PreprintCited by 27Memory and Neural MechanismsNeuroscience and Neuropharmacology ResearchNeurogenesis and neuroplasticity mechanisms

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Perineuronal nets affect memory and learning after synapse withdrawal

Open access
Ruzicka, Jiri, Dalecka, Marketa, Safrankova, Kristyna, Peretti, Diego, Mallucci, Giovanna, Jendelova, Pavla, Kwok, Jessica CF, Fawcett, James W·2021·Translational Psychiatry

Abstract

Perineuronal nets (PNNs) enwrap mature neurons, playing a role in the control of plasticity and synapse dynamics. PNNs have been shown to have effects on memory formation, retention and extinction in a variety of animal models. It has been proposed that the cavities in PNNs which contain synapses can act as a memory store, which remains stable after events that cause synaptic withdrawal such as anoxia or hibernation. We examine this idea by monitoring positional memory before and after synaptic withdrawal caused by acute hibernation-like state (HLS). Animals lacking hippocampal PNNs due to enzymatic digestion by chondroitinase ABC or knockout of the PNN component aggrecan were compared with wild type controls. HLS-induced synapse withdrawal caused a memory deficit, but not to the level of naïve animals and not worsened by PNN attenuation. After HLS, animals lacking PNNs showed faster relearning. Absence of PNNs affected the restoration of inhibitory and excitatory synapses on PNN-bearing neurons. The results support a role for hippocampal PNNs in learning, but not in long-term memory storage.

Overview

Integrity signals

Registry

Crossref · 10.1101/2021.04.13.439599

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In the perirhinal cortex and hippocampus, ChABC digestion increases inhibitory inputs to PV interneurons.

    “In the perirhinal cortex and hippocampus, ChABC digestion increases inhibitory inputs to PV interneurons [43–45]”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [44]

  • Digestion of hippocampal PNNs with ChABC promotes re-learning of a once-trained Morris water maze task.

    “In contrast, digestion of hippocampal PNNs with ChABC promotes re-learning of a once-trained Morris water maze task (Ruzicka et al., 2021, unpublished results).”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as Ruzicka et al., 2021, unpublished results

