Age-dependent and region-specific alteration of parvalbumin neurons and perineuronal nets in the mouse cerebral cortex
Abstract
Cognitive function declines with age. Such function depends on γ-oscillation in the frontal cortex. Pyramidal neurons, and the parvalbumin-expressing interneurons (PV neurons) that control them, are important for the generation of γ-oscillation. The mechanism by which cognitive function declines is unclear. Perineuronal nets (PNNs) mainly surround the soma and proximal dendrites and axon segments of PV neurons in the cerebral cortex. Previous evidence indicates that PNNs inhibit neural plasticity. If this is true, an increase in the number of neurons surrounded by PNNs or in the thickness or density of the PNNs around neurons could decrease plasticity in the cortex. To determine if an aging-related change in cortical PNNs occurs, we examined the influence of aging on PV neurons and whether Wisteria floribunda agglutinin-positive PNNs differ depending on the cortical area. The results showed that the number of PV neurons/mm 2 did not change in many areas of the cortex as mice aged. In contrast, the number of neurons in the sensory cortex surrounded by PNNs increased as mice aged. Thus, with age, PNN density increases in some cortical areas but not in others. In addition, the expression level of PV protein in PV neurons decreased with aging in the whole cortex. We suggest that decreased expression of PV protein impairs fast spiking in PV neurons. We propose that PNNs surround more neurons as age increases. This aging-related increase in PNNs decreases plasticity in the cerebral cortex and reduces cognitive function. The first step in investigating this proposal would be to determine if PNN density increases with age.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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 appearance of PNNs coincides with the maturation of PV1 cells and the decrease of plasticity levels in neocortical regions, hippocampus, and amygdala.
“Although critical periods are specific for different systems and have a different time lines, the appearance of PNNs coincides with the maturation of PV1 cells and the decrease of plasticity levels, not only in neocortical regions (Pizzorusso et al., 2002;Ueno et al., 2018), but also in the hippocampus (Bukalo et al., 2001) and the amygdala (Gogolla et al., 2009).”
From Perineuronal Nets Regulate the Inhibitory Perisomatic Input onto Parvalbumin Interneurons and γ Activity in the Prefrontal Cortex (2020) · cites this paper as Ueno et al., 2018
Cites
Neuropathological alterations in Alzheimer disease
Serrano-Pozo, A., Frosch, M. P., Masliah, E., & Hyman, B. T. (2011) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006189 · Cited by 3,345 · see citing works
Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders
Zlokovic, B. V. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3114 · Cited by 2,969 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Parvalbumin neurons and gamma rhythms enhance cortical circuit performance
Sohal, V. S., Zhang, F., Yizhar, O., & Deisseroth, K. (2009) · Nature · doi:10.1038/nature07991 · Cited by 2,606 · see citing works
NeuN, a neuronal specific nuclear protein in vertebratesxs
Mullen, R. J., Buck, C. R., & Smith, A. M. (1992) · Development · doi:10.1242/dev.116.1.201 · Cited by 2,351 · see citing works
Cortical inhibitory neurons and schizophrenia
Lewis, D. A., Hashimoto, T., & Volk, D. W. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1648 · Cited by 2,297 · see citing works
Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks
Bartos, M., Vida, I., & Jonas, P. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2044 · Cited by 2,070 · see citing works
Alzheimer Mechanisms and Therapeutic Strategies
Huang, Y., & Mucke, L. (2012) · Cell · doi:10.1016/j.cell.2012.02.040 · Cited by 1,758 · see citing works
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 · see citing works
Neural plasticity in the ageing brain
Burke, S. N., & Barnes, C. A. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1809 · Cited by 1,600 · see citing works
Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420 · see citing works
Calcium-binding proteins in the nervous system
Baimbridge, K. G., Celio, M. R., & ROGERS, J. H. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90081-i · Cited by 1,336 · see citing works
Paxinos and Franklin's the Mouse Brain in Stereotaxic Coordinates
Paxinos, G., & Franklin, K. B. J. (2012) · Cited by 1,267 · see citing works
Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., Maffei, L., & Tonegawa, S. (1999) · Cell · doi:10.1016/s0092-8674(00)81509-3 · Cited by 1,198 · see citing works
Kaufman, D. L., Houser, C. R., & Tobin, A. J. (1991) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1991.tb08211.x · Cited by 789 · see citing works
Hippocampus and entorhinal cortex in mild cognitive impairment and early AD
Pennanen, C., Kivipelto, M., Tuomainen, S., Hartikainen, P. H., Hänninen, T., Laakso, M. P., Hallikainen, M., Vanhanen, M., Nissinen, A. M., Helkala, E., et al. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00084-8 · Cited by 646 · see citing works
Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins
Bandtlow, C. E., & Zimmermann, D. R. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.4.1267 · Cited by 632 · see citing works
Extracellular matrix molecules and synaptic plasticity
Dityatev, A., & Schachner, M. (2003) · Nature Reviews Neuroscience · doi:10.1038/nrn1115 · Cited by 564 · see citing works
Age-related changes in behavior in C57BL/6J mice from young adulthood to middle age
Shoji, H., Takao, K., Hattori, S., & Miyakawa, T. (2016) · Molecular Brain · doi:10.1186/s13041-016-0191-9 · Cited by 452 · see citing works
Self-citationThe perineuronal net and the control of CNS plasticity
Wang, D., & Fawcett, J. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1375-y · Cited by 373 · see citing works
Calcium buffering properties of calbindin D28k and parvalbumin in rat sensory neurones.
Chard, P. S., Bleakman, D., Christakos, S., Fullmer, C. S., & Miller, R. J. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019950 · Cited by 346 · see citing works
The role of the prefrontal cortex in higher cognitive functions
Frith, C., & Dolan, R. (1996) · Cognitive Brain Research · doi:10.1016/s0926-6410(96)00054-7 · Cited by 343 · see citing works
Evidence that Alzheimer’s disease is a microvascular disorder: the role of constitutive nitric oxide
de la Torre, J. C., & Stefano, G. B. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00043-6 · Cited by 307 · see citing works
Calcium homeostasis and modulation of synaptic plasticity in the aged brain
Foster, T. C. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00283.x · Cited by 303 · see citing works
Developmental and cell type‐specific expression of the neuronal marker NeuN in the murine cerebellum
Weyer, A., & Schilling, K. (2003) · Journal of Neuroscience Research · doi:10.1002/jnr.10655 · Cited by 266 · see citing works
The exercise-induced expression of BDNF within the hippocampus varies across life-span
Adlard, P. A., Perreau, V. M., & Cotman, C. W. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.05.006 · Cited by 260 · see citing works
Freeman, S. H., Kandel, R., Cruz, L., Rozkalne, A., Newell, K. L., Frosch, M. P., Hedley‐Whyte, E. T., Locascio, J. J., Lipsitz, L. A., & Hyman, B. T. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31818fc72f · Cited by 212 · see citing works
Age-Dependent Ocular Dominance Plasticity in Adult Mice
Lehmann, K., & Löwel, S. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003120 · Cited by 175 · see citing works
Kleschevnikov, A. M., Belichenko, P. V., Faizi, M., Jacobs, L. F., Htun, K. E., Shamloo, M., & Mobley, W. C. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1673-12.2012 · Cited by 174 · see citing works
Successful brain aging: plasticity, environmental enrichment, and lifestyle
Mora, F. (2013) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2013.15.1/fmora · Cited by 172 · see citing works
Patz, S. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhg132 · Cited by 170 · see citing works
Murray, A., Wołoszynowska-Fraser, M. U., Ansel-Bollepalli, L., Marshall-Phelps, K. L., Foggetti, A., Crouch, B., Riedel, G., & Wulff, P. (2015) · Scientific Reports · doi:10.1038/srep16778 · Cited by 165 · see citing works
Downregulation of Parvalbumin at Cortical GABA Synapses Reduces Network Gamma Oscillatory Activity
Volman, V., Behrens, M. M., & Sejnowski, T. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3041-11.2011 · Cited by 164 · see citing works
Do, K. Q., Cuenod, M., & Hensch, T. K. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv065 · Cited by 158 · see citing works
Morawski, M., Brückner, G., Jäger, C., Seeger, G., & Arendt, T. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.022 · Cited by 156 · see citing works
Berretta, S., Pantazopoulos, H., Markota, M., Brown, C., & Batzianouli, E. T. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2014.12.040 · Cited by 152 · see citing works
Lewis, D. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08156.x · Cited by 142 · see citing works
Chang, Y. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh144 · Cited by 139 · see citing works
Rapp, P., Deroche, P. S., Mao, Y., & Burwell, R. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.11.1171 · Cited by 131 · see citing works
BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events
Gooney, M., Messaoudi, E., Maher, F. O., Bramham, C. R., & Lynch, M. A. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.01.003 · Cited by 124 · see citing works
Distinct Firing Patterns of Neuronal Subtypes in Cortical Synchronized Activities
Kawaguchi, Y. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07261.2001 · Cited by 123 · see citing works
Protective Properties of Neural Extracellular Matrix
Suttkus, A., Morawski, M., & Arendt, T. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8990-4 · Cited by 108 · see citing works
F-actin marks the rhizoid pole in living Pelvetia compressa zygotes
Alessa, L., & Kropf, D. L. (1999) · Development · doi:10.1242/dev.126.1.201 · Cited by 90 · see citing works
GABA through the Ages: Regulation of Cortical Function and Plasticity by Inhibitory Interneurons
Lehmann, K., Steinecke, A., & Bolz, J. (2012) · Neural Plasticity · doi:10.1155/2012/892784 · Cited by 89 · see citing works
ECM in brain aging and dementia
Morawski, M., Filippov, M., Tzinia, A., Tsilibary, E., & Vargova, L. (2014) · Progress in Brain Research · doi:10.1016/b978-0-444-63486-3.00010-4 · Cited by 84 · see citing works
Dysfunction of Mouse Cerebral Arteries during Early Aging
Balbi, M., Ghosh, M., Longden, T. A., Vega, M. J., Gesierich, B. G., Hellal, F., Lourbopoulos, A. I., Nelson, M. T., & Plesnila, N. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.107 · Cited by 83 · see citing works
Zheng, K., An, J. J., Yang, F., Xu, W., Xu, Q., Wu, J., Hökfelt, T. G. M., Fisahn, A., Xu, B., & Lu, B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114241108 · Cited by 82 · see citing works
Experience-Dependent Intrinsic Plasticity in Interneurons of Barrel Cortex Layer IV
Sun, Q. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00562.2009 · Cited by 70 · see citing works
The Role of the Human Entorhinal Cortex in a Representational Account of Memory
Schultz, H., Sommer, T., & Peters, J. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00628 · Cited by 70 · see citing works
Early Cortical Changes in Gamma Oscillations in Alzheimer’s Disease
Klein, A. S., Donoso, J. R., Kempter, R., Schmitz, D., & Beed, P. S. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00083 · Cited by 63 · see citing works
Farajnia, S., Meijer, J. H., & Michel, S. H. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.12.040 · Cited by 60 · see citing works
Modulating excitation through plasticity at inhibitory synapses
Chevaleyre, V., & Piskorowski, R. A. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00093 · Cited by 58 · see citing works
Distinguishing adaptive plasticity from vulnerability in the aging hippocampus
Gray, D. T., & Barnes, C. A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.001 · Cited by 57 · see citing works
Okamoto, M., Mori, S., Ichimura, M., & Endô, H. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90660-2 · Cited by 52 · see citing works
Self-citationLoss of MeCP2 disrupts cell autonomous and autocrine BDNF signaling in mouse glutamatergic neurons
Sampathkumar, C., Wu, Y.-J., Vadhvani, M., Trimbuch, T., Eickholt, B. J., & Rosenmund, C. (2016) · eLife · doi:10.7554/elife.19374 · Cited by 51 · see citing works
Jessen, S. B., Mathiesen, C., Lind, B. L., & Lauritzen, M. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv261 · Cited by 48 · see citing works
Karetko-Sysa, M., Skangiel-Kramska, J., & Nowicka, D. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.05.022 · Cited by 45 · see citing works
Lekic, P., Rubbino, I., Krasnoshtein, F., Cheifetz, S., McCulloch, C. A., & Tenenbaum, H. C. (1997) · The Anatomical Record · doi:10.1002/(sici)1097-0185(199703)247:3 · Cited by 42 · see citing works
Rietveld, L., Stuss, D. P., McPhee, D., & Delaney, K. R. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00145 · Cited by 39 · see citing works
Karetko, M., Skangiel-Kramska, J., & Nowicka, D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.049 · Cited by 37 · see citing works
Young, N. M., & Williams, R. E. (1985) · Canadian Journal of Biochemistry and Cell Biology · doi:10.1139/o85-039 · Cited by 28 · see citing works
Lu, C. B., Vreugdenhil, M., & Toescu, E. C. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.01.001 · Cited by 18 · see citing works
Takahashi, T., Emson, P. C., & Arai, H. (2002) · Psychogeriatrics · doi:10.1111/j.1479-8301.2002.tb00030.x · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders
Wen, T. H., Binder, D. K., Ethell, I. M., & Razak, K. A. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00270 · Cited by 170 · see citing works
Carceller, H., Guirado, R., Ripolles-Campos, E., Teruel-Marti, V., & Nacher, J. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.0291-20.2020 · Cited by 112 · see citing works
An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity
Carulli, D., & Verhaagen, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052434 · Cited by 123 · see citing works
The aging mouse brain: cognition, connectivity and calcium
Radulescu, C. I., Cerar, V., Haslehurst, P., Kopanitsa, M. V., & Barnes, S. J. (2021) · Cell Calcium · doi:10.1016/j.ceca.2021.102358 · Cited by 105 · see citing works
Regulation of thyroid-disrupting chemicals to protect the developing brain
Gilbert, M. E., O’Shaughnessy, K. L., & Axelstad, M. (2020) · Endocrinology · doi:10.1210/endocr/bqaa106 · Cited by 83 · see citing works
Regulation of Perineuronal Nets in the Adult Cortex by the Activity of the Cortical Network
Devienne, G. F., Picaud, S., Cohen, I., Piquet, J., Tricoire, L., Testa, D., Nardo, A. A. D., Rossier, J., Cauli, B., & Lambolez, B. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0434-21.2021 · Cited by 78 · see citing works
Perineuronal Nets: Subtle Structures with Large Implications
Carceller, H., Gramuntell, Y., Klimczak, P., & Nácher, J. (2022) · The Neuroscientist · doi:10.1177/10738584221106346 · Cited by 48 · see citing works
Kumar, P., Goettemoeller, A. M., Espinosa‐García, C., Tobin, B. R., Tfaily, A., Nelson, R. S., Natu, A., Dammer, E. B., Santiago, J. V., Malepati, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-47028-7 · Cited by 48 · see citing works
Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats
Griffiths, B. B., Madden, A. M. K., Edwards, K. A., Zup, S. L., & Stary, C. M. (2019) · Brain and Behavior · doi:10.1002/brb3.1265 · Cited by 39 · see citing works
Calcium-activated potassium channels: implications for aging and age-related neurodegeneration
Trombetta-Lima, M., Krabbendam, I. E., & Dolga, A. M. (2020) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2020.105748 · Cited by 39 · see citing works
Santos‐Silva, T., Colodete, D. A. E., Lisboa, J. R., Freitas, I. D. S., Lopes, C. F. B., Hadera, V., Lima, T. S. A., Souza, A. J., & Gomes, F. V. (2024) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13994 · Cited by 36 · see citing works
Minocycline Treatment Reverses Sound Evoked EEG Abnormalities in a Mouse Model of Fragile X Syndrome
Lovelace, J. W., Ethell, I. M., Binder, D. K., & Razak, K. A. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00771 · Cited by 36 · see citing works
Reinhard, S. M., Rais, M., Afroz, S., Hanania, Y., Pendi, K., Espinoza, K., Rosenthal, R., Binder, D. K., Ethell, I. M., & Razak, K. A. (2019) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2019.107042 · Cited by 33 · see citing works
Age-Related Central Gain with Degraded Neural Synchrony in the Auditory Brainstem of Mice and Humans
Rumschlag, J. A., McClaskey, C. M., Dias, J. W., Kerouac, L. B., Noble, K. V., Panganiban, C. H., Lang, H., & Harris, K. C. (2022) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2022.03.014 · Cited by 33 · see citing works
The Role of Perineuronal Nets in Physiology and Disease: Insights from Recent Studies
Auer, S., Schicht, M., Hoffmann, L., Budday, S., Frischknecht, R., Blümcke, I., & Paulsen, F. P. (2025) · Cells · doi:10.3390/cells14050321 · Cited by 30 · see citing works
Bucher, E., Collins, J. M., King, A. E., Vickers, J. C., & Kirkcaldie, M. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02327-3 · Cited by 29 · see citing works
Sugitani, K., Egorova, D., Mizumoto, S., Nishio, S., Yamada, S., Kitagawa, H., Oshima, K., Nadano, D., Matsuda, T., & Miyata, S. (2021) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2020.129804 · Cited by 28 · see citing works
Klimczak, P., Rizzo, A., Castillo-Gómez, E., Pérez-Rando, M., Gramuntell, Y., Beltrán, M. A. C. S., & Nácher, J. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.733989 · Cited by 29 · see citing works
Perineuronal nets affect memory and learning after synapse withdrawal
Růžička, J., Dalecká, M., Safrankova, K., Peretti, D., Mallucci, G. R., Jendelová, P., Kwok, J. C. F., & Fawcett, J. W. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02226-z · Cited by 27 · see citing works
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2018) · IBRO Reports · doi:10.1016/j.ibror.2018.11.006 · Cited by 26 · see citing works
Self-citationMafi, A. M., Hofer, L. N., Russ, M. G., Young, J. W., & Mellott, J. G. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00027 · Cited by 25 · see citing works
Pinna, A., & Colasanti, A. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.689473 · Cited by 26 · see citing works
Lau, B. Y. B., Layo-Carris, D. E., Emery, B. A., Everett, M., Kumar, A., Stevenson, P. K., Reynolds, K. G., Cherosky, A., Bowyer, S.-A. H., Roth, S., et al. (2020) · eNeuro · doi:10.1523/eneuro.0500-19.2020 · Cited by 24 · see citing works
How do neurons age? A focused review on the aging of the microtubular cytoskeleton
Richardson, B., Goedert, T., Quraishe, S., Deinhardt, K., & Mudher, A. K. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.390974 · Cited by 24 · see citing works
Lehner, A., Hoffmann, L., Rampp, S., Coras, R., Paulsen, F. P., Frischknecht, R., Hamer, H. M., Walther, K., Brandner, S., Hofer, W., et al. (2024) · Epilepsia Open · doi:10.1002/epi4.12963 · Cited by 21 · see citing works
Adolescent Parvalbumin Expression in the Left Orbitofrontal Cortex Shapes Sociability in Female Mice
Jeon, Y.-S., Jeong, D., Kweon, H., Kim, J., Kim, C. Y., Oh, Y., Lee, Y.-H., Kim, C. H., Kim, S., Jeong, J., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0918-22.2023 · Cited by 22 · see citing works
Gattoni, G., & Bernocchi, G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092364 · Cited by 20 · see citing works
Gray, D. T., Khattab, S., Meltzer, J., McDermott, K., Schwyhart, R., Sinakevitch, I. G., Härtig, W., & Barnes, C. A. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac366 · Cited by 16 · see citing works
Szegedi, V., Tiszlavicz, Á., Furdan, S., Douida, A., Bakos, E., Barzó, P., Tamás, G., Szűcs, A. L., & Lamsa, K. P. (2024) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2024.04.020 · Cited by 18 · see citing works
Ueno, H., Fujii, K., Takao, K., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2019) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.12.008 · Cited by 18 · see citing works
Self-citationRogalla, M. M., & Hildebrandt, K. J. (2020) · eNeuro · doi:10.1523/eneuro.0511-19.2020 · Cited by 18 · see citing works
Reinhard, S. M., Abundez-Toledo, M., Espinoza, K., & Razak, K. A. (2019) · Hearing Research · doi:10.1016/j.heares.2019.107781 · Cited by 15 · see citing works
Mafi, A. M., Russ, M. G., Hofer, L. N., Pham, V. Q., Young, J. W., & Mellott, J. G. (2021) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2021.04.001 · Cited by 14 · see citing works
Trnski, S., Nikolić, B., Ilić, K., Drlje, M., Bobić‐Rasonja, M., Darmopil, S., Petanjek, Z., Hranilović, D., & Milošević, N. J. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.810980 · Cited by 15 · see citing works
Dynamic regulation of the extracellular matrix in reward memory processes: a question of time
Valeri, J., Gisabella, B., & Pantazopoulos, H. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1208974 · Cited by 13 · see citing works
Perineuronal nets: Role in normal brain physiology and aging, and pathology of various diseases
Zhu, K., Fu, Y., Zhao, Y., Niu, B., & Han, L. (2025) · Ageing Research Reviews · doi:10.1016/j.arr.2025.102756 · Cited by 16 · see citing works
Morphett, J., Whittaker, A. L., Reichelt, A. C., & Hutchinson, M. R. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105568 · Cited by 12 · see citing works
Editorial: Perineuronal Nets as Therapeutic Targets for the Treatment of Neuropsychiatric Disorders
Browne, C. A., Conant, K. E., Lasek, A. W., & Nácher, J. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2022.889800 · Cited by 12 · see citing works
Wang, W., Deng, D., Jenkins, K., Zinsmaier, A. K., Zhou, Q., & Bao, S. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.12.006 · Cited by 10 · see citing works
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 · see citing works
Devienne, G. F., Picaud, S., Cohen, I., Piquet, J., Tricoire, L., Testa, D., Nardo, A. A. D., Rossier, J., Cauli, B., & Lambolez, B. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/671719 · Cited by 11 · see citing works
Perineuronal nets in the developing brain: implications for neurodevelopmental disorders
Ackerman, J. M., Ford, T. J. L., Kattewar, S. S., & Kim, W.-Y. (2025) · Molecular Brain · doi:10.1186/s13041-025-01261-3 · Cited by 10 · see citing works
Ueno, H., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2019) · International Journal of Radiation Biology · doi:10.1080/09553002.2019.1564081 · Cited by 9 · see citing works
Self-citationTargeting CA2 Perineuronal Nets Restores Recognition Memory and Theta Oscillations in Aged Mice
Mehak, S. F., Shivakumar, A. B., Jijimon, F., Gupta, A., Pillai, V. G., & Gangadharan, G. (2025) · Aging Cell · doi:10.1111/acel.70139 · Cited by 6 · see citing works
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 6 · see citing works
Dang, T. N., Tien, S. N., Ochi, R., Le, D. T., Nishio, K., Kuwamura, H., Kurose, T., Fujita, N., Nishijo, H., Nakamura, Y., et al. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114786 · Cited by 6 · see citing works
Gallo, M. T., Virenque, A., Golinelli, A., Fumagalli, F., Ċastrén, E., Brivio, P., & Calabrese, F. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03223-6 · Cited by 5 · see citing works
Towner, T. T., Coleman, H. J., Goyden, M. A., Vore, A. S., Papastrat, K. M., Varlinskaya, E. I., & Werner, D. F. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.110195 · Cited by 6 · see citing works
Regulation of CNS Plasticity Through the Extracellular Matrix
Warren, P. M., Dickens, S., Gigout, S., Fawcett, J. W., & Kwok, J. C. F. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190635374.013.11 · Cited by 5 · see citing works
Extracellular matrix and microglial regulation of cognitive agingPreprint
Gray, D. T., Gutierrez, A., Jami‐Alahmadi, Y., Pandey, V., Pan, L., Zhang, Y., Wohlschlegel, J. A., McDevitt, R. A., & Biase, L. M. D. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.04.574215 · Cited by 5 · see citing works
Midbrain extracellular matrix and microglia are associated with cognition in aging mice
Gray, D. T., Gutierrez, A., Jami‐Alahmadi, Y., Pandey, V., Pan, L., Zhang, Y., Wohlschlegel, J. A., McDevitt, R. A., & Biase, L. M. D. (2025) · Nature Communications · doi:10.1038/s41467-025-66434-z · Cited by 4 · see citing works
Schob, S., Puchta, J., Winter, K., Michalski, D., Mages, B., Martens, H., Emmer, A., Hoffmann, K., Gaunitz, F., Meinicke, A., et al. (2021) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2021.102036 · Cited by 4 · see citing works
Kumar, P., Goettemoeller, A. M., Espinosa‐García, C., Tobin, B. R., Tfaily, A., Nelson, R. S., Natu, A., Dammer, E. B., Santiago, J. V., Malepati, S., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.17.541038 · Cited by 4 · see citing works
Perineuronal Nets: Old Structures, New Functions
Tewari, B. P., Chaunsali, L., & Sontheimer, H. W. (2026) · The Neuroscientist · doi:10.1177/10738584261421180 · Cited by 3 · see citing works
García-Cerro, S., Gómez-Garrido, A., Soria, F. N., Loucera, C., & Crespo‐Facorro, B. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02210-3 · Cited by 3 · see citing works
Fingolimod increases parvalbumin-positive neurons in adult mice
Ueno, H., Takahashi, Y., Murakami, S., Wani, K., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2022) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2022.06.005 · Cited by 3 · see citing works
Self-citationAlmassri, L. S., Ohl, A. P., Iafrate, M. C., Wade, A. D., Tokar, N. J., Mafi, A. M., Beebe, N. L., Young, J. W., & Mellott, J. G. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1271008 · Cited by 3 · see citing works
Descriptive study of perineuronal net in enteric nervous system of humans and mice
da Silva, M. D. V., Bacarin, C. C., Machado, C. C. A., Franciosi, A., Mendes, J. D. D. L., Watanabe, P. D. S., Miqueloto, C. A., Fattori, V., Albarracin, O. Y. E., Verri, W. A., Jr., et al. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16159 · Cited by 3 · see citing works
Eisele, B. S., Wu, A. J., Luka, Z., Hale, A. T., & York, J. D. (2021) · Advances in Biological Regulation · doi:10.1016/j.jbior.2021.100858 · Cited by 3 · see citing works
Mukhtar, S., Kataria, S., Cimaglia, G., & Beccano-Kelly, D. A. (2025) · Current Research in Physiology · doi:10.1016/j.crphys.2025.100166 · Cited by 2 · see citing works
Schamber, P., Darbhamulla, S., Boyer, M., Pelletier, M., Hartman, H., Friedman, O., Zhang, S., Blais, A. Y., Oh, S., Zhong, H., et al. (2026) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1014571 · Cited by 2 · see citing works
Emery, B. A., Everett, M., Dunn, L. R., Lau, B. Y. B., & Krishnan, K. (2026) · Frontiers in Neuroscience · doi:10.3389/fnins.2026.1769195 · Cited by 2 · see citing works
Parvalbumin interneurons under stress: converging mechanisms of vulnerability
Santos‐Silva, T., Godoy, L. D., Guimarães, F. S., & Gomes, F. V. (2026) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyag043 · Cited by 1 · see citing works
Szabó, F., Sigutova, V., Schneider, A. M., Hoerder‐Suabedissen, A., & Molnár, Z. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.06.592829 · Cited by 1 · see citing works
Schwyhart, R. (2020) · UA Campus Repository (The University of Arizona)
Schob, S., Puchta, J., Winter, K., Michalski, D., Mages, B., Martens, H., Emmer, A., Hoffmann, K., Gaunitz, F., Meinicke, A., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-747032/v1
Szabó, F., Sigutova, V., Schneider, A. M., Hoerder‐Suabedissen, A., & Molnár, Z. (2024) · Journal of Anatomy · doi:10.1111/joa.14181 · Cited by 1 · see citing works
Sun, T., Li, Q., Liu, B., Chen, J., Li, A., Jiang, T., Gong, H., & Li, X. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26135934
Radulović, J., Zhang, H., Petrovic, Z., Wood, E. M., Cicvaric, A., Krispil-Alon, M., Jovasevic, V., Parker, K., Bassett, T. E., Carboncino, A., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-6864379/v1
Devienne, G. F. (2019) · theses.fr (ABES) · doi:10.70675/453418efzc908z49e0zba6fz71fefaa50691
Bhuiyan, M. H., Smith, M. J., Hinkley, S. F. R., & Clarkson, A. N. (2026) · Neuroprotection/Neuroprotection (Chichester, England. Print) · doi:10.1002/nep3.70043
Zhang, H., Petrovic, Z., Wood, E. M., Cicvaric, A., Krispil-Alon, M., Jovasevic, V., Parker, K., Bassett, T. E., Carboncino, A., Guedea, A. L., et al. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003908
Belz, L., Aouci, R., Allain, B., Henderson, F., Fontaine, A., Desgagne, P., Calzaroni, L., Fabre, V., Pardi, M. B., Levi, G., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.07.23.740286
Jenike, A. E., Brown, T. E., Impey, S., Sorg, B. A., & Aicher, S. A. (2026) · Brain Research · doi:10.1016/j.brainres.2026.150507
Chronic nicotine reverses age-related decline of interneuron markers in mouse auditory cortex
Intskirveli, I., Lazar, R., Hidalgo, D., & Metherate, R. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1876409
Wei, X., Módy, I., Wu, Y., Gajjar, A., Singh, G., Neerathalingam, V., Sun, A., Huang, R., Holley, S. M., & Lu, D. (2026) · Current Issues in Molecular Biology · doi:10.3390/cimb48100978
- Authors
- Ueno, H., Takao, K., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Okamoto, M., Aoki, S., & Ishihara, T.
- Affiliations
- Okayama University (JP)
- University of Toyama (JP)
- Kawasaki Medical School (JP)
- Corresponding author
- Ueno, Hiroshi
- Venue
- Neurochemistry International
- Publisher
- Elsevier BV
- Published
- 2018-01
- Volume
- 112
- Pages
- 59-70
- ISSN
- 0197-0186 (ISSN-L)
- OpenAlex
- W2767601667
- Cited by
- 72
- References
- 63
- Citations by year
- 2026: 10 · 2025: 11 · 2024: 9 · 2023: 6 · 2022: 7 · 2021: 10 · 2020: 9 · 2019: 7 · 2018: 3
- FWCI
- 2.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurochemistry International (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ryobi Teien Memory Foundation
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- parvalbumin neurons, perineuronal nets, brain aging, gamma oscillations, fast spiking, cortical interneurons, neuroplasticity, cognitive decline, sensory cortex, Wisteria floribunda agglutinin, mouse cortex
- MeSH terms
- Age Factors, Aging, Animals, Cerebral Cortex, Male, Mice, Inbred C57BL, Nerve Net, Neurons, Parvalbumins, Peripheral Nerves, Mice
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
