Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning
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The perineuronal net (PNN) surrounds neurons in the central nervous system and is thought to regulate developmental plasticity. A few studies have shown an involvement of the PNN in hippocampal plasticity and memory storage in adult animals. In addition to the hippocampus, plasticity in the medial prefrontal cortex (mPFC) has been demonstrated to be critical for the storage of long-term memory, particularly memories for temporally separated events. In the present study, we examined the role of PNN in the acquisition and retention of memories for trace (in which the conditioned and unconditioned stimuli are temporally separated) and delayed (in which the conditioned and unconditioned stimuli overlap) fear conditioning in both the hippocampus and the mPFC. Consistent with a role for the hippocampus in memory storage in both delayed and trace fear conditioning, removal of hippocampal PNN disrupted contextual and trace fear memory. Disruption of the PNN in the mPFC impaired long-term trace and conditioned stimulus (CS)-elicited fear memory in the trace fear conditioning task. Interestingly, CS-elicited fear memory was also impaired when a delayed fear conditioning paradigm was used. These findings further support a role for the PNN in neural plasticity and implicate PNN-regulated plasticity in neocortical memory storage.
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PNN degradation in the hippocampus, medial prefrontal cortex (mPFC), anterior cingulate cortex, BLA, or auditory cortex impairs the expression of fear conditioning.
“Since then, other studies have shown that PNN degradation in the hippocampus, medial prefrontal cortex (mPFC), anterior cingulate cortex, BLA, or auditory cortex impairs the expression of fear conditioning [62, 83–85].”
From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [83]
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory.
Tsien, J. Z., Huerta, P. T., & Tonegawa, S. (1996) · Cell · doi:10.1016/s0092-8674(00)81827-9 · Cited by 1,782 · cited 1× · see citing works
“during training in order to store learned information (Tsien et al. 1996; Blum et al. 1999).”
BackgroundReactivation 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
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 · see citing works
Burgos-Robles, A., Vidal-Gonzalez, I., & Quirk, G. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0378-09.2009 · Cited by 530 · see citing works
Blum, S., Moore, A. N., Adams, F., & Dash, P. K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03535.1999 · Cited by 522 · see citing works
Self-citationWisteria 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 · see citing works
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 · 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
Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat
Weiss, C., Bouwmeester, H., Power, J., & Disterhoft, J. F. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00096-5 · Cited by 262 · see citing works
Bukalo, O., Schachner, M., & Dityatev, A. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00082-3 · Cited by 236 · see citing works
Laviolette, S. R., Lipski, W. J., & Grace, A. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1168-05.2005 · Cited by 235 · see citing works
A Role for Prefrontal Cortex in Memory Storage for Trace Fear Conditioning
Runyan, J. D., Moore, A. N., & Dash, P. K. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4880-03.2004 · Cited by 224 · see citing works
Self-citationGewirtz, J. C., Falls, W. A., & Davis, M. E. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.4.712 · Cited by 222 · see citing works
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 · see citing works
Cortical involvement in acquisition and extinction of trace eyeblink conditioning.
Weible, A. P., McEchron, M. D., & Disterhoft, J. F. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.6.1058 · Cited by 212 · see citing works
Hendry, S., Jones, E. G., Hockfield, S. J., & McKay, R. D. G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-02-00518.1988 · Cited by 205 · see citing works
Baeg, E. H. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.5.441 · Cited by 205 · see citing works
Brückner, G., Hausen, D., Härtig, W., Drlicek, M., Arendt, T., & Brauer, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00071-8 · Cited by 196 · see citing works
Lesions of the Caudal Area of Rabbit Medial Prefrontal Cortex Impair Trace Eyeblink Conditioning
Kronforst-Collins, M. A., & Disterhoft, J. F. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1997.3818 · Cited by 191 · see citing works
Cortical involvement in acquisition and extinction of trace eyeblink conditioning.