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 83

  1. 10.1152/ajpregu.00117.2013 · DOI
  2. 10.1016/j.brainres.2016.07.020 · DOI
  3. 2017, RTN3 Is a Novel Cold-Induced Protein and Mediates Neuroprotective Effects of RBM3, Current biology: CB, 27, 638, 10.1016/j.cub.2017.01.047 · DOI
  4. 10.1155/2016/7931693 · DOI · Paper page
  5. 2020, NPY-Y1 receptor signaling controls spatial learning and perineuronal net expression, Neuropharmacology, 184, 108425
  6. 10.1523/JNEUROSCI.0394-12.2012 · DOI · Paper page
  7. 2019, Perineuronal nets in the lateral hypothalamus area regulate cue-induced reinstatement of cocaine-seeking behavior, Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology, 44, 850, 10.1038/s41386-018-0212-8 · DOI · Paper page
  8. 2017, Role of perineuronal nets in the anterior dorsal lateral hypothalamic area in the acquisition of cocaine-induced conditioned place preference and self-administration, Neuropharmacology, 118, 124, 10.1016/j.neuropharm.2017.03.018 · DOI · Paper page
  9. 10.1101/lm.134706 · DOI
  10. 10.1016/S0306-4522(01)00082-3 · DOI · Paper page
  11. 2018, Activation of adenosine A2A or A2B receptors causes hypothermia in mice, Neuropharmacology, 139, 268, 10.1016/j.neuropharm.2018.02.035 · DOI
  12. 2017, Hypothermia in mouse is caused by adenosine A1 and A3 receptor agonists and AMP via three distinct mechanisms, Neuropharmacology, 114, 101, 10.1016/j.neuropharm.2016.11.026 · DOI
  13. 10.1124/jpet.115.229872 · DOI
  14. 10.1523/JNEUROSCI.0245-16.2016 · DOI · Paper page
  15. 10.1093/brain/awq145 · DOI · Paper page
  16. Christensen, A.C. , K.K. Lensjo , M.E. lepperod , S.-A. Dragly , H. Sutterud , J.S. Blackstad , M. Fyhn , and T. Hafting . 2020. Perineuronal nets stabilize the grid cell network. BioRxiv. · DOI
  17. 10.1016/j.neuroscience.2018.07.004 · DOI
  18. 2020, Targeting chondroitinase ABC to axons enhances the ability of chondroitinase to promote neurite outgrowth and sprouting, PloS one, 15, e0221851, 10.1371/journal.pone.0221851 · DOI
  19. 10.1074/jbc.M600544200 · DOI · Paper page
  20. 10.1038/nature12866 · DOI · Paper page
  21. 2019, The potential of memory enhancement through modulation of perineuronal nets, Br J Pharmacol, 176, 3611, 10.1111/bph.14672 · DOI
  22. Fawcett, J.W. , T. Oohashi , and T. Pizzorusso . 2019. The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function. Nat Rev Neurosci. · DOI · Paper page
  23. 10.18632/aging.101256 · DOI · Paper page
  24. 10.1038/nn.2338 · DOI · Paper page
  25. 10.1126/science.1099901 · DOI · Paper page
  26. 10.1016/j.neuroscience.2010.08.032 · DOI · Paper page
  27. 10.1126/science.1174146 · DOI · Paper page
  28. 2019, Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses, Scientific reports, 9, 13939, 10.1038/s41598-019-50404-9 · DOI · Paper page
  29. 10.1073/pnas.1310272111 · DOI · Paper page
  30. 10.3389/fncel.2018.00149 · DOI · Paper page
  31. 10.1038/s41598-017-04007-x · DOI
  32. 10.1101/lm.030197.112 · DOI · Paper page
  33. Irvine, S.F. , and J.C.F. Kwok . 2018. Perineuronal Nets in Spinal Motoneurones: Chondroitin Sulphate Proteoglycan around Alpha Motoneurones. International journal of molecular sciences. 19. · DOI
  34. 10.1016/j.neuroscience.2013.02.014 · DOI
  35. 2014, Aging somatosensory cortex displays increased density of WFA-binding perineuronal nets associated with GAD-negative neurons, Neuroscience, 277, 734, 10.1016/j.neuroscience.2014.07.049 · DOI
  36. 2019, Adenosine A1 receptor-mediated protection of mouse hippocampal synaptic transmission against oxygen and/or glucose deprivation: a comparative study, Journal of neurophysiology, 122, 721, 10.1152/jn.00813.2018 · DOI
  37. 10.1126/science.280.5372.2121 · DOI · Paper page
  38. 10.1007/s12035-019-1526-1 · DOI · Paper page
  39. 10.1016/B978-0-444-63486-3.00008-6 · DOI
  40. 10.1152/jn.00098.2017 · DOI
  41. 10.1038/mp.2017.1 · DOI · Paper page
  42. Lensjo, K.K. , A.C. Christensen , S. Tennoe , M. Fyhn , and T. Hafting . 2017a. Differential Expression and Cell-Type Specificity of Perineuronal Nets in Hippocampus, Medial Entorhinal Cortex, and Visual Cortex Examined in the Rat and Mouse. eNeuro. 4. · DOI · Paper page
  43. 10.1523/JNEUROSCI.2504-16.2016 · DOI · Paper page
  44. 10.1111/j.1471-4159.2007.05066.x · DOI
  45. 2013, Perineuronal nets increase inhibitory GABAergic currents during the critical period in rats, International journal of ophthalmology, 6, 120
  46. 2020, Perineuronal net expression in the brain of a hibernating mammal, Brain Struct Funct, 225, 45, 10.1007/s00429-019-01983-w · DOI
  47. 2019, Perineuronal Net Formation during the Critical Period for Neuronal Maturation in the Hypothalamic Arcuate Nucleus, Nature metabolism, 1, 212, 10.1038/s42255-018-0029-0 · DOI
  48. 10.1155/2016/1305801 · DOI · Paper page
  49. 10.1016/j.biocel.2012.01.010 · DOI · Paper page
  50. 10.1098/rstb.2014.0046 · DOI · Paper page
  51. 10.1093/cercor/bhq017 · DOI · Paper page
  52. 10.1038/297681a0 · DOI · Paper page
  53. 2015, The effect of retrosplenial cortex lesions in rats on incidental and active spatial learning, Front Behav Neurosci, 9, 11
  54. 10.1016/0301-0082(79)90005-4 · DOI
  55. 2019, Space and Memory (Far) Beyond the Hippocampus: Many Subcortical Structures Also Support Cognitive Mapping and Mnemonic Processing, Front Neural Circuits, 13, 52, 10.3389/fncir.2019.00052 · DOI
  56. 10.1155/2016/9847696 · DOI
  57. 2015, Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala, Translational psychiatry, 5, e496, 10.1038/tp.2014.128 · DOI · Paper page
  58. 10.1038/nature14142 · DOI
  59. 10.1016/j.tins.2019.04.003 · DOI · Paper page
  60. 10.1523/JNEUROSCI.6267-11.2013 · DOI · Paper page
  61. 10.1038/s41593-019-0424-1 · DOI
  62. 10.1523/JNEUROSCI.1122-18.2018 · DOI · Paper page
  63. 2018, Neuroplasticity in stroke recovery. The role of microglia in engaging and modifying synapses and networks, The European journal of neuroscience, 47, 1414, 10.1111/ejn.13959 · DOI · Paper page
  64. 10.1111/jnc.12783 · DOI
  65. Shi, W. , X. Wei , X. Wang , S. Du , W. Liu , J. Song , and Y. Wang . 2019. Perineuronal nets protect long-term memory by limiting activity-dependent inhibition from parvalbumin interneurons. Proc Natl Acad Sci U S A. · DOI · Paper page
  66. 10.1523/JNEUROSCI.3592-14.2015 · DOI · Paper page
  67. Slaker, M.L. , E.T. Jorgensen , D.M. Hegarty , X. Liu , Y. Kong , F. Zhang , R.J. Linhardt , T.E. Brown , S.A. Aicher , and B.A. Sorg . 2018. Cocaine Exposure Modulates Perineuronal Nets and Synaptic Excitability of Fast-Spiking Interneurons in the Medial Prefrontal Cortex. eNeuro. 5. · DOI · Paper page
  68. 10.1016/j.neuroscience.2013.08.050 · DOI · Paper page
  69. 10.3389/fncel.2014.00244 · DOI · Paper page
  70. 10.1126/science.aat5397 · DOI
  71. Tanaka, K.Z. , and T.J. McHugh . 2018. The Hippocampal Engram as a Memory Index. J Exp Neurosci. 12:1179069518815942. · DOI
  72. 10.1016/j.semcdb.2018.09.011 · DOI
  73. 10.1073/pnas.1713530115 · DOI · Paper page
  74. 10.1073/pnas.1310158110 · DOI · Paper page
  75. 2019, Layer-specific expression of extracellular matrix molecules in the mouse somatosensory and piriform cortices, IBRO reports, 6, 1, 10.1016/j.ibror.2018.11.006 · DOI
  76. 10.1016/j.neuint.2017.11.001 · DOI · Paper page
  77. 2014, Reducing hippocampal extracellular matrix reverses early memory deficits in a mouse model of Alzheimer’s disease, Acta Neuropathol Commun, 2, 76
  78. 2018, The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders, Frontiers in molecular neuroscience, 11, 270, 10.3389/fnmol.2018.00270 · DOI · Paper page
  79. 10.3389/fncel.2015.00427 · DOI
  80. 2014, Interplay between intra-and interhemispheric remodeling of neural networks as a substrate of functional recovery after stroke: adaptive versus maladaptive reorganization, Neuroscience, 283, 178, 10.1016/j.neuroscience.2014.06.066 · DOI
  81. 10.1523/JNEUROSCI.5390-13.2014 · DOI · Paper page
  82. 10.1016/j.expneurol.2014.11.013 · DOI · Paper page
  83. 10.1016/j.neurobiolaging.2017.08.002 · DOI · Paper page

Cited by

Sorted by citations

Metadata

Authors
Ruzicka, J., Dalecka, M., Safrankova, K., Peretti, D., Mallucci, G., Jendelova, P., Kwok, J. C., & Fawcett, J. W.
Affiliations
  • Czech Academy of Sciences, Institute of Experimental Medicine (CZ)
  • University of Cambridge (GB)
  • University of Leeds (GB)
Venue
Translational Psychiatry
Publisher
openRxiv
Published
2021-04-14
Volume
12
Issue
1
Pages
480-480
ISSN
2158-3188 (ISSN-L)
OpenAlex
W4309438518
Cited by
27
References
1
Citations by year
2026: 5 · 2025: 8 · 2024: 10 · 2023: 2 · 2022: 2
FWCI
2.84
Type
journal article
Language
en
Open access
Locations
  • Translational Psychiatry (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • Apollo
  • Apollo (cc-by)
Funders
  • Epilepsy Research UK
  • Ministerstvo Školství, Mládeže a Tělovýchovy (LM2018129, Large RI Project LM2018129 Czech-BioImaging, LM2018129Czech-BioImaging, CZ.02., CZ.02.1.01/0.0./0.0/15_003/0000419, CZ.02.1.01/0.0/0.0/18_046/0016045, CZ.02.1.01/0.0/0.0/15_003, CZ.02.1.01, CZ.02.1.01/0.0, NEURORECON CZ.02.1.01/0.0/0.0/15_003/0000419)
  • Medical Research Council (WFL-UK-008-15, CZ.02.1.01/0.0/0.0/15_003/0000419, MR/R004463/1, 19-10365S, MR/V002694, MR/V002694/1)
  • European Regional Development Fund (02.1.01/0.0/0.0, CZ.02, CZ.02.1.01, CZ.02.1.01/0.0, LM2018129, CZ.02.1.01/0.0/0.0/18_046/0016045, CZ.02.1.01/0.0/0.0, /0.0/15_003/0000419)
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, hippocampus, place memory, memory extinction, anoxia, chondroitinase ABC, aggrecan, excitatory synapses, memory storage, learning
MeSH terms
Animals, Extracellular Matrix, Learning, Neurons, Synapses, Extracellular Matrix Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review