The DOI matches its Crossref record; 63 of the 63 references it cites were found in a registry or an index.
Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons
Open accessAbstract
Perineuronal nets (PNNs) are specialized complexes of extracellular matrix molecules that surround the somata of fast-spiking neurons throughout the vertebrate brain. PNNs are particularly prevalent throughout the auditory brainstem, which transmits signals with high speed and precision. It is unknown whether PNNs contribute to the fast-spiking ability of the neurons they surround. Whole-cell recordings were made from medial nucleus of the trapezoid body (MNTB) principal neurons in acute brain slices from postnatal day 21 (P21) to P27 mice. PNNs were degraded by incubating slices in chondroitinase ABC (ChABC) and were compared to slices that were treated with a control enzyme (penicillinase). ChABC treatment did not affect the ability of MNTB neurons to fire at up to 1000 Hz when driven by current pulses. However, f – I (frequency–intensity) curves constructed by injecting Gaussian white noise currents superimposed on DC current steps showed that ChABC treatment reduced the gain of spike output. An increase in spike threshold may have contributed to this effect, which is consistent with the observation that spikes in ChABC-treated cells were delayed relative to control-treated cells. In addition, parvalbumin-expressing fast-spiking cortical neurons in >P70 slices that were treated with ChABC also had reduced excitability and gain. The development of PNNs around somata of fast-spiking neurons may be essential for fast and precise sensory transmission and synaptic inhibition in the brain.
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?
In the citing paper
“As PNNs are implicated in neuronal health and function, protecting cells against neurotoxins such as Aβ1–42 [39] and oxidative stress [65] in addition to modulating neuronal activity [63, 66], the microglia-mediated loss of these structures in disease likely plays an important role in AD pathogenesis.”
From Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain (2020) · cites this paper as [63]
In the citing paper
“However, it is important to recognize that in addition to changes in the excitability of inhibitory neurons as suggested here and by others55, PNN degradation may also alter synaptic activity56 and hence network excitability.”
From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [55]
In the citing paper
“However, the role of PNNs in neural and network excitability is only beginning to be understood (Balmer, 2016; Murase et al., 2017; Wen et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
In the citing paper
“Perineuronal net dysfunction in schizophrenia may also drive changes in GABAergic cell function leading to network dysfunction, as normal PNN expression regulates excitability of PV cells (Liu et al., 2013; Balmer, 2016).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
In the citing paper
“While this mechanism has not been confirmed, chABC-mediated removal of chondroitin sulfate side chains from PNNs reduced spiking of PV cells in adult rats (Balmer, 2016; Lensjø et al., 2017) and increased spiking variability (Lensjø et al., 2017).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
In the citing paper
“As PNNs regulate PV cell activity (Balmer, 2016; Lensjø et al., 2017) and protect PV cells from oxidative stress (Cabungcal et al., 2013), PNNs can be potentially targeted to control seizures.”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
In the citing paper
“chABC-mediated degradation of PNNs around PV cells in brainstem and central auditory neurons has similar effects, resulting in reduced PV cell excitability and gain (Balmer, 2016).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Balmer, 2016
In the citing paper
“Chondroitinase ABC, an enzyme that cleaves PNN proteoglycans, reduces GABA A inhibitory postsynaptic currents (Liu et al. 2013) and reduces excitability of PV fast-spiking cortical interneurons (Balmer 2016).”