Weible, A. P., McEchron, M. D., & Disterhoft, J. F. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.6.1058 · Cited by 181 · 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
Gewirtz, J. C., Falls, W. A., & Davis, M. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.4.712 · Cited by 174 · 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
Medial prefrontal cortex and Pavlovian conditioning: Trace versus delay conditioning.
McLaughlin, J., Skaggs, H., Churchwell, J., & Powell, D. A. (2002) · Behavioral Neuroscience · doi:10.1037/0735-7044.116.1.37 · Cited by 134 · see citing works
Brückner, G., Seeger, G., Brauer, K., Härtig, W., Kacza, J., & Bigl, V. (1994) · Brain Research · doi:10.1016/s0006-8993(09)90012-9 · Cited by 132 · see citing works
Chondroitin sulphate proteoglycans: Key modulators of spinal cord and brain plasticity
Bartus, K., James, N. D., Bosch, K. D., & Bradbury, E. J. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.08.008 · Cited by 117 · see citing works
Saghatelyan, A., Gorissen, S., Albert, M., Hertlein, B., Schachner, M., & Dityatev, A. E. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00216.x · Cited by 117 · see citing works
Brückner, G., Grosche, J., Hartlage‐Rübsamen, M., Schmidt, S., & Schachner, M. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(03)00036-x · Cited by 116 · see citing works
Nowicka, D., Soulsby, S., Skangiel‐Kramska, J., & Glazewski, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06996.x · Cited by 110 · see citing works
Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat
Alpár, A., Gärtner, U., Härtig, W., & Brückner, G. (2006) · Brain Research · doi:10.1016/j.brainres.2006.08.069 · Cited by 93 · see citing works
Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning
Esclassan, F., Coutureau, É., Scala, G. D., & Marchand, A. R. (2008) · Hippocampus · doi:10.1002/hipo.20473 · Cited by 92 · see citing works
Aggrecan-based extracellular matrix is an integral part of the human basal ganglia circuit
Brückner, G., Morawski, M., & Arendt, T. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.10.033 · Cited by 90 · see citing works
A unified theory for systems and cellular memory consolidation
Dash, P. K., Hebert, A. E., & Runyan, J. D. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.02.001 · Cited by 72 · see citing works
Self-citationTrace fear conditioning enhances synaptic and intrinsic plasticity in rat hippocampus
Song, C., Detert, J. A., Sehgal, M., & Moyer, J. R. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00692.2011 · Cited by 64 · see citing works
Gilmartin, M. R., & McEchron, M. D. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.164 · Cited by 62 · see citing works
Pyramidal cells ensheathed by perineuronal nets in human motor and somatosensory cortex
Hausen, D., Brückner, G., Drlicek, M., Härtig, W., Brauer, K., & Bigl, V. (1996) · NeuroReport · doi:10.1097/00001756-199607290-00006 · Cited by 59 · see citing works
Neural Population-Level Memory Traces in the Mouse Hippocampus
Chen, G., Wang, L. P., & Tsien, J. Z. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008256 · Cited by 56 · see citing works
Nakamura, M., Nakano, K., Morita, S., Nakashima, T., Oohira, A., & Miyata, S. (2009) · Brain Research · doi:10.1016/j.brainres.2008.11.022 · Cited by 54 · see citing works
Distribution of cat‐301 immunoreactivity in the frontal and parietal lobes of the macaque monkey
McGuire, P. K., Hockfield, S. J., & Goldman, P. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902880207 · Cited by 45 · see citing works
Effect of hyaluronidase on brain extracellular matrix in vivo and optic nerve regeneration
Tona, A., & Bignami, A. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490360209 · Cited by 25 · see citing works
Gáti, G., Morawski, M., Lendvai, D., Matthews, R. T., Jäger, C., Zachar, G., Arendt, T., & Alpár, A. (2010) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2010.07.002 · Cited by 18 · see citing works
