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Neural Plasticity
Volume 2018, Article ID 5735789, 13 pages
https://doi.org/10.1155/2018/5735789
Review Article

Proteolytic Remodeling of Perineuronal Nets: Effects on Synaptic Plasticity and Neuronal Population Dynamics

1Department of Neuroscience, Georgetown University Medical Center, 3800 Reservoir Rd NW, Washington, DC 20007, USA
2Interdisciplinary Program in Neuroscience, Georgetown University Medical Center, 3800 Reservoir Rd NW, Washington, DC 20007, USA
3Department of Pharmacology, Georgetown University Medical Center, 3800 Reservoir Rd NW, Washington, DC 20007, USA

Correspondence should be addressed to Katherine Conant; ude.nwotegroeg@48cek

Received 17 August 2017; Revised 3 November 2017; Accepted 27 November 2017; Published 4 February 2018

Academic Editor: Tomasz Wójtowicz

Copyright © 2018 P. Lorenzo Bozzelli et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. F. Happel and R. Frischknecht, “Neuronal plasticity in the juvenile and adult brain regulated by the extracellular matrix,” in Composition and Function of the Extracellular Matrix in the Human Body, F Travascio, Ed., INTECH, Rijeka, Croatia, 2016. View at Publisher · View at Google Scholar
  2. E. D. Gundelfinger, R. Frischknecht, D. Choquet, and M. Heine, “Converting juvenile into adult plasticity: a role for the brain’s extracellular matrix,” The European Journal of Neuroscience, vol. 31, no. 12, pp. 2156–2165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. G. W. Huntley, “Synaptic circuit remodelling by matrix metalloproteinases in health and disease,” Nature Reviews. Neuroscience, vol. 13, no. 11, pp. 743–757, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Sonderegger and K. Matsumoto-Miyai, “Activity-controlled proteolytic cleavage at the synapse,” Trends in Neurosciences, vol. 37, no. 8, pp. 413–423, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Conant, M. Allen, and S. T. Lim, “Activity dependent CAM cleavage and neurotransmission,” Frontiers in Cellular Neuroscience, vol. 9, p. 305, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Tsilibary, A. Tzinia, L. Radenovic et al., “Neural ECM proteases in learning and synaptic plasticity,” Progress in Brain Research, vol. 214, pp. 135–157, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. A. C. W. Smith, M. D. Scofield, and P. W. Kalivas, “The tetrapartite synapse: extracellular matrix remodeling contributes to corticoaccumbens plasticity underlying drug addiction,” Brain Research, vol. 1628, Part A, pp. 29–39, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Wlodarczyk, I. Mukhina, L. Kaczmarek, and A. Dityatev, “Extracellular matrix molecules, their receptors, and secreted proteases in synaptic plasticity,” Developmental Neurobiology, vol. 71, no. 11, pp. 1040–1053, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Dityatev, M. Schachner, and P. Sonderegger, “The dual role of the extracellular matrix in synaptic plasticity and homeostasis,” Nature Reviews Neuroscience, vol. 11, no. 11, pp. 735–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. B. A. Sorg, S. Berretta, J. M. Blacktop et al., “Casting a wide net: role of perineuronal nets in neural plasticity,” The Journal of Neuroscience, vol. 36, no. 45, pp. 11459–11468, 2016. View at Publisher · View at Google Scholar · View at Scopus
  11. J. C. F. Kwok, G. Dick, D. Wang, and J. W. Fawcett, “Extracellular matrix and perineuronal nets in CNS repair,” Developmental Neurobiology, vol. 71, no. 11, pp. 1073–1089, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Berretta, H. Pantazopoulos, M. Markota, C. Brown, and E. T. Batzianouli, “Losing the sugar coating: potential impact of perineuronal net abnormalities on interneurons in schizophrenia,” Schizophrenia Research, vol. 167, no. 1-3, pp. 18–27, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Slaker, J. M. Blacktop, and B. A. Sorg, “Caught in the net: perineuronal nets and addiction,” Neural Plasticity, vol. 2016, Article ID 7538208, 8 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  14. L. W. Lau, R. Cua, M. B. Keough, S. Haylock-Jacobs, and V. W. Yong, “Pathophysiology of the brain extracellular matrix: a new target for remyelination,” Nature Reviews Neuroscience, vol. 14, no. 10, pp. 722–729, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Weber, U. Bartsch, M. N. Rasband et al., “Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS,” The Journal of Neuroscience, vol. 19, no. 11, pp. 4245–4262, 1999. View at Google Scholar