In the citing paper
“Our findings reporting increased intensities of WFA labelled PNNs around PV+ interneurons suggest altered plasticity of PV+ cells as PNNs have been known to regulate synaptic and cellular plasticity of the cells they encapsulate (45) and digestion of PNNs around PV+ cells has been shown to reduce the fast spiking properties and excitability of PV+ cells (73)”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [73]
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
NIH Image to ImageJ: 25 years of image analysis
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012) · Nature Methods · doi:10.1038/nmeth.2089 · Cited by 64,638
Ion Channels/Excitable Membranes
(2011) · Springer eBooks · doi:10.1007/springerreference_33998 · Cited by 4,066
The action of calcium on the electrical properties of squid axons
FRANKENHAEUSER, B., & Hodgkin, A. L. (1957) · The Journal of Physiology · doi:10.1113/jphysiol.1957.sp005808 · Cited by 1,839
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
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
PTPσ Is a Receptor for Chondroitin Sulfate Proteoglycan, an Inhibitor of Neural Regeneration
Shen, Y., Tenney, A. P., Busch, S. A., Horn, K. P., Cuascut, F. X., Liu, K., He, Z., Silver, J., & Flanagan, J. G. (2009) · Science · doi:10.1126/science.1178310 · Cited by 682
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
Experience-driven plasticity of visual cortex limited by myelin and nogo receptor
McGee, A. W., Yang, Y., Fischer, Q. S., Daw, N. W., & Strittmatter, S. M. (2005) · Science · doi:10.1126/science.1114362 · Cited by 643
Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., & Huang, Z. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1851-04.2004 · Cited by 596
Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity
Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009) · Nature Neuroscience · doi:10.1038/nn.2338 · Cited by 554
Perineuronal nets: past and present
Celio, M. R., Spreafico, R., De Biasi, S., & Vitellaro-Zuccarello, L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01298-3 · Cited by 497
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
Taschenberger, H., & von Gersdorff, H. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09162.2000 · Cited by 486
Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation
García‐Alías, G., Barkhuysen, S., Buckle, M., & Fawcett, J. W. (2009) · Nature Neuroscience · doi:10.1038/nn.2377 · Cited by 474
Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons
Härtig, W., Brauer, K., & Brückner, G. (1992) · NeuroReport · doi:10.1097/00001756-199210000-00012 · Cited by 440
Hebbian synapses in visual cortex
Kirkwood, A., & Bear, M. F. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01634.1994 · Cited by 418
A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex
Kuhlman, S. J., Olivas, N. D., Tring, E., Ikrar, T., Xu, X., & Trachtenberg, J. T. (2013) · Nature · doi:10.1038/nature12485 · Cited by 412
SYNAPTIC MECHANISMS FOR CODING TIMING IN AUDITORY NEURONS
Trussell, L. O. (1999) · Annual Review of Physiology · doi:10.1146/annurev.physiol.61.1.477 · Cited by 412
Optimizing Synaptic Architecture and Efficiency for High-Frequency Transmission
Taschenberger, H., Leão, R. M., Rowland, K. C., Spirou, G. A., & von Gersdorff, H. (2002) · Neuron · doi:10.1016/s0896-6273(02)01137-6 · Cited by 389
Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator
Mataga, N., Mizuguchi, Y., & Hensch, T. K. (2004) · Neuron · doi:10.1016/j.neuron.2004.11.028 · Cited by 371
Structural and functional recovery from early monocular deprivation in adult rats
Pizzorusso, T., Medini, P., Landi, S., Baldini, S., Berardi, N., & Maffei, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602657103 · Cited by 367
Dityatev, A., Brückner, G., Dityateva, G., Grosche, J., Kleene, R., & Schachner, M. (2007) · Developmental Neurobiology · doi:10.1002/dneu.20361 · Cited by 365
Brückner, G., Brauer, K., Härtig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girard, N., Oertel, W. H., & Reichenbach, A. (1993) · Glia · doi:10.1002/glia.440080306 · Cited by 358
Guidance Molecules in Axon RegenerationPreprint
Giger, R. J., Hollis, E. R., II, & Tuszynski, M. H. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001867 · Cited by 353
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
Spike initiation by transmembrane current: a white‐noise analysis.
