Modulation of Perineuronal Nets and Parvalbumin with Developmental Song Learning
Open accessAbstract
Neural circuits and behavior are shaped during developmental phases of maximal plasticity known as sensitive or critical periods. Neural correlates of sensory critical periods have been identified, but their roles remain unclear. Factors that define critical periods in sensorimotor circuits and behavior are not known. Birdsong learning in the zebra finch occurs during a sensitive period similar to that for human speech. We now show that perineuronal nets, which correlate with sensory critical periods, surround parvalbumin-positive neurons in brain areas that are dedicated to singing. The percentage of both total and parvalbumin-positive neurons with perineuronal nets increased with development. In HVC (this acronym is the proper name), a song area important for sensorimotor integration, the percentage of parvalbumin neurons with perineuronal nets correlated with song maturity. Shifting the vocal critical period with tutor song deprivation decreased the percentage of neurons that were parvalbumin positive and the relative staining intensity of both parvalbumin and a component of perineuronal nets. Developmental song learning shares key characteristics with sensory critical periods, suggesting shared underlying mechanisms.
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
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 implementation of the adult form of ECM coincides with the closure of critical periods of postnatal development and culminates with the maturation of PNNs and PNN-like perisynaptic ECM aggregates.
“The implementation of this adult form of ECM coincides with the closure of critical periods of postnatal development, during which neuronal circuits are shaped by experience, and culminates with the maturation of PNNs and PNN-like perisynaptic ECM aggregates (Balmer et al., 2009; Gogolla et al., 2009; Gundelfinger et al., 2010; McRae et al., 2007; Nowicka et al., 2009; Pizzorusso et al., 2002;”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Balmer et al., 2009
In songbirds, percentage of total and parvalbumin-positive neurons with PNNs increases with development.
“the percentage of both total and parvalbumin-positive neurons with PNNs increased with development (Balmer et al., 2009)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Balmer et al., 2009
In high vocal center, percentage of parvalbumin neurons with PNNs correlates with song maturity.
“the percentage of parvalbumin neurons with PNNs correlated with song maturity”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Balmer et al., 2009
Tutor song deprivation decreases percentage of parvalbumin-positive neurons and relative staining intensity of parvalbumin and PNNs.
“shifting the vocal critical period with tutor song deprivation decreased the percentage of neurons that were parvalbumin positive and the relative staining intensity of both parvalbumin and PNNs (Balmer et al., 2009)”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Balmer et al., 2009
Perineuronal nets have been observed throughout the central nervous system of different organisms, including frogs, birds, and mammals.
“PNNs have been observed throughout the CNS of different organisms, including frogs, birds and mammals (Celio et al., 1998;Balmer et al., 2009;Gaál et al., 2014;Morawski et al., 2009).”
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 Balmer et al., 2009
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
Dynamic predictions: Oscillations and synchrony in top–down processing
Engel, A. K., Fries, P., & Singer, W. (2001) · Nature Reviews Neuroscience · doi:10.1038/35094565 · Cited by 3,454 · see citing works
SINGLE-CELL RESPONSES IN STRIATE CORTEX OF KITTENS DEPRIVED OF VISION IN ONE EYE
Wiesel, T. N., & Hubel, D. H. (1963) · Journal of Neurophysiology · doi:10.1152/jn.1963.26.6.1003 · Cited by 2,628 · see citing works
Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices
Buschman, T. J., & Miller, E. K. (2007) · Science · doi:10.1126/science.1138071 · Cited by 2,380 · see citing works
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323 · see citing works
Sensitive periods in the development of the brain and behavior
