNs gradually restore control plasticity levels (Romberg et al., 2013)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Romberg et al., 2013
ChABC depletion of PNNs enhances object recognition and facilitates long-term depression in perirhinal cortex.
“a depletion of PNNs in animals following localized digestion with ChABC was shown to result in enhanced object recognition, in addition to a facilitation of long-term depression in the perirhinal cortex”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Romberg et al., 2013
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Yang, S., Hilton, S., Alves, J. N., Saksida, L. M., Bussey, T., Matthews, R. T., Kitagawa, H., Spillantini, M. G., Kwok, J. C. F., & Fawcett, J. W. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.08.002 · Cited by 61 · see citing works
Self-citationModulation of semaphorin3A in perineuronal nets during structural plasticity in the adult cerebellum
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Differential regulation of perineuronal nets in the brain and spinal cord with exercise training
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- Authors
- Romberg, C., Yang, S., Melani, R., Andrews, M. R., Horner, A. E., Spillantini, M. G., Bussey, T. J., Fawcett, J. W., Pizzorusso, T., & Saksida, L. M.
- Affiliations
- Max Planck Institute of Psychiatry (DE)
- University of Cambridge (GB)
- Neuroscience Institute (IT)
- University of St Andrews (GB)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2013-04-17
- Volume
- 33
- Issue
- 16
- Pages
- 7057-7065
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3655688
- OpenAlex
- W2060784568
- Cited by
- 231
- References
- 55
- Citations by year
- 2026: 13 · 2025: 19 · 2024: 13 · 2023: 20 · 2022: 21 · 2021: 23 · 2020: 23 · 2019: 19 · 2018: 19 · 2017: 20 · 2016: 12 · 2015: 6 · 2014: 18 · 2013: 5
- FWCI
- 7.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Florence Research (University of Florence) (submittedVersion)
- ePrints Soton (University of Southampton) (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Scuola Normale Superiore di Pisa (submittedVersion)
- Funders
- Wellcome Trust (089703, 223326)
- Acorda Therapeutics
- Alzheimer's Research Trust
- National Institute for Health and Care Research
- European Commission (254801, 223524, 223326)
- Medical Research Council (MC_G1000734)
- NIHR Cambridge Biomedical Research Centre
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- perineuronal nets, chondroitinase ABC, object recognition memory, long-term depression, perirhinal cortex, synaptic plasticity, extracellular matrix, memory enhancement, chondroitin sulfate proteoglycans, adult brain plasticity
- MeSH terms
- Proteoglycan Link Protein, Analysis of Variance, Animals, Animals, Newborn, Cerebral Cortex, Electric Stimulation, Extracellular Matrix, Genotype, Male, Mice, Inbred BALB C, Mice, Transgenic, Neurons, Penicillinase, Proteoglycans, Time Factors, Extracellular Matrix Proteins, Excitatory Postsynaptic Potentials, Chondroitin ABC Lyase, Recognition, Psychology, Long-Term Synaptic Depression, Mice
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