Bryant, H. L., & Segundo, J. P. (1976) · The Journal of Physiology · doi:10.1113/jphysiol.1976.sp011516 · Cited by 330
THE ROLE OF TIMING IN THE BRAIN STEM AUDITORY NUCLEI OF VERTEBRATES
Oertel, D. (1999) · Annual Review of Physiology · doi:10.1146/annurev.physiol.61.1.497 · Cited by 321
Massey, J. M., Hubscher, C. H., Wagoner, M. R., Decker, J. A., Amps, J., Silver, J., & Onifer, S. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5467-05.2006 · Cited by 320
Reducing Intracortical Inhibition in the Adult Visual Cortex Promotes Ocular Dominance Plasticity
Harauzov, A., Spolidoro, M., DiCristo, G., De Pasquale, R., Cancedda, L., Pizzorusso, T., Viegi, A., Berardi, N., & Maffei, L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.2233-09.2010 · Cited by 319
Perineuronal Nets Suppress Plasticity of Excitatory Synapses on CA2 Pyramidal Neurons
Carstens, K. E., Phillips, M. L., Pozzo-Miller, L., Weinberg, R. J., & Dudek, S. M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0245-16.2016 · Cited by 271
Srinivasan, J., Schachner, M., & Catterall, W. A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15753 · Cited by 249
Very long-term memories may be stored in the pattern of holes in the perineuronal net
Tsien, R. Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310158110 · Cited by 244
Bukalo, O., Schachner, M., & Dityatev, A. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00082-3 · Cited by 236
Henze, D. A., & Buzsáki, G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00167-1 · Cited by 235
Romberg, C., Yang, S., Melani, R., Andrews, M. R., Horner, A. E., Spillantini, M. G., Bussey, T. J., Fawcett, J. W., Pizzorusso, T., & Saksida, L. M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.6267-11.2013 · Cited by 231
Kochlamazashvili, G., Henneberger, C., Bukalo, O., Dvoretskova, E., Senkov, O., Lievens, P. M.-J., Westenbroek, R., Engel, A. K., Catterall, W. A., Rusakov, D. A., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.030 · Cited by 215
Modulation of Perineuronal Nets and Parvalbumin with Developmental Song Learning
Balmer, T. S., Carels, V. M., Frisch, J. L., & Nick, T. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.2974-09.2009 · Cited by 181
Self-citationGaltrey, C. M., Asher, R. A., Nothias, F., & Fawcett, J. W. (2007) · Brain · doi:10.1093/brain/awl372 · Cited by 169
Seeger, G., Brauer, K., Ha¨rtig, W., & Bru¨ckner, G. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90044-2 · Cited by 156
Cellular mechanisms for preservation of timing in central auditory pathways
Trussell, L. O. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80027-x · Cited by 153
Synaptic Transmission at the Calyx of Held Under In Vivo–Like Activity Levels
Hermann, J. J., Pecka, M., von Gersdorff, H., Grothe, B., & Klug, A. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00355.2007 · Cited by 147
Sound localization: Jeffress and beyond
Ashida, G., & Carr, C. E. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.05.008 · Cited by 142
The medial nucleus of the trapezoid body: Comparative physiology
Kopp‐Scheinpflug, C., Tolnai, S., Malmierca, M. S., & Rübsamen, R. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.088 · Cited by 123
Morawski, M., Reinert, T., Meyer-Klaucke, W., Wagner, F. E., Tröger, W., Reinert, A., Jäger, C., Brückner, G., & Arendt, T. (2015) · Scientific Reports · doi:10.1038/srep16471 · Cited by 116
Hrabětová, S., Masri, D., Tao, L., Xiao, F., & Nicholson, C. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.170092 · Cited by 113
Molecular control of brain plasticity and repair
Fawcett, J. (2009) · Progress in Brain Research · doi:10.1016/s0079-6123(09)17534-9 · Cited by 105
KCNQ5 channels control resting properties and release probability of a synapse
Huang, H. Y., & Trussell, L. O. (2011) · Nature Neuroscience · doi:10.1038/nn.2830 · Cited by 91
Kim, J. H., Renden, R., & von Gersdorff, H. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3389-12.2013 · Cited by 86
Two-Dimensional Time Coding in the Auditory Brainstem
Slee, S. J., Higgs, M. H., Fairhall, A. L., & Spain, W. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2666-05.2005 · Cited by 84
Bertolotto, A., Manzardo, E., & Guglielmone, R. (1996) · Cell and Tissue Research · doi:10.1007/s004410050538 · Cited by 82
Construction of perineuronal net-like structure by cortical neurons in culture
Miyata, S., Nishimura, Y., Hayashi, N., & Oohira, A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.031 · Cited by 75
Blosa, M., Sonntag, M., Jäger, C., Weigel, S., Seeger, J., Frischknecht, R., Seidenbecher, C. I., Matthews, R. T., Arendt, T., Rübsamen, R., et al. (2015) · The Journal of Physiology · doi:10.1113/jp270849 · Cited by 74
Härtig, W., Singer, A., Grosche, J., Brauer, K., Ottersen, O. P., & Brückner, G. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02211-9 · Cited by 62
Blosa, M., Sonntag, M., Brückner, G., Jäger, C., Seeger, G., Matthews, R. T., Rübsamen, R., Arendt, T., & Morawski, M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.003 · Cited by 60
Effects of Digesting Chondroitin Sulfate Proteoglycans on Plasticity in Cat Primary Visual Cortex
Vorobyov, V., Kwok, J. C. F., Fawcett, J. W., & Sengpiel, F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2283-12.2013 · Cited by 51
Perineuronal nets in the auditory system
Sonntag, M., Blosa, M., Schmidt, S., Rübsamen, R., & Morawski, M. (2015) · Hearing Research · doi:10.1016/j.heares.2014.12.012 · Cited by 50
Kuhlman, S. J., Lu, J., Lazarus, M. S., & Huang, Z. J. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000797 · Cited by 48
Emergence of Adaptive Computation by Single Neurons in the Developing Cortex
Mease, R. A., Famulare, M., Gjorgjieva, J., Moody, W. J., & Fairhall, A. L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3263-12.2013 · Cited by 45
Myers, A. K., Ray, J., & Kulesza, R. J. (2012) · Brain Research · doi:10.1016/j.brainres.2012.05.024 · Cited by 34
Action Potential Timing Precision in Dorsal Cochlear Nucleus Pyramidal Cells
Street, S. E., & Manis, P. B. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00469.2006 · Cited by 31
Murakami, T., Tsubouchi, M., Tubouchi, Y., Taguchi, T., & Ohtsuka, A. (1994) · PubMed · doi:10.18926/amo/31092 · Cited by 21
Johnston, J., Postlethwaite, M., & Forsythe, I. D. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.06.025 · Cited by 13
The Binding of Iron to Perineuronal Nets: A Combined Nuclear Microscopy and Mössbauer Study
Morawski, M., Reinert, T., Brückner, G., Wagner, F. E., Arendt, T. H., & Tröger, W. (2005) · Hyperfine Interactions · doi:10.1007/s10751-005-9116-1 · Cited by 12
Flagged first, then by citations
Cited by
Sorted by citations
Perineuronal nets stabilize the grid cell network
Christensen, A. C., Lensjø, K. K., Lepperød, M. E., Dragly, S.-A., Sutterud, H., Blackstad, J. S., Fyhn, M., & Hafting, T. (2021) · Nature Communications · doi:10.1038/s41467-020-20241-w · Cited by 1,865
Critical period regulation across multiple timescales
Reh, R. K., Dias, B. G., Nelson, C. A., Kaufer, D., Werker, J. F., Kolb, B., Levine, J. D., & Hensch, T. K. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820836117 · Cited by 492
Neuron–glia interactions in the pathophysiology of epilepsy
Patel, D. C., Tewari, B. P., Chaunsali, L., & Sontheimer, H. W. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0126-4 · Cited by 476
Microglia facilitate loss of perineuronal nets in the Alzheimer's disease brain
Crapser, J. D., Spangenberg, E. E., Barahona, R. A., Arreola, M. A., Hohsfield, L. A., & Green, K. N. (2020) · EBioMedicine · doi:10.1016/j.ebiom.2020.102919 · Cited by 280
Crosstalk between glia, extracellular matrix and neurons
Song, I., & Dityatev, A. E. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.03.003 · Cited by 270
Metadata
- Authors
- Balmer, T. S.
- Affiliations
- Marine Biological Laboratory (US)
- Corresponding author
- Balmer, Timothy S.
- ORCID
- Balmer, Timothy S.
- Venue
- eneuro
- Publisher
- Society for Neuroscience
- Published
- 2016-07
- Volume
- 3
- Issue
- 4
- Pages
- ENEURO.0112-16.2016
- ISSN
- 2373-2822 (ISSN-L)
- PMC
- PMC4987413
- OpenAlex
- W2467652827
- Cited by
- 220
- References
- 63
- Citations by year
- 2026: 13 · 2025: 26 · 2024: 24 · 2023: 18 · 2022: 19 · 2021: 22 · 2020: 28 · 2019: 24 · 2018: 28 · 2017: 18
- FWCI
- 13.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- eNeuro (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Open Access Server of the Woods Hole Scientific Community (Woods Hole Scientific Community) (submittedVersion, cc-by)
- Funders
- Grass Foundation
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- perineuronal nets, fast-spiking neurons, neuronal excitability, medial nucleus of the trapezoid body, auditory brainstem, chondroitinase ABC, extracellular matrix, parvalbumin interneurons, spike threshold, synaptic inhibition, sensory transmission
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Central Nervous System Agents, Extracellular Matrix, Female, Immunohistochemistry, Male, Mice, Inbred C57BL, Microscopy, Fluorescence, Neurons, Penicillinase, Patch-Clamp Techniques, Chondroitin ABC Lyase, Tissue Culture Techniques, Superior Olivary Complex
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