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Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity
Sorg, B. A., Berretta, S., Blacktop, J. M., Fawcett, J. W., Kitagawa, H., Kwok, J. C. F., & Miquel, M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2351-16.2016 · Cited by 454 · see citing works
Neural Stem Cell Transplantation for Neurodegenerative Diseases
De Gioia, R., Biella, F., Citterio, G., Rizzo, F., Abati, E., Nizzardo, M., Bresolin, N., Comi, G. P., & Corti, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093103 · Cited by 247 · see citing works
Perineuronal Nets: Plasticity, Protection, and Therapeutic Potential
Reichelt, A. C., Hare, D. J., Bussey, T. J., & Saksida, L. M. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.04.003 · Cited by 219 · see citing works
Slaker, M., Churchill, L., Todd, R. P., Blacktop, J. M., Zuloaga, D. G., Raber, J., Darling, R. A., Brown, T. E., & Sorg, B. A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3592-14.2015 · Cited by 208 · see citing works
Prefrontal cortical regulation of fear learning
Gilmartin, M. R., Balderston, N. L., & Helmstetter, F. J. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.05.004 · Cited by 197 · 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
Miyata, S., & Kitagawa, H. (2017) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2017.06.010 · Cited by 171 · see citing works
Vitamin D in Synaptic Plasticity, Cognitive Function, and Neuropsychiatric Illness
Mayne, P., & Burne, T. H. J. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.01.003 · Cited by 162 · see citing works
Arranz, A. M., Perkins, K. L., Irie, F., Lewis, D. P., Hrabe, J., Xiao, F., Itano, N., Kimata, K., Hrabetova, S., & Yamaguchi, Y. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3458-13.2014 · Cited by 154 · see citing works
Perineuronal nets in brain physiology and disease
Testa, D., Prochiantz, A., & Nardo, A. A. D. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.09.011 · Cited by 141 · 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
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
Removal of perineuronal nets disrupts recall of a remote fear memory
Thompson, E. H., Lensjø, K. K., Wigestrand, M. B., Malthe-Sørenssen, A., Hafting, T., & Fyhn, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713530115 · Cited by 118 · 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
Cerebellar plasticity and associative memories are controlled by perineuronal nets
Carulli, D., Broersen, R., de Winter, F., Muir, E. M., Mešković, M., de Waal, M., de Vries, S., Boele, H.-J., Canto, C. B., De Zeeuw, C. I., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1916163117 · Cited by 110 · see citing works
Yamada, J., Ohgomori, T., & Jinno, S. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12792 · Cited by 99 · see citing works
Hyaluronan modulates TRPV1 channel opening, reducing peripheral nociceptor activity and pain
Caires, R., Luis, E., Taberner, F. J., Fernandez-Ballester, G. J., Ferrer-Montiel, A. V., Balazs, E. A., Gomis, A., Belmonte, C., & de la Peña, E. (2015) · Nature Communications · doi:10.1038/ncomms9095 · Cited by 97 · see citing works
Understanding the physical basis of memory: Molecular mechanisms of the engram
Luis, C. O. S., & Ryan, T. J. (2022) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2022.101866 · Cited by 103 · 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
Guadagno, A., Belliveau, C., Mechawar, N., & Walker, C. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.669120 · Cited by 92 · see citing works
Baker, K., Gray, A. R., & Richardson, R. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000203 · Cited by 89 · see citing works
Sex Differences in the Development of the Rodent Corticolimbic System
Premachandran, H., Zhao, M., & Arruda-Carvalho, M. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.583477 · Cited by 89 · see citing works
iPlasticity: Induced juvenile‐like plasticity in the adult brain as a mechanism of antidepressants
Umemori, J., Winkel, F., Didio, G., Llach Pou, M., & Castrén, E. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12683 · Cited by 80 · see citing works
A Sweet Talk: The Molecular Systems of Perineuronal Nets in Controlling Neuronal Communication
Spijker, H. M. V. ‘., & Kwok, J. C. F. (2017) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2017.00033 · Cited by 82 · see citing works
Zhao, Y., Gibb, S. L., Zhao, J., Moore, A. N., Hylin, M. J., Menge, T. D., Xue, H., Baimukanova, G., Potter, D. R., Johnson, E. M., et al. (2016) · Stem Cells · doi:10.1002/stem.2310 · Cited by 80 · see citing works
Self-citationMirzadeh, 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
Releasing Addiction Memories Trapped in Perineuronal Nets
Lasek, A. W., Chen, H., & Chen, W.-Y. (2018) · Trends in Genetics · doi:10.1016/j.tig.2017.12.004 · Cited by 71 · see citing works
Reichelt, A. C., Gibson, G. D., Abbott, K. N., & Hare, D. J. (2019) · Food & Function · doi:10.1039/c8fo02118j · Cited by 65 · see citing works
Drzewiecki, C. M., Willing, J., & Juraska, J. M. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02137-z · Cited by 67 · see citing works
Blocking human fear memory with the matrix metalloproteinase inhibitor doxycycline
Bach, D. R., Tzovara, A., & Vunder, J. (2018) · Molecular Psychiatry · doi:10.1038/mp.2017.65 · Cited by 64 · see citing works
Schmidt, U., Herrmann, L., Hagl, K., Novak, B., Huber, C., Holsboer, F., Wotjak, C., & Buell, D. R. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00066 · Cited by 58 · see citing works
Brain extracellular space, hyaluronan, and the prevention of epileptic seizures
Perkins, K. L., Arranz, A. M., Yamaguchi, Y., & Hrabětová, S. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0017 · Cited by 55 · see citing works
Lesnikova, A., Casarotto, P. C., Fred, S. M., Voipio, M., Winkel, F., Steinzeig, A., Antila, H., Umemori, J., Biojone, C., & Castrén, E. (2021) · The Journal of Neuroscience · doi:10.1523/jneurosci.2228-20.2020 · Cited by 56 · 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
Caught in the Net: Perineuronal Nets and Addiction
Slaker, M. L., Blacktop, J. M., & Sorg, B. A. (2016) · Neural Plasticity · doi:10.1155/2016/7538208 · Cited by 50 · see citing works
Cope, E. C., Zych, A. D., Katchur, N. J., Waters, R. C., Laham, B. J., Diethorn, E. J., Park, C. Y., Meara, W. R., & Gould, E. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01174-2 · Cited by 49 · see citing works
Hyaluronan synthesis by developing cortical neurons in vitro
Fowke, T. M., Karunasinghe, R. N., Bai, J.-Z., Jordan, S., Gunn, A. J., & Dean, J. M. (2017) · Scientific Reports · doi:10.1038/srep44135 · Cited by 47 · see citing works
How Stress Influences the Dynamic Plasticity of the Brain’s Extracellular Matrix
Laham, B. J., & Gould, E. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.814287 · Cited by 47 · see citing works
Successes and Hurdles in Stem Cells Application and Production for Brain Transplantation
Henriques, D., Moreira, R., Schwamborn, J. C., de Almeida, L. P., & Mendonça, L. S. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01194 · Cited by 46 · see citing works
Chondroitin 4- O -sulfation regulates hippocampal perineuronal nets and social memory
Huang, H., Joffrin, A. M., Zhao, Y., Miller, G. M., Zhang, G. C., Oka, Y., & Hsieh‐Wilson, L. C. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301312120 · Cited by 41 · see citing works
Parvalbumin - Positive Neurons in the Neocortex: A Review
Druga, R., Salaj, M., & Al‐Redouan, A. (2023) · Physiological Research · doi:10.33549/physiolres.935005 · Cited by 42 · 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