  16. A. Haunsø, M. Ibrahim, U. Bartsch, M. Letiembre, M. R. Celio, and P. A. Menoud, “Morphology of perineuronal nets in tenascin-R and parvalbumin single and double knockout mice,” Brain Research, vol. 864, no. 1, pp. 142–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. K. K. Lensjo, A. C. Christensen, S. Tennoe, M. Fyhn, and T. Hafting, “Differential expression and cell-type specificity of perineuronal nets in hippocampus, medial entorhinal cortex, and visual cortex examined in the rat and mouse,” eNeuro, vol. 4, no. 3, article ENEURO.0379-16, 2017. View at Publisher · View at Google Scholar
  18. A. Alpar, U. Gartner, W. Hartig, and G. Bruckner, “Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat,” Brain Research, vol. 1120, no. 1, pp. 13–22, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Vedunova, T. Sakharnova, E. Mitroshina et al., “Seizurelike activity in hyaluronidase-treated dissociated hippocampal cultures,” Frontiers in Cellular Neuroscience, vol. 7, p. 149, 2013. View at Google Scholar
  20. G. Seeger, K. Brauer, W. Härtig, and G. Brückner, “Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry,” Neuroscience, vol. 58, no. 2, pp. 371–388, 1994. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Bertolotto, E. Manzardo, and R. Guglielmone, “Immunohistochemical mapping of perineuronal nets containing chondroitin unsulfate proteoglycan in the rat central nervous system,” Cell and Tissue Research, vol. 283, no. 2, pp. 283–295, 1996. View at Publisher · View at Google Scholar · View at Scopus
  22. M. R. Celio, “Calbindin D-28k and parvalbumin in the rat nervous system,” Neuroscience, vol. 35, no. 2, pp. 375–475, 1990. View at Publisher · View at Google Scholar · View at Scopus
  23. D. Carulli, K. E. Rhodes, D. J. Brown et al., “Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components,” The Journal of Comparative Neurology, vol. 494, no. 4, pp. 559–577, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. K. E. Carstens, M. L. Phillips, L. Pozzo-Miller, R. J. Weinberg, and S. M. Dudek, “Perineuronal nets suppress plasticity of excitatory synapses on CA2 pyramidal neurons,” The Journal of Neuroscience, vol. 36, no. 23, pp. 6312–6320, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Lee, C. A. Leamey, and A. Sawatari, “Perineuronal nets play a role in regulating striatal function in the mouse,” PLoS One, vol. 7, no. 3, article e32747, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Cornez, F. N. Madison, A. Van der Linden et al., “Perineuronal nets and vocal plasticity in songbirds: a proposed mechanism to explain the difference between closed-ended and open-ended learning,” Developmental Neurobiology, vol. 77, no. 8, pp. 975–994, 2017. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Dityatev, G. Bruckner, G. Dityateva, J. Grosche, R. Kleene, and M. Schachner, “Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets,” Developmental Neurobiology, vol. 67, no. 5, pp. 570–588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. K. A. Giamanco and R. T. Matthews, “Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix,” Neuroscience, vol. 218, pp. 367–384, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Guimaraes, S. Zaremba, and S. Hockfield, “Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301,” The Journal of Neuroscience, vol. 10, no. 9, pp. 3014–3024, 1990. View at Google Scholar
  30. P. A. McRae, M. M. Rocco, G. Kelly, J. C. Brumberg, and R. T. Matthews, “Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex,” The Journal of Neuroscience, vol. 27, no. 20, pp. 5405–5413, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Ye and Q. L. Miao, “Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex,” Matrix Biology, vol. 32, no. 6, pp. 352–363, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Sugiyama, A. A. Di Nardo, S. Aizawa et al., “Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity,” Cell, vol. 134, no. 3, pp. 508–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Spatazza, H. H. C. Lee, A. A. Di Nardo et al., “Choroid-plexus-derived Otx2 homeoprotein constrains adult cortical plasticity,” Cell Reports, vol. 3, no. 6, pp. 1815–1823, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Beurdeley, J. Spatazza, H. H. C. Lee et al., “Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex,” The Journal of Neuroscience, vol. 32, no. 27, pp. 9429–9437, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. H. H. C. Lee, C. Bernard, Z. Ye et al., “Genetic Otx2 mis-localization delays critical period plasticity across brain regions,” Molecular Psychiatry, vol. 22, no. 5, p. 785, 2017. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Li, T. Asteriou, B. Bernert, C. H. Heldin, and P. Heldin, “Growth factor regulation of hyaluronan synthesis and degradation in human dermal fibroblasts: importance of hyaluronan for the mitogenic response of PDGF-BB,” The Biochemical Journal, vol. 404, no. 2, pp. 327–336, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. T. K. Hensch, “Controlling the critical period,” Neuroscience Research, vol. 47, no. 1, pp. 17–22, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Miyata and H. Kitagawa, “Mechanisms for modulation of neural plasticity and axon regeneration by chondroitin sulphate,” Journal of Biochemistry, vol. 157, no. 1, pp. 13–22, 2015. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J. W. Fawcett, and L. Maffei, “Reactivation of ocular dominance plasticity in the adult visual cortex,” Science, vol. 298, no. 5596, pp. 1248–1251, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Antonini and M. Stryker, “Rapid remodeling of axonal arbors in the visual cortex,” Science, vol. 260, no. 5115, pp. 1819–1821, 1993. View at Publisher · View at Google Scholar
  41. L. de Vivo, S. Landi, M. Panniello et al., “Extracellular matrix inhibits structural and functional plasticity of dendritic spines in the adult visual cortex,” Nature Communications, vol. 4, p. 1484, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Gogolla, P. Caroni, A. Luthi, and C. Herry, “Perineuronal nets protect fear memories from erasure,” Science, vol. 325, no. 5945, pp. 1258–1261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Simonetti, H. Lee, M. Bourke, C. A. Leamey, and A. Sawatari, “Enrichment from birth accelerates the functional and cellular development of a motor control area in the mouse,” PLoS One, vol. 4, no. 8, article e6780, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Nishijima, M. Kawakami, and I. Kita, “A bout of treadmill exercise increases matrix metalloproteinase-9 activity in the rat hippocampus,” Neuroscience Letters, vol. 594, pp. 144–149, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. V. Tamasi, P. Petschner, C. Adori et al., “Transcriptional evidence for the role of chronic venlafaxine treatment in neurotrophic signaling and neuroplasticity including also glutamatergic [corrected] - and insulin-mediated neuronal processes,” PLoS One, vol. 9, no. 11, article e113662, 2014. View at Publisher · View at Google Scholar · View at Scopus
  46. M. J. Vegh, C. M. Heldring, W. Kamphuis et al., “Reducing hippocampal extracellular matrix reverses early memory deficits in a mouse model of Alzheimer’s disease,” Acta Neuropathologica Communications, vol. 2, no. 1, p. 76, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. K. K. Lensjo, M. E. Lepperod, G. Dick, T. Hafting, and M. Fyhn, “Removal of perineuronal nets unlocks juvenile plasticity through network mechanisms of decreased inhibition and increased gamma activity,” The Journal of Neuroscience, vol. 37, no. 5, pp. 1269–1283, 2017. View at Publisher · View at Google Scholar · View at Scopus
  48. Z. Y. Sun, P. L. Bozzelli, A. Caccavano et al., “Disruption of perineuronal nets increases the frequency of sharp wave ripple events,” Hippocampus, vol. 28, no. 1, pp. 42–52, 2018. View at Publisher · View at Google Scholar
  49. T. H. Wen, S. Afroz, S. M. Reinhard et al., “Genetic reduction of matrix metalloproteinase-9 promotes formation of perineuronal nets around parvalbumin-expressing interneurons and normalizes auditory cortex responses in developing Fmr1knock-out mice,” Cerebral Cortex, vol. 13, pp. 1–14, 2017. View at Publisher · View at Google Scholar
  50. S. Oray, A. Majewska, and M. Sur, “Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation,” Neuron, vol. 44, no. 6, pp. 1021–1030, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. M. W. Lark, H. Williams, L. A. Hoernner et al., “Quantification of a matrix metalloproteinase-generated aggrecan G1 fragment using monospecific anti-peptide serum,” Biochemical Journal, vol. 307, no. 1, pp. 245–252, 1995. View at Publisher · View at Google Scholar
  52. E. C. Arner, M. A. Pratta, C. P. Decicco et al., “Aggrecanase: a target for the design of inhibitors of cartilage degradation,” Annals of the New York Academy of Sciences, vol. 878, pp. 92–107, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. M. L. Lemons, J. D. Sandy, D. K. Anderson, and D. R. Howland, “Intact aggrecan and fragments generated by both aggrecanse and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury,” The Journal of Neuroscience, vol. 21, no. 13, pp. 4772–4781, 2001. View at Google Scholar
  54. C. B. Little, C. R. Flannery, C. E. Hughes et al., “Aggrecanase versus matrix metalloproteinases in the catabolism of the interglobular domain of aggrecan in vitro,” Biochemical Journal, vol. 344, Part 1, pp. 61–68, 1999. View at Publisher · View at Google Scholar
  55. M. Durigova, H. Nagase, J. S. Mort, and P. J. Roughley, “MMPs are less efficient than ADAMTS5 in cleaving aggrecan core protein,” Matrix Biology, vol. 30, no. 2, pp. 145–153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Nakamura, Y. Fujii, I. Inoki et al., “Brevican is degraded by matrix metalloproteinases and aggrecanase-1 (ADAMTS4) at different sites,” The Journal of Biological Chemistry, vol. 275, no. 49, pp. 38885–38890, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. J. Mayer, M. G. Hamel, and P. E. Gottschall, “Evidence for proteolytic cleavage of brevican by the ADAMTSs in the dentate gyrus after excitotoxic lesion of the mouse entorhinal cortex,” BMC Neuroscience, vol. 6, no. 1, p. 52, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. R. T. Matthews, S. C. Gary, C. Zerillo et al., “Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member,” The Journal of Biological Chemistry, vol. 275, no. 30, pp. 22695–22703, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Nakada, H. Miyamori, D. Kita et al., “Human glioblastomas overexpress ADAMTS-5 that degrades brevican,” Acta Neuropathologica, vol. 110, no. 3, pp. 239–246, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. J. M. Ajmo, A. K. Eakin, M. G. Hamel, and P. E. Gottschall, “Discordant localization of WFA reactivity and brevican/ADAMTS-derived fragment in rodent brain,” BMC Neuroscience, vol. 9, p. 14, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Demircan, V. Topcu, T. Takigawa et al., “ADAMTS4 and ADAMTS5 knockout mice are protected from versican but not aggrecan or brevican proteolysis during spinal cord injury,” BioMed Research International, vol. 2014, Article ID 693746, 8 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. M. D. Howell and P. E. Gottschall, “Lectican proteoglycans, their cleaving metalloproteinases, and plasticity in the central nervous system extracellular microenvironment,” Neuroscience, vol. 217, pp. 6–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Levy, J. M. Brooks, J. Chen, J. Su, and M. A. Fox, “Cell-specific and developmental expression of lectican-cleaving proteases in mouse hippocampus and neocortex,” The Journal of Comparative Neurology, vol. 523, no. 4, pp. 629–648, 2015. View at Publisher · View at Google Scholar · View at Scopus
  64. U. Rauch, P. Gao, A. Janetzko et al., “Isolation and characterization of developmentally regulated chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies,” The Journal of Biological Chemistry, vol. 266, no. 22, pp. 14785–14801, 1991. View at Google Scholar
  65. R. Lin, T. W. Rosahl, P. J. Whiting, J. W. Fawcett, and J. C. F. Kwok, “6-Sulphated chondroitins have a positive influence on axonal regeneration,” PLoS One, vol. 6, no. 7, article e21499, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. S. Miyata, Y. Komatsu, Y. Yoshimura, C. Taya, and H. Kitagawa, “Persistent cortical plasticity by upregulation of chondroitin 6-sulfation,” Nature Neuroscience, vol. 15, no. 3, pp. 414–422, 2012. View at Publisher · View at Google Scholar · View at Scopus
  67. H. Wang, Y. Katagiri, T. E. McCann et al., “Chondroitin-4-sulfation negatively regulates axonal guidance and growth,” Journal of Cell Science, vol. 121, Part 18, pp. 3083–3091, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. S. Miyata and H. Kitagawa, “Chondroitin 6-sulfation regulates perineuronal net formation by controlling the stability of aggrecan,” Neural Plasticity, vol. 2016, Article ID 1305801, 13 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Foscarin, R. Raha-Chowdhury, J. W. Fawcett, and J. C. F. Kwok, “Brain ageing changes proteoglycan sulfation, rendering perineuronal nets more inhibitory,” Aging, vol. 9, no. 6, pp. 1607–1622, 2017. View at Publisher · View at Google Scholar
  70. E. K. Rankin-Gee, P. A. McRae, E. Baranov, S. Rogers, L. Wandrey, and B. E. Porter, “Perineuronal net degradation in epilepsy,” Epilepsia, vol. 56, no. 7, pp. 1124–1133, 2015. View at Publisher · View at Google Scholar · View at Scopus
  71. T. H. Hsieh, H. H. Lee, M. Q. Hameed, A. Pascual-Leone, T. K. Hensch, and A. Rotenberg, “Trajectory of parvalbumin cell impairment and loss of cortical inhibition in traumatic brain injury,” Cerebral Cortex, vol. 27, no. 12, pp. 5509–5524, 2017. View at Publisher · View at Google Scholar
  72. P. V. Belichenko, J. Miklossy, and M. R. Celio, “HIV-I induced destruction of neocortical extracellular matrix components in AIDS victims,” Neurobiology of Disease, vol. 4, no. 3-4, pp. 301–310, 1997. View at Publisher · View at Google Scholar · View at Scopus
  73. C. Hobohm, A. Gunther, J. Grosche, S. Rossner, D. Schneider, and G. Bruckner, “Decomposition and long-lasting downregulation of extracellular matrix in perineuronal nets induced by focal cerebral ischemia in rats,” Journal of Neuroscience Research, vol. 80, no. 4, pp. 539–548, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. R. Guirado, M. Perez-Rando, D. Sanchez-Matarredona, E. Castren, and J. Nacher, “Chronic fluoxetine treatment alters the structure, connectivity and plasticity of cortical interneurons,” The International Journal of Neuropsychopharmacology, vol. 17, no. 10, pp. 1635–1646, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Kovalevich and D. Langford, “Neuronal toxicity in HIV CNS disease,” Future Virology, vol. 7, no. 7, pp. 687–698, 2012. View at Publisher · View at Google Scholar · View at Scopus
  76. K. Conant, J. C. McArthur, D. E. Griffin, L. Sjulson, L. M. Wahl, and D. N. Irani, “Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia,” Annals of Neurology, vol. 46, no. 3, pp. 391–398, 1999. View at Publisher · View at Google Scholar
  77. A. B. Ragin, Y. Wu, R. Ochs et al., “Serum matrix metalloproteinase levels correlate with brain injury in human immunodeficiency virus infection,” Journal of Neurovirology, vol. 15, no. 3, pp. 275–281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  78. B. Sporer, R. Paul, U. Koedel et al., “Presence of matrix metalloproteinase-9 activity in the cerebrospinal fluid of human immunodeficiency virus—infected patients,” The Journal of Infectious Diseases, vol. 178, no. 3, pp. 854–857, 1998. View at Publisher · View at Google Scholar
  79. R. Suryadevara, S. Holter, K. Borgmann et al., “Regulation of tissue inhibitor of metalloproteinase-1 by astrocytes: links to HIV-1 dementia,” Glia, vol. 44, no. 1, pp. 47–56, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. G. M. Liuzzi, C. M. Mastroianni, M. P. Santacroce et al., “Increased activity of matrix metalloproteinases in the cerebrospinal fluid of patients with HIV-associated neurological diseases,” Journal of Neurovirology, vol. 6, no. 2, pp. 156–163, 2000. View at Publisher · View at Google Scholar
  81. N. E. J. Berman, J. K. Marcario, C. Yong et al., “Microglial activation and neurological symptoms in the SIV model of NeuroAIDS: association of MHC-II and MMP-9 expression with behavioral deficits and evoked potential changes,” Neurobiology of Disease, vol. 6, no. 6, pp. 486–498, 1999. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Medina-Flores, G. Wang, S. J. Bissel, M. Murphey-Corb, and C. A. Wiley, “Destruction of extracellular matrix proteoglycans is pervasive in simian retroviral neuroinfection,” Neurobiology of Disease, vol. 16, no. 3, pp. 604–616, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. W. D. Marks, J. J. Paris, C. J. Schier et al., “HIV-1 Tat causes cognitive deficits and selective loss of parvalbumin, somatostatin, and neuronal nitric oxide synthase expressing hippocampal CA1 interneuron subpopulations,” Journal of Neurovirology, vol. 22, no. 6, pp. 747–762, 2016. View at Publisher · View at Google Scholar · View at Scopus
  84. R. M. Lafrenie, L. M. Wahl, J. S. Epstein, I. K. Hewlett, K. M. Yamada, and S. Dhawan, “HIV-1-Tat modulates the function of monocytes and alters their interactions with microvessel endothelial cells. A mechanism of HIV pathogenesis,” The Journal of Immunology, vol. 156, no. 4, pp. 1638–1645, 1996. View at Google Scholar
  85. A. Kumar, S. Dhawan, A. Mukhopadhyay, and B. B. Aggarwal, “Human immunodeficiency virus-1-tat induces matrix metalloproteinase-9 in monocytes through protein tyrosine phosphatase-mediated activation of nuclear transcription factor NF-κB,” FEBS Letters, vol. 462, no. 1-2, pp. 140–144, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. M. M. Verbeek, I. Otte-Holler, J. van den Born et al., “Agrin is a major heparan sulfate proteoglycan accumulating in Alzheimer’s disease brain,” The American Journal of Pathology, vol. 155, no. 6, pp. 2115–2125, 1999. View at Publisher · View at Google Scholar
  87. J. van Horssen, I. Otte-Holler, G. David et al., “Heparan sulfate proteoglycan expression in cerebrovascular amyloid β deposits in Alzheimer’s disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains,” Acta Neuropathologica, vol. 102, no. 6, pp. 604–614, 2001. View at Publisher · View at Google Scholar
  88. D. A. DeWitt, J. Silver, D. R. Canning, and G. Perry, “Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer’s disease,” Experimental Neurology, vol. 121, no. 2, pp. 149–152, 1993. View at Publisher · View at Google Scholar · View at Scopus
  89. M. D. Howell, L. A. Bailey, M. A. Cozart, B. M. Gannon, and P. E. Gottschall, “Hippocampal administration of chondroitinase ABC increases plaque-adjacent synaptic marker and diminishes amyloid burden in aged APPswe/PS1dE9 mice,” Acta Neuropathologica Communications, vol. 3, no. 1, p. 54, 2015. View at Publisher · View at Google Scholar
  90. S. Baig, G. K. Wilcock, and S. Love, “Loss of perineuronal net N-acetylgalactosamine in Alzheimer’s disease,” Acta Neuropathologica, vol. 110, no. 4, pp. 393–401, 2005. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Morawski, G. Bruckner, C. Jager, G. Seeger, R. T. Matthews, and T. Arendt, “Involvement of perineuronal and perisynaptic extracellular matrix in Alzheimer’s disease neuropathology,” Brain Pathology, vol. 22, no. 4, pp. 547–561, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. G. Bruckner, D. Hausen, W. Hartig, M. Drlicek, T. Arendt, and K. Brauer, “Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer’s disease,” Neuroscience, vol. 92, no. 3, pp. 791–805, 1999. View at Publisher · View at Google Scholar · View at Scopus
  93. W. Hartig, C. Klein, K. Brauer et al., “Hyperphosphorylated protein tau is restricted to neurons devoid of perineuronal nets in the cortex of aged bison,” Neurobiology of Aging, vol. 22, no. 1, pp. 25–33, 2001. View at Publisher · View at Google Scholar · View at Scopus
  94. S. Miyata, Y. Nishimura, and T. Nakashima, “Perineuronal nets protect against amyloid β-protein neurotoxicity in cultured cortical neurons,” Brain Research, vol. 1150, pp. 200–206, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Morawski, G. Bruckner, C. Jager, G. Seeger, and T. Arendt, “Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer’s disease,” Neuroscience, vol. 169, no. 3, pp. 1347–1363, 2010. View at Publisher · View at Google Scholar · View at Scopus
  96. P. A. McRae, E. Baranov, S. L. Rogers, and B. E. Porter, “Persistent decrease in multiple components of the perineuronal net following status epilepticus,” The European Journal of Neuroscience, vol. 36, no. 11, pp. 3471–3482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. P. A. McRae, E. Baranov, S. Sarode, A. R. Brooks-Kayal, and B. E. Porter, “Aggrecan expression, a component of the inhibitory interneuron perineuronal net, is altered following an early-life seizure,” Neurobiology of Disease, vol. 39, no. 3, pp. 439–448, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. F. Matsui, S. Kawashima, T. Shuo et al., “Transient expression of juvenile-type neurocan by reactive astrocytes in adult rat brains injured by kainate-induced seizures as well as surgical incision,” Neuroscience, vol. 112, no. 4, pp. 773–781, 2002. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Okamoto, J. Sakiyama, S. Mori et al., “Kainic acid-induced convulsions cause prolonged changes in the chondroitin sulfate proteoglycans neurocan and phosphacan in the limbic structures,” Experimental Neurology, vol. 184, no. 1, pp. 179–195, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. N. Heck, J. Garwood, J. P. Loeffler, Y. Larmet, and A. Faissner, “Differential upregulation of extracellular matrix molecules associated with the appearance of granule cell dispersion and mossy fiber sprouting during epileptogenesis in a murine model of temporal lobe epilepsy,” Neuroscience, vol. 129, no. 2, pp. 309–324, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. B. Scheffler, A. Faissner, H. Beck et al., “Hippocampal loss of tenascin boundaries in Ammon’s horn sclerosis,” Glia, vol. 19, no. 1, pp. 35–46, 1997. View at Publisher · View at Google Scholar
  102. M. G. Naffah-Mazzacoratti, G. A. Arganaraz, M. A. Porcionatto et al., “Selective alterations of glycosaminoglycans synthesis and proteoglycan expression in rat cortex and hippocampus in pilocarpine-induced epilepsy,” Brain Research Bulletin, vol. 50, no. 4, pp. 229–239, 1999. View at Publisher · View at Google Scholar · View at Scopus
  103. S. Kurazono, M. Okamoto, J. Sakiyama et al., “Expression of brain specific chondroitin sulfate proteoglycans, neurocan and phosphacan, in the developing and adult hippocampus of Ihara’s epileptic rats,” Brain Research, vol. 898, no. 1, pp. 36–48, 2001. View at Publisher · View at Google Scholar · View at Scopus
  104. A. Szklarczyk, J. Lapinska, M. Rylski, R. D. McKay, and L. Kaczmarek, “Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus,” The Journal of Neuroscience, vol. 22, no. 3, pp. 920–930, 2002. View at Google Scholar
  105. F. A. Konopacki, M. Rylski, E. Wilczek et al., “Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA,” Neuroscience, vol. 150, no. 1, pp. 31–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. N. Suenaga, T. Ichiyama, M. Kubota, H. Isumi, J. Tohyama, and S. Furukawa, “Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures,” Journal of the Neurological Sciences, vol. 266, no. 1-2, pp. 126–130, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. G. M. Wilczynski, F. A. Konopacki, E. Wilczek et al., “Important role of matrix metalloproteinase 9 in epileptogenesis,” The Journal of Cell Biology, vol. 180, no. 5, pp. 1021–1035, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. D. Dubey, P. A. McRae, E. K. Rankin-Gee et al., “Increased metalloproteinase activity in the hippocampus following status epilepticus,” Epilepsy Research, vol. 132, pp. 50–58, 2017. View at Publisher · View at Google Scholar · View at Scopus
  109. E. Pollock, M. Everest, A. Brown, and M. O. Poulter, “Metalloproteinase inhibition prevents inhibitory synapse reorganization and seizure genesis,” Neurobiology of Disease, vol. 70, pp. 21–31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  110. W. Yuan, R. T. Matthews, J. D. Sandy, and P. E. Gottschall, “Association between protease-specific proteolytic cleavage of brevican and synaptic loss in the dentate gyrus of kainate-treated rats,” Neuroscience, vol. 114, no. 4, pp. 1091–1101, 2002. View at Publisher · View at Google Scholar · View at Scopus
  111. M. Karetko-Sysa, J. Skangiel-Kramska, and D. Nowicka, “Disturbance of perineuronal nets in the perilesional area after photothrombosis is not associated with neuronal death,” Experimental Neurology, vol. 231, no. 1, pp. 113–126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  112. S. Thomas Carmichael, L. Wei, C. M. Rovainen, and T. A. Woolsey, “New patterns of intracortical projections after focal cortical stroke,” Neurobiology of Disease, vol. 8, no. 5, pp. 910–922, 2001. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Madinier, M. J. Quattromani, C. Sjolund, K. Ruscher, and T. Wieloch, “Enriched housing enhances recovery of limb placement ability and reduces aggrecan-containing perineuronal nets in the rat somatosensory cortex after experimental stroke,” PLoS One, vol. 9, no. 3, article e93121, 2014. View at Publisher · View at Google Scholar · View at Scopus
  114. N. G. Harris, Y. A. Mironova, D. A. Hovda, and R. L. