The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.
Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex
Open accessAbstract
Significance: The brain’s extracellular matrix (ECM) mediates structural stability by enwrapping synaptic contacts fundamental for long-term memory storage. Whether the ECM in the adult brain might thereby govern learning-related plasticity, lifelong memory reformation, and higher cognitive functions is largely unknown. Here, we enzymatically degraded the ECM in the auditory cortex of adult Mongolian gerbils during a reversal learning task. Such local weakening of the structurally rigid ECM specifically accelerated strategy changes required for reversal learning. It neither affected general sensory learning nor erased already established, learned memory traces. Thus, ECM modulation might promote the cognitive flexibility that can build on learned behaviors, and has further implications to develop new tools for guided neuroplasticity with therapeutic potential.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In adult mammalian life, auditory learning is limited, but cortex-dependent auditory relearning regains the agility of the juvenile state after ECM digestion [140] (Fig. 2F).”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [140]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“This treatment promotes neuronal plasticity in different neocortical regions, such as the visual (Pizzorusso et al., 2002) and auditory cortices (Happel et al., 2014).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Happel et al., 2014
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323
Balleine, B. W., & O'Doherty, J. P. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.131 · Cited by 1,775
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679
Recanzone, G., Schreiner, C., & Merzenich, M. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-01-00087.1993 · Cited by 1,266
A disinhibitory microcircuit for associative fear learning in the auditory cortex
Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., & Lüthi, A. (2011) · Nature · doi:10.1038/nature10674 · Cited by 840
Hyaluronidases: Their Genomics, Structures, and Mechanisms of Action
Stern, R., & Jedrzejas, M. J. (2006) · Chemical Reviews · doi:10.1021/cr050247k · Cited by 806
Perineuronal Nets Protect Fear Memories from Erasure
Gogolla, N., Caroni, P., Lüthi, A., & Herry, C. (2009) · Science · doi:10.1126/science.1174146 · Cited by 760
The Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644
Decision theory, reinforcement learning, and the brain
Dayan, P., & Daw, N. D. (2008) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.8.4.429 · Cited by 580
The dual role of the extracellular matrix in synaptic plasticity and homeostasis
Dityatev, A., Schachner, M., & Sonderegger, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2898 · Cited by 559
Flagged first, then by citations
Research works printed but not linked: 1
- 10.1037/0735-7044.107.1.82 · DOI
Cited by
Sorted by citations
Items 101–174 of 174
Longitudinal in vivo imaging of perineuronal nets
Benbenishty, A., Peled-Hajaj, S., Krishnaswamy, V. R., Har-Gil, H., Havusha-Laufer, S., Ruggiero, A., Slutsky, I., Blinder, P., & Sagi, I. (2023) · Neurophotonics · doi:10.1117/1.nph.10.1.015008 · Cited by 11
Unsupervised discovery of family specific vocal usage in the Mongolian gerbilPreprint
Peterson, R. E., Choudhri, A., Mitelut, C., Tanelus, A., Capo-Battaglia, A., Williams, A. H., Schneider, D. M., & Sanes, D. H. (2023) · eLife · doi:10.7554/elife.89892.3 · Cited by 17
Quraishe, S., Newman, T. A., & Anderson, L. A. (2019) · Journal of Neuroscience Research · doi:10.1002/jnr.24537 · Cited by 10
Aronitz, E. M., Kamermans, B. A., & Duffy, K. R. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25127 · Cited by 11
Senkov, O., Mironov, A. A., & Dityatev, A. E. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00425 · Cited by 10
Beebe, N. L., & Schofield, B. R. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24383 · Cited by 10
Liu, P., Zhao, Y., Xiong, W., Pan, Y., Zhu, M., & Zhu, X. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.12.024 · Cited by 10