The potential of memory enhancement through modulation of perineuronal nets
Duncan, J. A., Foster, R., & Kwok, J. C. F. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14672 · Cited by 37 · see citing works
Inhibitory control in neuronal networks relies on the extracellular matrix integrity
Dzyubenko, E., Fleischer, M., Manrique‐Castano, D., Borbor, M., Kleinschnitz, C., Faissner, A., & Hermann, D. M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03861-3 · Cited by 39 · see citing works
Zhang, L., Gao, Y.-Z., Zhao, C., Xia, J., Yang, J., & Ji, M. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109382 · 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
Xue, Y.-X., Zhu, Z., Han, H.-B., Liu, J., Meng, S., Chen, C., Yang, J., Wu, P., & Lü, L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.56 · Cited by 34 · see citing works
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Mohan, V., Wyatt, E. V., Gotthard, I., Phend, K. D., Diestel, S., Duncan, B. W., Weinberg, R. J., Tripathy, A., & Maness, P. F. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00346 · Cited by 34 · see citing works
Regulation of the E/I-balance by the neural matrisome
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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
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
Primary cilia are required for the persistence of memory and stabilization of perineuronal nets
Jovasevic, V., Zhang, H., Sananbenesi, F., Guedea, A. L., Soman, K. V., Wiktorowicz, J. E., Fischer, A., & Radulovic, J. (2021) · iScience · doi:10.1016/j.isci.2021.102617 · 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
Dubišová, J., Burianova, J. S., Svobodová, L., Makovický, P., Martínez-Varea, N., Cimpean, A., Fawcett, J. W., Kwok, J. C. F., & Kubinová, Š. (2022) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2022.01.011 · Cited by 31 · see citing works
Yang, X. (2020) · Reviews in the Neurosciences · doi:10.1515/revneuro-2019-0117 · Cited by 29 · see citing works
NPY-Y1 receptor signaling controls spatial learning and perineuronal net expression
Bertocchi, I., Mele, P., Ferrero, G., Oberto, A., Carulli, D., & Eva, C. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108425 · Cited by 26 · 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
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
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
Widmer, Y. F., Bilican, A., Bruggmann, R., & Sprecher, S. G. (2018) · Genetics · doi:10.1534/genetics.118.301106 · Cited by 25 · see citing works
Liu, L., Zhang, Y., Men, S., Li, X., Hou, S., & Ju, J. (2023) · Hippocampus · doi:10.1002/hipo.23503 · Cited by 26 · see citing works
Li, X., Wu, X., Lu, T., Kuang, C., Si, Y., Zheng, W., Li, Z., & Xue, Y.-X. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063412 · Cited by 25 · 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
Tamming, R. J., Dumeaux, V., Jiang, Y. Y., Shafiq, S., Langlois, L., Ellegood, J., Qiu, L. R., Lerch, J. P., & Bérubé, N. G. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107838 · Cited by 24 · see citing works
Dzyubenko, E., Willig, K. I., Yin, D., Sardari, M., Tokmak, E., Labus, P., Schmermund, B., & Hermann, D. M. (2023) · Journal of Biomedical Science · doi:10.1186/s12929-023-00971-x · Cited by 24 · see citing works
Alexander, G. M., Nikolova, V. D., Stöber, T. M., Gruzdev, A., Moy, S. S., & Dudek, S. M. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1626-24.2024 · Cited by 24 · see citing works
The Neurovascular Unit as a Locus of Injury in Low-Level Blast-Induced Neurotrauma
Elder, G. A., Sosa, M. A. G., Gasperi, R. D., Garcia, G. S. P., Perez, G. M., Abutarboush, R., Kawoos, U., Zhu, C. W., Janssen, W. G. M., Stone, J. R., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25021150 · Cited by 24 · see citing works
Niekisch, H., Steinhardt, J., Berghäuser, J., Bertazzoni, S., Kaschinski, E., Kasper, J., Kisse, M., Mitlöhner, J., Singh, J. B., Weber, J., et al. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.2499-18.2019 · Cited by 22 · see citing works
Zhang, H., Chen, G., Kuang, H., & Tsien, J. Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079454 · Cited by 21 · see citing works
Perineuronal Net Receptor PTPσ Regulates Retention of Memories
Lesnikova, A., Casarotto, P., Moliner, R., Fred, S. M., Biojone, C., & Castrén, E. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.672475 · Cited by 21 · see citing works
Jorgensen, E. T., Gonzalez, A. E., Harkness, J. H., Hegarty, D. M., Thakar, A., Burchi, D. J., Aadland, J. A., Aicher, S. A., Sorg, B. A., & Brown, T. E. (2020) · Addiction Biology · doi:10.1111/adb.12947 · Cited by 20 · see citing works
Neuronal Plasticity in the Juvenile and Adult Brain Regulated by the Extracellular Matrix
Happel, M. F. K., & Frischknecht, R. (2016) · InTech eBooks · doi:10.5772/62452 · Cited by 19 · see citing works
Griffiths, B. B., Sahbaie, P., Rao, A. N., Arvola, O., Xu, L., Liang, D., Ouyang, Y., Clark, J. D., Giffard, R. G., & Stary, C. M. (2019) · NeuroMolecular Medicine · doi:10.1007/s12017-019-08532-y · Cited by 18 · see citing works
Hyaluronidase reduced edema after experimental traumatic brain injury
Washington, P. M., Lee, C., Dwyer, M. K., Konofagou, E., Kernie, S., & Morrison, B. (2020) · Journal of Cerebral Blood Flow and Metabolism · doi:10.1177/0271678x19882780 · Cited by 12 · see citing works
El‐Tabbal, M., Niekisch, H., Henschke, J. U., Budinger, E., Frischknecht, R., Deliano, M., & Happel, M. F. K. (2021) · Communications Biology · doi:10.1038/s42003-021-01837-4 · Cited by 15 · see citing works
Anderson, M. D., Paylor, J. W., Scott, G. A., Greba, Q., Winship, I. R., & Howland, J. G. (2020) · Learning & Memory · doi:10.1101/lm.050245.119 · Cited by 16 · see citing works
Sun, W., Yang, Y., Chen, X., Cheng, Y., Li, X., & An, L. (2021) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.1c00081 · Cited by 15 · see citing works
Pesarico, A. P., Carceller, H., Guirado, R., Coviello, S., & Nácher, J. (2022) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2022.110512 · Cited by 16 · see citing works
Illa, M., Brito, V., Plà, L., Eixarch, E., Arbat‐Plana, A., Batallé, D., Muñoz‐Moreno, E., Crispi, F., Udina, E., Figueras, F., et al. (2017) · Fetal Diagnosis and Therapy · doi:10.1159/000481171 · Cited by 16 · see citing works
Amplified cortical neural responses as animals learn to use novel activity patterns
Akitake, B., Douglas, H. M., LaFosse, P. K., Beirán, M., Deveau, C. E., O’Rawe, J. F., Li, A. J., Ryan, L., Duffy, S. P., Zhou, Z., et al. (2023) · Current Biology · doi:10.1016/j.cub.2023.04.032 · Cited by 14 · see citing works
Do Perineuronal Nets Stabilize the Engram of a Synaptic Circuit?
Lev‐Ram, V., Lemieux, S. P., Deerinck, T. J., Bushong, E. A., Perez, A. J., Pritchard, D. R., Toyama, B. H., Park, S. K. R., McClatchy, D. B., Savas, J. N., et al. (2024) · Cells · doi:10.3390/cells13191627 · Cited by 15 · see citing works
Syková, E., Voříšek, I., Starčuk, Z., Kratochvíla, J., Pavlova, I., Ichikawa, Y., Kwok, J. C. F., Kmonı́čková, E., Myronchenko, S., Hromádka, T., et al. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0517-24.2024 · Cited by 13 · see citing works
Perineuronal nets in HVC and plasticity in male canary song
Cornez, G., Valle, S. R., dos Santos, E. B., Chiver, I., Müller, W., Ball, G. F., Cornil, C. A., & Balthazart, J. (2021) · PLoS ONE · doi:10.1371/journal.pone.0252560 · Cited by 13 · see citing works
Aberrant perineuronal nets alter spinal circuits, impair motor function, and increase plasticity
Sánchez-Ventura, J., Canal, C., Hidalgo, J., Penas, C., Navarro, X., Espin, A. T., Fouad, K., & Udina, E. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114220 · Cited by 12 · 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
Horii‐Hayashi, N., Sasagawa, T., & Nishi, M. (2016) · Anatomical Science International · doi:10.1007/s12565-016-0375-5 · Cited by 12 · see citing works
Chronic fluoxetine dissociates contextual from auditory fear memory
Sanders, J., & Mayford, M. R. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.08.057 · Cited by 11 · see citing works
Mueller-Buehl, C., Pakusch, J., Bader, V., Winklhofer, K. F., Mark, M. D., & Faissner, A. (2025) · Scientific Reports · doi:10.1038/s41598-025-89580-2 · Cited by 9 · see citing works
Liu, P., Zhao, Y., Xiong, W., Pan, Y., Zhu, M., & Zhu, X. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.12.024 · Cited by 9 · see citing works
Obray, J. D., Denton, A. R., Carroll-Deaton, J., Marquardt, K., Chandler, L. J., & Scofield, M. D. (2024) · Alcohol · doi:10.1016/j.alcohol.2024.12.006 · Cited by 8 · see citing works
Blanco, I., Deasy, S., Amontree, M., Gabriel, M., Caccavano, A., Vicini, S., Glasgow, E., & Conant, K. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03007-y · Cited by 4 · see citing works
Designing Tools for Assumption-Proof Brain Mapping
Marblestone, A. H., & Boyden, E. S. (2014) · Neuron · doi:10.1016/j.neuron.2014.09.004 · Cited by 7 · see citing works
Extracellular matrix controls neuronal features that mediate the persistence of fear
Pignataro, A., Pagano, R., Guarneri, G., Middei, S., & Ammassari‐Teule, M. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1440-0 · Cited by 7 · 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
Protocol for assessing the role of hippocampal perineuronal nets in aversive memories
Jovasevic, V., Zhang, H., Petrovic, Z., Cicvaric, A., & Radulović, J. (2021) · STAR Protocols · doi:10.1016/j.xpro.2021.100931 · Cited by 6 · see citing works
Protocols for the Evaluation of Neurodevelopmental Alterations in Rabbit Models In Vitro and In Vivo
Plà, L., Kühne, B. A., Guardia-Escote, L., Vázquez‐Aristizabal, P., Loreiro, C., Flick, B., Gratacós, E., Barenys, M., & Illa, M. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.918520 · Cited by 6 · see citing works
Perineuronal Nets: From Structure to Neurological Disorders
Li, X., Li, N., Zhao, P., Ren, D., Luo, B., & Zhou, T. G. (2023) · Current Medicinal Chemistry · doi:10.2174/0109298673258290231009111633 · Cited by 6 · see citing works
Khan, M. Z., Zheng, Y., Yuan, K., Han, Y., & Lü, L. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114230 · Cited by 5 · see citing works
Lemieux, S. P., Lev‐Ram, V., Tsien, R. Y., & Ellisman, M. H. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.29.569151 · Cited by 5 · see citing works
- Authors
- Hylin, M. J., Orsi, S. A., Moore, A. N., & Dash, P. K.
- Venue
- Learning & Memory
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2013-04-16
- Volume
- 20
- Issue
- 5
- Pages
- 267-273
- ISSN
- 1072-0502 (ISSN-L)
- 1549-5485
- PMC
- PMC3630486
- OpenAlex
- W1972625759
- Semantic Scholar
- 59ceada8f5c777f2b97f4aab91151e49b26422ea
- Cited by
- 143
- References
- 42
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 12 · 2023: 13 · 2022: 14 · 2021: 15 · 2020: 17 · 2019: 13 · 2018: 5 · 2017: 14 · 2016: 8 · 2015: 3 · 2014: 6 · 2013: 2
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Learning & Memory (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (R01MH072933, MH072933)
- National Institute of Neurological Disorders and Stroke (NS053588, R01NS053588)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- perineuronal nets, fear conditioning, hippocampus, medial prefrontal cortex, contextual fear memory, neuroplasticity, memory storage
- MeSH terms
- Animals, Conditioning, Classical, Extracellular Matrix, Fear, Hippocampus, Hyaluronoglucosaminidase, Male, Neurons, Prefrontal Cortex, Chondroitin ABC Lyase, Rats, Long-Evans, Rats
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