Knudsen, E. I. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/0898929042304796 · Cited by 1,842 · 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
Birdsong and human speech: common themes and mechanisms
Doupe, A. J., & Kuhl, P. K. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.567 · Cited by 1,633 · see citing works
Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks
Buzsáki, G., & Chrobak, J. J. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80012-3 · Cited by 878 · see citing works
Konishi, M. (1965) · Zeitschrift für Tierpsychologie · doi:10.1111/j.1439-0310.1965.tb01688.x · Cited by 832 · see citing works
Parvalbumin in Most γ-Aminobutyric Acid-Containing Neurons of the Rat Cerebral Cortex
Celio, M. R. (1986) · Science · doi:10.1126/science.3945815 · Cited by 740 · see citing works
A procedure for an automated measurement of song similarity
Tchernichovski, O., Nottebohm, F., Ho, C. E., Pesaran, B., & Mitra, P. P. (2000) · Animal Behaviour · doi:10.1006/anbe.1999.1416 · Cited by 723 · see citing works
Inhibitory threshold for critical-period activation in primary visual cortex
Fagiolini, M., & Hensch, T. K. (2000) · Nature · doi:10.1038/35004582 · Cited by 716 · see citing works
Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons
Tamás, G., Buhl, E. H., Lörincz, A., & Somogyi, P. (2000) · Nature Neuroscience · doi:10.1038/73936 · Cited by 648 · see citing works
Sleep Enhances Plasticity in the Developing Visual Cortex
Frank, M. G., Issa, N. P., & Stryker, M. P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00279-3 · Cited by 523 · see citing works
Belmonte, M. K., Cook, E. H., Anderson, G. M., Rubenstein, J. L. R., Greenough, W. T., Beckel-Mitchener, A., Courchesne, E., Boulanger, L. M., Powell, S. B., Levitt, P. R., et al. (2004) · Molecular Psychiatry · doi:10.1038/sj.mp.4001499 · Cited by 442 · see citing works
Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons
Galarreta, M., & Hestrin, S. (2001) · Science · doi:10.1126/science.1061395 · Cited by 389 · see citing works
Song learning in zebra finches: some effects of song model availability on what is learnt and when
Eales, L. A. (1985) · Animal Behaviour · doi:10.1016/s0003-3472(85)80189-5 · Cited by 376 · see citing works
Neural mechanisms of birdsong memory
Bolhuis, J. J., & Gahr, M. L. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1904 · Cited by 373 · see citing works
Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R., & Schachner, M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20361 · Cited by 365 · see citing works
Birdsong and speech development: could there be parallels?
Marler, P. (1971) · PubMed · Cited by 352 · see citing works
Härtig, W., Derouiche, A., Welt, K., Brauer, K., Grosche, J., Mäder, M., Reichenbach, A., & Brückner, G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01784-9 · Cited by 339 · see citing works
How sleep affects the developmental learning of bird song
Derégnaucourt, S., Mitra, P. P., Fehér, O., Pytte, C., & Tchernichovski, O. (2005) · Nature · doi:10.1038/nature03275 · Cited by 320 · see citing works
Critical period revisited: impact on vision
Morishita, H., & Hensch, T. K. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.05.009 · Cited by 311 · see citing works
Sensory Deprivation Alters Aggrecan and Perineuronal Net Expression in the Mouse Barrel Cortex
McRae, P. A., Rocco, M. M., Kelly, G., Brumberg, J. C., & Matthews, R. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5425-06.2007 · Cited by 272 · see citing works
Ontogeny of brain nuclei controlling song learning and behavior in zebra finches
Bottjer, S., Glaessner, S., & Arnold, A. P. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-06-01556.1985 · Cited by 225 · see citing works
Galtrey, C. M., Kwok, J. C. F., Carulli, D., Rhodes, K. E., & Fawcett, J. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06108.x · Cited by 203 · see citing works
Zaremba, S., Guimaraes, A., Kalb, R. G., & Hockfield, S. J. (1989) · Neuron · doi:10.1016/0896-6273(89)90305-x · Cited by 182 · see citing works
Computerized EEG analyses of autistic children
Cantor, D. S., Thatcher, R. W., Hrybyk, M., & Kaye, H. (1986) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01531728 · Cited by 180 · see citing works
A surface antigen expressed by a subset of neurons in the vertebrate central nervous system.
Hockfield, S. J., & McKay, R. D. G. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.18.5758 · Cited by 175 · see citing works
Abnormal EEG lateralization in boys with autism
Stroganova, T. A., Nygren, G., Tsetlin, M. M., Posikera, I. N., Gillberg, C., Elam, M., & Orekhova, E. V. (2007) · Clinical Neurophysiology · doi:10.1016/j.clinph.2007.05.005 · Cited by 163 · see citing works
Sur, M., Frost, D., & Hockfield, S. J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00874.1988 · Cited by 156 · see citing works
Aste, N., Balthazart, J., Absil, P., Grossmann, R., M�lhbauer, E., Viglietti‐Panzica, C., & Panzica, G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980629)396:2 · Cited by 147 · see citing works
Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders
Cristo, G. D. (2007) · Clinical Genetics · doi:10.1111/j.1399-0004.2007.00822.x · Cited by 131 · see citing works
A systems neuroscience approach to autism: Biological, cognitive, and clinical perspectives
Eigsti, I., & Shapiro, T. (2003) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.10081 · Cited by 117 · see citing works
Androgens and estrogens induce seasonal‐like growth of song nuclei in the adult songbird brain
Tramontin, A. D., Wingfield, J. C., & Brenowitz, E. A. (2003) · Journal of Neurobiology · doi:10.1002/neu.10263 · Cited by 114 · see citing works
Gil, D., Naguib, M., Riebel, K., Rutstein, A. N., & Gahr, M. L. (2006) · Journal of Neurobiology · doi:10.1002/neu.20312 · Cited by 113 · see citing works
Shifting baselines in attention research
Driver, J., & Frith, C. (2000) · Nature reviews. Neuroscience · doi:10.1038/35039083 · Cited by 111 · see citing works
Calcium‐binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata)
Wild, J. M., Williams, M. N., Howie, G., & MOONEY, R. D. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20403 · Cited by 108 · see citing works
State and Neuronal Class-Dependent Reconfiguration in the Avian Song System
Rauske, P. L., Shea, S. D., & Margoliash, D. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00655.2002 · Cited by 91 · see citing works
Cellerino, A., Siciliano, R., Domenici, L., & Maffei, L. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90514-3 · Cited by 77 · see citing works
Boseret, G., Carere, C., Ball, G. F., & Balthazart, J. (2006) · Journal of Neurobiology · doi:10.1002/neu.20268 · Cited by 70 · see citing works
Delayed development of song control nuclei in the zebra finch is related to behavioral development
Herrmann, K., & Bischof, H. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902450204 · Cited by 67 · see citing works
Hermanson, O., & Blomqvist, A. (1997) · The Journal of comparative neurology · doi:10.1002/(sici)1096-9861(19971013)387:1 · Cited by 61 · see citing works
Braun, K., Scheich, H., Zuschratter, W., Heizmann, C. W., Matute, C., & Streit, P. (1988) · Brain Research · doi:10.1016/0006-8993(88)90609-9 · Cited by 52 · see citing works
D'Costa, A. P., Prevette, D. M., Houenou, L. J., Wang, S., Zackenfels, K., Rohrer, H., Zapf, J., Caroni, P., & Oppenheim, R. W. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19980905)36:3 · Cited by 49 · see citing works
Yazaki‐Sugiyama, Y., & MOONEY, R. D. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00467.2004 · Cited by 39 · see citing works
HVC Neural Sleep Activity Increases With Development and Parallels Nightly Changes in Song Behavior
Crandall, S. R., Adam, M. K., Kinnischtzke, A. K., & Nick, T. A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00128.2007 · Cited by 36 · see citing works
Self-citationLeitner, S., & Catchpole, C. K. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20521 · Cited by 34 · see citing works
Developmental Modulation of the Temporal Relationship Between Brain and Behavior
Crandall, S. R., Aoki, N., & Nick, T. A. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00907.2006 · Cited by 24 · see citing works
Self-citationTorres, E. M., Meldrum, A., Kirik, D., & Dunnett, S. B. (2006) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2006.05.016 · Cited by 21 · see citing works
Day, N. F., Kinnischtzke, A. K., Adam, M. K., & Nick, T. A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90501.2008 · Cited by 19 · see citing works
Self-citationDaily and developmental modulation of “premotor” activity in the birdsong system
Day, N. F., Kinnischtzke, A. K., Adam, M., & Nick, T. A. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20739 · Cited by 18 · see citing works
Self-citationTheunissen, F. E. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00690.2004 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Importance of investing in adolescence from a developmental science perspective
Dahl, R. E., Allen, N. B., Wilbrecht, L., & Suleiman, A. B. (2018) · Nature · doi:10.1038/nature25770 · Cited by 1,196 · see citing works
Adolescence as a neurobiological critical period for the development of higher-order cognition
Larsen, B., & Luna, B. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.09.005 · Cited by 853 · see citing works
Critical periods in speech perception: New directions
Werker, J. F., & Hensch, T. K. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015104 · Cited by 774 · see citing works
Balancing Plasticity/Stability Across Brain Development
Takesian, A. E., & Hensch, T. K. (2013) · Progress in Brain Research · doi:10.1016/b978-0-444-63327-9.00001-1 · Cited by 667 · see citing works
The roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
Fawcett, J. W., Oohashi, T., & Pizzorusso, T. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0196-3 · Cited by 589 · see citing works
Animals lacking link protein have attenuated perineuronal nets and persistent plasticity
Carulli, D., Pizzorusso, T., Kwok, J. C. F., Putignano, E., Poli, A., Forostyak, S., Andrews, M. R., Deepa, S. S., Glant, T. T., & Fawcett, J. W. (2010) · Brain · doi:10.1093/brain/awq145 · Cited by 495 · see citing works
Fear erasure in mice requires synergy between antidepressant drugs and extinction training
Karpova, N. N., Pickenhagen, A., Lindholm, J., Tiraboschi, E., Kulesskaya, N., Ágústsdóttir, A., Antila, H., Popova, D., Akamine, Y., Sullivan, R., et al. (2011) · Science · doi:10.1126/science.1214592 · Cited by 382 · see citing works
Otx2 Binding to Perineuronal Nets Persistently Regulates Plasticity in the Mature Visual Cortex
Beurdeley, M., Spatazza, J., Lee, H. H. C., Sugiyama, S., Bernard, C., Di Nardo, A. A., Hensch, T. K., & Prochiantz, A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0394-12.2012 · Cited by 398 · see citing works
The 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
Autism: A “Critical Period” Disorder?
LeBlanc, J. J., & Fagiolini, M. (2011) · Neural Plasticity · doi:10.1155/2011/921680 · Cited by 301 · see citing works
Lensjø, K. K., Lepperød, M. E., Dick, G., Hafting, T., & Fyhn, M. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2504-16.2016 · Cited by 281 · see citing works
Callaghan, B. L., & Tottenham, N. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.204 · Cited by 268 · see citing works
Reinhard, S. M., Razak, K., & Ethell, I. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00280 · Cited by 219 · see citing works
Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons
Balmer, T. S. (2016) · eneuro · doi:10.1523/eneuro.0112-16.2016 · Cited by 220 · see citing works
Self-citationErasing Fear Memories with Extinction Training: Figure 1.
Quirk, G. J., Paré, D., Richardson, R., Herry, C., Monfils, M., Schiller, D., & Vicentic, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4268-10.2010 · Cited by 220 · see citing works
The brain interstitial system: Anatomy, modeling, in vivo measurement, and applications
Lei, Y., Han, H., Yuan, F., Javeed, A., & Zhao, Y. L. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.12.007 · Cited by 215 · see citing works
Aggrecan Directs Extracellular Matrix-Mediated Neuronal Plasticity
Rowlands, D., Lensjø, K. K., Dinh, T., Yang, S., Andrews, M. R., Hafting, T., Fyhn, M., Fawcett, J. W., & Dick, G. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1122-18.2018 · Cited by 204 · see citing works
Translating Birdsong: Songbirds as a Model for Basic and Applied Medical Research
Brainard, M. S., & Doupe, A. J. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-152826 · Cited by 208 · see citing works
Cognitive-Affective Functions of the Cerebellum
Rudolph, S., Badura, A., Lutzu, S., Pathak, S. S., Thieme, A. G., Verpeut, J. L., Wagner, M. J., Yang, Y., & Fioravante, D. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1451-23.2023 · Cited by 196 · see citing works
The extracellular matrix and perineuronal nets in memory
Fawcett, J. W., Fyhn, M., Jendelova, P., Kwok, J. C. F., Ruzicka, J., & Sorg, B. A. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01634-3 · Cited by 169 · see citing works
Extracellular matrix abnormalities in schizophrenia
Berretta, S. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.08.010 · Cited by 179 · see citing works
Early life nutrition and neural plasticity
Georgieff, M. K., Brunette, K. E., & Tran, P. V. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000061 · Cited by 177 · see citing works
Happel, M. F. K., Niekisch, H., Castiblanco Rivera, L. L., Ohl, F. W., Deliano, M., & Frischknecht, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310272111 · Cited by 176 · 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
Geissler, M., Gottschling, C., Aguado, A., Rauch, U., Wetzel, C. H., Hatt, H., & Faissner, A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3275-12.2013 · Cited by 140 · see citing works
The perineuronal net component of the extracellular matrix in plasticity and epilepsy
McRae, P. A., & Porter, B. E. (2012) · Neurochemistry International · doi:10.1016/j.neuint.2012.08.007 · Cited by 143 · see citing works
Lensjø, K. K., Christensen, A. C., Tennøe, S., Fyhn, M., & Hafting, T. (2017) · eneuro · doi:10.1523/eneuro.0379-16.2017 · Cited by 133 · see citing works
Wingert, J. C., & Sorg, B. A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.673210 · Cited by 129 · see citing works
Brain ageing changes proteoglycan sulfation, rendering perineuronal nets more inhibitory
Foscarin, S., Raha-Chowdhury, R., Fawcett, J. W., & Kwok, J. C. F. (2017) · Aging · doi:10.18632/aging.101256 · Cited by 139 · see citing works
Oohashi, T., Edamatsu, M., Bekku, Y., & Carulli, D. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.09.010 · Cited by 131 · see citing works
Riga, D., Kramvis, I., Koskinen, M. K., van Bokhoven, P., van der Harst, J. E., Heistek, T. S., Jaap Timmerman, A., van Nierop, P., van der Schors, R. C., Pieneman, A. W., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aai8753 · Cited by 128 · 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 Interstitial System of the Brain in Health and Disease
Shetty, A. K., & Zanirati, G. (2020) · Aging and Disease · doi:10.14336/ad.2020.0103 · Cited by 114 · see citing works
Perineuronal nets and schizophrenia: The importance of neuronal coatings
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.03.018 · Cited by 95 · see citing works
Fretham, S. J. B., Carlson, E. S., Wobken, J. D., Tran, P. V., Petryk, A., & Georgieff, M. K. (2012) · Hippocampus · doi:10.1002/hipo.22004 · Cited by 95 · see citing works
Neural ECM molecules in synaptic plasticity, learning, and memory
Senkov, O., Anđjus, P. R., Radenović, L., Soriano, E., & Dityatev, A. E. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63486-3.00003-7 · Cited by 94 · see citing works
Baker, K., Gray, A. R., & Richardson, R. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000203 · Cited by 89 · see citing works
Larsen, B., Cui, Z., Adebimpe, A., Pines, A., Alexander-Bloch, A., Bertolero, M., Calkins, M. E., Gur, R. E., Gur, R. C., Mahadevan, A. S., et al. (2022) · Science Advances · doi:10.1126/sciadv.abj8750 · Cited by 80 · see citing works
Developmental Changes in EEG Phenotypes in a Mouse Model of Fragile X Syndrome
Wen, T. H., Lovelace, J. W., Ethell, I. M., Binder, D. K., & Razak, K. A. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.047 · Cited by 75 · see citing works
Diverse functions of perineuronal nets
Karetko, M., & Skangiel-Kramska, J. (2009) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2009-1766 · Cited by 76 · see citing works
Mix, A., Benali, A., Eysel, U. T., & Funke, K. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07425.x · Cited by 78 · see citing works
Mirzadeh, Z., Alonge, K. M., Cabrales, E., Herranz‐Pérez, V., Scarlett, J. M., Brown, J. M., Hassouna, R., Matsen, M. E., Hồng, N. T., García‐Verdugo, J. M., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-018-0029-0 · Cited by 76 · see citing works
Circadian Rhythms of Perineuronal Net Composition
Pantazopoulos, H., Gisabella, B., Rexrode, L., Benefield, D., Yıldız, E., Seltzer, P., Valeri, J., Chelini, G., Reich, A., Ardelt, M., et al. (2020) · eNeuro · doi:10.1523/eneuro.0034-19.2020 · Cited by 73 · see citing works
Yamada, J., & Jinno, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.061 · Cited by 71 · see citing works
Beebe, N. L., Young, J. W., Mellott, J. G., & Schofield, B. R. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0217-16.2016 · Cited by 71 · see citing works
Slaker, M. L., Jorgensen, E. T., Hegarty, D. M., Liu, X., Kong, Y., Zhang, F., Linhardt, R. J., Brown, T. E., Aicher, S. A., & Sorg, B. A. (2018) · eneuro · doi:10.1523/eneuro.0221-18.2018 · Cited by 64 · see citing works
Slaker, M. L., Barnes, J., Sorg, B. A., & Grimm, J. W. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168256 · Cited by 57 · see citing works
Perineuronal net degradation rescues CA2 plasticity in a mouse model of Rett syndrome
Carstens, K. E., Lustberg, D. J., Shaughnessy, E. K., McCann, K. E., Alexander, G. M., & Dudek, S. M. (2021) · Journal of Clinical Investigation · doi:10.1172/jci137221 · Cited by 57 · see citing works
Bath, K. G., Russo, S. J., Pleil, K. E., Wohleb, E. S., Duman, R. S., & Radley, J. J. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.05.001 · Cited by 55 · see citing works
Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice
Brewton, D. H., Kokash, J., Jimenez, O., Pena, E. R., & Razak, K. A. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00270 · Cited by 54 · see citing works
Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex
Harkness, J. H., Gonzalez, A. E., Bushana, P. N., Jorgensen, E. T., Hegarty, D. M., Nardo, A. A. D., Prochiantz, A., Wisor, J. P., Aicher, S. A., Brown, T. E., et al. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02229-4 · Cited by 51 · see citing works
Hyperexcitability and homeostasis in fragile X Syndrome.
Liu, X., Kumar, V., Tsai, N.-P., & Auerbach, B. D. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.805929 · Cited by 53 · see citing works
Umemori, J., Winkel, F., Ċastrén, E., & Karpova, N. N. (2015) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2015.05.006 · Cited by 52 · see citing works
Yu, Z., Chen, N., Hu, D., Chen, W., Yuan, Y., Meng, S., Zhang, W., Lu, L., Han, Y., & Shi, J. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00004 · Cited by 52 · see citing works
Horita, H., Kobayashi, M., Liu, W.-C., Oka, K., Jarvis, E. D., & Wada, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042173 · Cited by 50 · see citing works
Critical Period Regulation by Thyroid Hormones: Potential Mechanisms and Sex-Specific Aspects
Batista, G., & Hensch, T. K. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00077 · Cited by 48 · 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
Callaghan, B. L., Graham, B. M., Li, S., & Richardson, R. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00090 · Cited by 48 · see citing works
Perineuronal Nets Play a Role in Regulating Striatal Function in the Mouse
Lee, H., Leamey, C. A., & Sawatari, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032747 · Cited by 47 · see citing works
Expression of aggrecan components in perineuronal nets in the mouse cerebral cortex
Ueno, H., Fujii, K., Suemitsu, S., Murakami, S., Kitamura, N., Wani, K., Aoki, S., Okamoto, M., Ishihara, T., & Takao, K. (2018) · IBRO Reports · doi:10.1016/j.ibror.2018.01.002 · Cited by 47 · see citing works
Convergent Differential Regulation of Parvalbumin in the Brains of Vocal Learners
Hara, E., Rivas, M., Ward, J. M., Okanoya, K., & Jarvis, E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029457 · Cited by 53 · 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
Neuroplasticity and MRI: A perfect match
Hamaide, J., Groof, G. D., & der Linden, A. V. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.08.005 · Cited by 46 · see citing works
Mori, C., & Wada, K. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1804-14.2015 · Cited by 39 · 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
Karetko, M., Skangiel-Kramska, J., & Nowicka, D. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.049 · Cited by 37 · see citing works
Bitanihirwe, B. K. Y., Mauney, S. A., & Woo, T.-U. W. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.03.1047 · Cited by 37 · see citing works
From molecules to behavior: Implications for perineuronal net remodeling in learning and memory
Sanchez, B., Kraszewski, P., Lee, S., & Cope, E. C. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.16036 · Cited by 37 · see citing works
White, S. A. (2009) · Brain and Language · doi:10.1016/j.bandl.2009.10.002 · Cited by 36 · see citing works
Cornez, G., Madison, F. N., der Linden, A. V., Cornil, C. A., Yoder, K. M., Ball, G. F., & Balthazart, J. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22485 · Cited by 36 · see citing works
Nguyen, A., Khaleel, H. M., & Razak, K. A. (2017) · Hearing Research · doi:10.1016/j.heares.2017.04.015 · Cited by 36 · see citing works
Chondroitin Sulfate Proteoglycan Tenascin-R Regulates Glutamate Uptake by Adult Brain Astrocytes
Okuda, H., Tatsumi, K., Morita, S., Shibukawa, Y., Korekane, H., Horii-Hayashi, N., Wada, Y., Taniguchi, N., & Wanaka, A. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.504787 · Cited by 33 · see citing works
Fear Erasure Facilitated by Immature Inhibitory Neuron Transplantation
Yang, W., Liu, T., Cao, J.-W., Chen, X.-F., Liu, X., Wang, M., Su, X., Zhang, S., Qiu, B., Hu, W., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.018 · Cited by 33 · see citing works
The protein tyrosine phosphatase RPTPζ/phosphacan is critical for perineuronal net structure
Eill, G. J., Sinha, A., Morawski, M., Viapiano, M. S., & Matthews, R. T. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.010830 · Cited by 32 · see citing works
The protein tyrosine phosphatase RPTPζ/phosphacan is critical for perineuronal net structure
Eill, G. J., Sinha, A., Morawski, M., Viapiano, M. S., & Matthews, R. T. (2020) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)49907-8 · Cited by 32 · see citing works
Distinct roles for hyaluronan in neural stem cell niches and perineuronal nets
Su, W., Matsumoto, S. G., Sorg, B. A., & Sherman, L. S. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.01.022 · Cited by 32 · see citing works
Perineuronal nets and GABAergic cells in the inferior colliculus of guinea pigs
Foster, N. L., Mellott, J. G., & Schofield, B. R. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00053 · Cited by 30 · see citing works
Microglia shape AgRP neuron postnatal development via regulating perineuronal net plasticity
Sun, J. Y., Wang, X., Sun, R., Xiao, X., Wang, Y., Peng, Y., & Gao, Y. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02326-2 · Cited by 29 · see citing works
Seasonal changes of perineuronal nets and song learning in adult canaries (Serinus canaria)
Cornez, G., Collignon, C., Müller, W., Ball, G. F., Cornil, C. A., & Balthazart, J. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112437 · Cited by 29 · see citing works
Boerma, T., ter Haar, S. M., Ganga, R., Wijnen, F. N. K., Blom, E., & Wierenga, C. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105398 · Cited by 29 · see citing works
Recent Advances in the Genetics of Vocal Learning
Condro, M. C., & White, S. A. (2014) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2014.90003 · Cited by 27 · see citing works
Sexually dimorphic perineuronal nets in the rodent and primate reproductive circuit
Ciccarelli, A., Weijers, D., Kwan, W. C., Warner, C. E., Bourne, J. A., & Gross, C. T. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25167 · Cited by 28 · see citing works
Cornez, G., ter Haar, S. M., Cornil, C. A., & Balthazart, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123199 · Cited by 28 · see citing works
Mueller, A. L., Davis, A., Sovich, S., Carlson, S. S., & Robinson, F. R. (2016) · Neural Plasticity · doi:10.1155/2016/6021428 · Cited by 27 · see citing works
Vocal motor changes beyond the sensitive period for song plasticity
James, L. S., & Sakata, J. T. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00217.2014 · Cited by 28 · see citing works
Cornez, G., Jonckers, E., ter Haar, S. M., der Linden, A. V., Cornil, C. A., & Balthazart, J. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.0849 · Cited by 27 · see citing works
Mafi, 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
Cornez, G., Collignon, C., Müller, W., Cornil, C. A., Ball, G. F., & Balthazart, J. (2020) · eNeuro · doi:10.1523/eneuro.0361-19.2020 · Cited by 26 · see citing works
Bíró, L., Miskolczi, C., Szebik, H., Bruzsik, B., Varga, Z. K., Szente, L., Tóth, M., Halász, J., & Mikics, É. (2023) · Neurobiology of Stress · doi:10.1016/j.ynstr.2023.100546 · Cited by 26 · see citing works
Net gain and loss: influence of natural rewards and drugs of abuse on perineuronal nets
Brown, T. E., & Sorg, B. A. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-022-01337-x · Cited by 25 · see citing works
Cornez, G., Shevchouk, O. T., Ghorbanpoor, S., Ball, G. F., Cornil, C. A., & Balthazart, J. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.104643 · Cited by 25 · see citing works
Song learning and plasticity in songbirds
Rundstrom, P., & Creanza, N. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.003 · Cited by 24 · see citing works
The Role and Modulation of Spinal Perineuronal Nets in the Healthy and Injured Spinal Cord
Sánchez-Ventura, J., Lane, M. A., & Udina, E. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.893857 · Cited by 25 · see citing works
Glial regulation of critical period plasticity
Starkey, J., Horstick, E. J., & Ackerman, S. D. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1247335 · Cited by 27 · see citing works
Neural Circuits Underlying Vocal Learning in Songbirds
Sakata, J. T., & Yazaki‐Sugiyama, Y. (2020) · Springer handbook of auditory research · doi:10.1007/978-3-030-34683-6_2 · Cited by 22 · see citing works
Sexually dimorphic perineuronal net expression in the songbird
Meyer, C., Boroda, E., & Nick, T. A. (2013) · Basal Ganglia · doi:10.1016/j.baga.2013.10.002 · Cited by 22 · see citing works
Self-citationLondon, S. E. (2017) · Behavioural Processes · doi:10.1016/j.beproc.2017.11.008 · Cited by 23 · see citing works
Steinzeig, A., Cannarozzo, C., & Ċastrén, E. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14512 · Cited by 21 · see citing works
Dopamine D1 Receptor Activation Drives Plasticity in the Songbird Auditory Pallium
Macêdo-Lima, M., Boyd, H. M., & Remage‐Healey, L. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2823-20.2021 · Cited by 23 · see citing works
Sultana, R., Brooks, C. B., Shrestha, A., Ogundele, O. M., & Lee, C. C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011140 · Cited by 21 · see citing works
- Authors
- Balmer, T. S., Carels, V. M., Frisch, J. L., & Nick, T. A.
- Affiliations
- University of Minnesota (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-10-14
- Volume
- 29
- Issue
- 41
- Pages
- 12878-12885
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2769505
- OpenAlex
- W2080602594
- Cited by
- 181
- References
- 53
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 9 · 2023: 13 · 2022: 11 · 2021: 15 · 2020: 13 · 2019: 13 · 2018: 13 · 2017: 14 · 2016: 12 · 2015: 16 · 2014: 11 · 2013: 11 · 2012: 7
- FWCI
- 4.61
- 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)
- Funders
- University of Minnesota
- National Institute on Deafness and Other Communication Disorders (R01DC007384, K02DC008521)
- National Institute of Neurological Disorders and Stroke (R01NS050436)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- perineuronal nets, parvalbumin, zebra finch, critical period, HVC, sensorimotor integration, neuroplasticity
- MeSH terms
- Age Factors, Animals, Animals, Newborn, Cell Count, Critical Period, Psychological, Female, Learning, Male, Nerve Net, Neuronal Plasticity, Neurons, Parvalbumins, Social Isolation, Vocalization, Animal, Entropy, Finches, High Vocal Center, In Vitro Techniques
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