Wingert, J. C., Anguiano, J. N., Ramos, J. D., Blacktop, J. M., Gonzalez, A. E., Churchill, L., & Sorg, B. A. (2023) · Addiction Biology · doi:10.1111/adb.13334 · Cited by 9
Shareh, H., & Sani, M. E. (2019) · Iranian Journal of Psychiatry and Clinical Psychology · doi:10.32598/ijpcp.24.4.384 · Cited by 15
A Continuum Mechanics Model of Enzyme-Based Tissue Degradation in Cancer Therapies
Deville, M., Roberto Natalini, D., & Poignard, C. (2018) · Bulletin of Mathematical Biology · doi:10.1007/s11538-018-0515-2 · Cited by 8
Mazi, A. R., Karakoç, Y., Demirtaş, C., Aykın, U., & Yıldırım, M. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04690-2 · Cited by 7
Blanco, I., Deasy, S., Amontree, M., Gabriel, M., Caccavano, A., Vicini, S., Glasgow, E. F., & Conant, K. E. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03007-y · Cited by 7
Rauch, A.-K., Roßkothen-Kuhl, N., & Illing, R. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.11.025 · Cited by 7
Extracellular matrix controls neuronal features that mediate the persistence of fear
Pignataro, A., Pagano, R., Guarneri, G., Middei, S., & Ammassari‐Teule, M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1440-0 · Cited by 7
Sakata, J. T., Alonge, K. M., Diethorn, E. J., Krishnan, K., Milman, N., Ramsaran, A. I., Wan, X., & Sorg, B. A. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1367-25.2025 · Cited by 8
Extracellular matrix remodelling in neurological diseases
Kwok, J. C. F., & Dityatev, A. E. (2026) · Nature Reviews Neurology · doi:10.1038/s41582-026-01209-8 · Cited by 9
Rupert, D. D., Pagliaro, A. H., Choe, J., & Shea, S. D. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0838-23.2023 · Cited by 7
Brunswick, C. A., Carpenter, C. M., Dennis, N. A., & Kwapis, J. L. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106195 · Cited by 10
Beebe, N. L., Noftz, W. A., & Schofield, B. R. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.24926 · Cited by 5
Perineuronal Nets: From Structure to Neurological Disorders
Li, X., Li, N., Zhao, P., Ren, D., Luo, B., & Zhou, T. G. (2023) · Current Medicinal Chemistry · doi:10.2174/0109298673258290231009111633 · Cited by 6
Impact of the extracellular matrix on plasticity in juvenile and adult brains
Frischknecht, R., & Happel, M. F. K. (2016) · e-Neuroforum · doi:10.1007/s13295-015-0021-z · Cited by 6
Self-citationTziridis, K., Maul, A., Rasheed, J., Krauß, P., Schilling, A., & Schulze, H. (2024) · BMC Neuroscience · doi:10.1186/s12868-024-00904-w · Cited by 6
Amoah, D. (2022) · Brain Science Advances · doi:10.26599/bsa.2022.9050023 · Cited by 7
Singh, J. B., Perelló‐Amorós, B., Schneeberg, J., Mirzapourdelavar, H., Seidenbecher, C. I., Fejtová, A., Dityatev, A. E., & Frischknecht, R. (2025) · EMBO Reports · doi:10.1038/s44319-025-00644-w · Cited by 8
Self-citationDoes age protect against loss of tonotopy after acute deafness in adulthood?
Roßkothen-Kuhl, N., Green, S., & Jakob, T. F. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1424773 · Cited by 4
Dynamics of perineuronal nets over amphibian metamorphosis
Edwards, J. A., Risch, M., & Hoke, K. L. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25055 · Cited by 4
Houlton, J., Zubkova, O. V., & Clarkson, A. N. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094817 · Cited by 4
Cornez, G., Langro, J., Cornil, C. A., Balthazart, J., & Lynch, K. S. (2019) · Journal of Experimental Biology · doi:10.1242/jeb.212910 · Cited by 4
Bicakci, A. O., Tsai, P.-L., Kahl, E., Mayer, D., & Fendt, M. (2021) · Pharmaceuticals · doi:10.3390/ph14070643 · Cited by 3
Learning induces unique transcriptional landscapes in the auditory cortex
Graham, G., Chimenti, M. S., Knudtson, K. L., Grenard, D. N., Co, L., Sumner, M., Tchou, T., & Bieszczad, K. M. (2023) · Hearing Research · doi:10.1016/j.heares.2023.108878 · Cited by 4
Schneider, I., Schönfeld, R., Hanert, A., Philippen, S., Tödt, I., Granert, O., Mehdorn, H. M., Becktepe, J. S., Deuschl, G., Berg, D., et al. (2024) · Brain Communications · doi:10.1093/braincomms/fcae068 · Cited by 3
Kozma, R., Hu, S., Sokolov, Y., Wanger, T., Schulz, A. L., Woldeit, M. L., Gonçalves, A. I., Ruszinkó, M., & Ohl, F. W. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.641684 · Cited by 3
Self-citationPerineuronal Nets in the Superior Olivary Complex
Morawski, M., & Sonntag, M. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190849061.013.12 · Cited by 3
Unsupervised discovery of family specific vocal usage in the Mongolian gerbilPreprint
Peterson, R. E., Choudhri, A., Mitelut, C., Tanelus, A., Capo-Battaglia, A., Williams, A. H., Schneider, D. M., & Sanes, D. H. (2023) · eLife · doi:10.7554/elife.89892.1 · Cited by 3
Grødem, S., Thompson, E. H., Røe, M. B., Vatne, G. H., Nymoen, I., Buccino, A. P., Madland, T., Hafting, T., Fyhn, M., & Lensjø, K. K. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.20.585910 · Cited by 3
Nik, A. H., Heidari, H., Davoodi, H., & Jafari, A. (2021) · Journal of Research in Behavioural Sciences · doi:10.52547/rbs.19.1.13 · Cited by 2
Baidoe‐Ansah, D., Carceller, H., Mirzapourdelavar, H., Pérez-Rando, M., Strackeljan, L., Garcia-Vazquez, B., Seidenbecher, C. I., Kaushik, R., Nácher, J., & Dityatev, A. E. (2026) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-026-01762-2 · Cited by 2
Linking meta-learning to meta-structure
Schilling, M., Ritter, H. J., & Ohl, F. W. (2024) · Behavioral and Brain Sciences · doi:10.1017/s0140525x24000232 · Cited by 2
Self-citationPerineuronal nets in motor circuitry regulate the performance of learned vocalizations in songbirds
Wan, X., Wang, A. S., Storch, D.-S., Li, V. Y., & Sakata, J. T. (2025) · Communications Biology · doi:10.1038/s42003-025-07520-2 · Cited by 2
Hussain, A., & Razak, K. A. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.05.026 · Cited by 4
Nguyen, H. D., Miyazaki, H., Kawai, H., Wang, Z., Sakamoto, S., Takaki, M., & Oohashi, T. (2025) · Neuroscience Research · doi:10.1016/j.neures.2025.104922 · Cited by 2
Hyaluronidases as Targets for the Treatment of Neurological Diseases
Sherman, L. S., Sorg, B. A., Matsumoto, S. G., Su, W., Banine, F., & Back, S. A. (2025) · Proteoglycan Research · doi:10.1002/pgr2.70036 · Cited by 2
Acosta, M. C., Warren, I. D., Wendy Saltzman, A., & Razak, K. A. (2025) · The Journal of Comparative Neurology · doi:10.1002/cne.70104 · Cited by 1
Cellular mechanisms regulating the timing of organizational effects of sex steroid hormones
Sakata, J. T., & Balthazart, J. (2026) · Hormones and Behavior · doi:10.1016/j.yhbeh.2026.105923 · Cited by 1
Викторович, С. С., & Kazantsev, V. (2026) · The European Physical Journal Special Topics · doi:10.1140/epjs/s11734-026-02530-5 · Cited by 1
gomroky, P., & Zanjani, F. A. (2021) · خانواده پژوهی · doi:10.52547/jfr.17.3.369 · Cited by 1
Tinnitus is associated with increased extracellular matrix density in the auditory cortexPreprint
Tziridis, K., Rasheed, J., Krauß, P., Schilling, A., & Schulze, H. (2023) · doi:10.22541/au.170020631.15815554/v1 · Cited by 1
Kravikass, M., Bischof, L., Karandasheva, K., Furlanetto, F., Dolai, P., Falk, S., Karow, M., Kobow, K., Fabry, B., & Zaburdaev, V. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.13.708543 · Cited by 1
Einfluss der Extrazellulären Matrix auf plastische Prozesse in jungen und alten Gehirnen
Frischknecht, R., & Happel, M. F. K. (2016) · e-Neuroforum · doi:10.1007/s12269-015-0033-1 · Cited by 1
Self-citationOn the Intimate Relationship between Man and Machine
Deliano, M. (2013) · Epistemology & Philosophy of Science · doi:10.5840/eps201337335
Self-citationEl‐Tabbal, M., Niekisch, H., Henschke, J. U., Budinger, E., Frischknecht, R., Deliano, M., & Happel, M. F. K. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.05.04.076224
Self-citationSchulte, D., Rosenmund, C., & Gundelfinger, E. D. (2020) · e-Neuroforum · doi:10.1515/nf-2020-0027
Cisneros-Franco, J. M., Thomas, M. E., Regragui, I., Lane, C. P., Ouellet, L., & de Villers‐Sidani, E. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.13.905257
Elucidating Memory Specificity by Exploring Parvalbumin Interneuron Modulation of Perineuronal Nets
Yeung, B.-R. A. (2020) · TSpace (University of Toronto)
Perineuronal nets in memory processing and behavior
Thompson, E. H. (2020) · NORA - Norwegian Open Research Archives
Potential involvement of perineuronal nets in brain aging
Yamada, J., & Jinno, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-817990-1.00015-9
فعالیة برنامج قائم على المرونة المعرفیة فی تحسیـن السلوك الاستكشافی البیئی لدى أطفال الروضة
جبر, ط. م. م. (2022) · المجلة المصرية للدراسات النفسية · doi:10.21608/ejcj.2022.247908
Salehi, H., Hoseinian, S., & Yazdi, S. M. (2022) · doi:10.61838/kman.aftj.3.3.6
Unsupervised discovery of family specific vocal usage in the Mongolian gerbilPreprint
Peterson, R. E., Choudhri, A., Mitelut, C., Tanelus, A., Capo-Battaglia, A., Williams, A. H., Schneider, D. M., & Sanes, D. H. (2024) · eLife · doi:10.7554/elife.89892.2
Activity-dependent extracellular proteolytic cascade remodels ECM to promote structural plasticityPreprint
Singh, J. B., Perelló‐Amorós, B., Schneeberg, J., Seidenbecher, C. I., Fejtová, A., Dityatev, A. E., & Frischknecht, R. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.28.620597
Self-citationZhang, H., Cicvaric, A., Bassett, T. E., Wood, E. M., Petrovic, Z., & Radulović, J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00066-3
Preface to the Special Issue “Matrix Metalloproteinases in Health and Disease”
Amontree, M., & Conant, K. E. (2025) · Journal of Neurochemistry · doi:10.1111/jnc.70032
Ahangar, M., Matinnia, N., & Yazdi‐Ravandi, S. (2025) · Annals of Military and Health Sciences Research · doi:10.5812/amh-157210
Berrouschot, V., Sonntag, M., Reimann, K., Jäger, C., Martin, S., Holzer, M., Stieler, J., & Morawski, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-14942-9
Hummel, K., Stefansson, L., Gilbert, K. F., Amontree, M., Ma, J., Pak, D. T. S., & Conant, K. E. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.12.675856
Acun, E., Zempeltzi, M. M., Deane, K. E., Deliano, M., Kannan, V., Ohl, F. W., & Happel, M. F. K. (2025) · Communications Biology · doi:10.1038/s42003-025-09336-6
Self-citationChen, J.-S., Wu, C.-C., Chen, H.-C., Cheng, Y., Hsu, C.-Y., Lin, K.-Y., Lin, P.-J., Kwan, A., & Hsieh, P. C. H. (2026) · Research Square · doi:10.21203/rs.3.rs-8574092/v1
Chondroitin 4-sulphate depletion enhances synaptic plasticity and memory in agingPreprint
Burianova, J. S., Svoboda, J., Růžička, J., Štěpánková, K., Klausová, T., Gmiterková, L., Spundova, T., Martínez-Varea, N., Králíková, M., Tureček, R., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.28.702127
Douceau, S. (2020) · theses.fr (ABES) · doi:10.70675/6f1007f2z8468z4365zb07dz7d863bf32cd5
Rôle des astrocytes dans la période critique de la plasticité visuelle
Breton, R. (2023) · theses.fr (ABES) · doi:10.70675/9140a00az6c88z4fb6zaabfz9eb16e7593ca
Winne, J., Schrader, R., Anfuson, M., & Caras, M. L. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2601801123
Extracellular matrix and perineuronal nets in neural plasticity, memory, and epileptogenesis
Zhu, H., Li, Q., Li, Y., & Wang, W. (2026) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2026.1945520
Metadata
- Authors
- Happel, M. F. K., Niekisch, H., Castiblanco Rivera, L. L., Ohl, F. W., Deliano, M., & Frischknecht, R.
- Affiliations
- Otto-von-Guericke-Universität Magdeburg (DE)
- Department of Systems Physiology of Learning and
- Center for Behavioral Brain Sciences (DE)
- Leibniz Institute for Neurobiology (DE)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-02-03
- Volume
- 111
- Issue
- 7
- Pages
- 2800-2805
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3932855
- OpenAlex
- W2074133215
- Cited by
- 176
- References
- 47
- Citations by year
- 2026: 9 · 2025: 18 · 2024: 11 · 2023: 11 · 2022: 13 · 2021: 15 · 2020: 22 · 2019: 12 · 2018: 14 · 2017: 18 · 2016: 12 · 2015: 10 · 2014: 10
- FWCI
- 9.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Leibniz-Gemeinschaft
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- extracellular matrix, auditory cortex, cognitive flexibility, reversal learning, synaptic plasticity, neuroplasticity, Mongolian gerbil
- MeSH terms
- Acoustic Stimulation, Analysis of Variance, Animals, Auditory Cortex, Cognition, Discrimination Learning, Extracellular Matrix, Fluorescence, Gerbillinae, Immunohistochemistry, Male, Neuronal Plasticity, Reversal Learning, Memory, Long-Term
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
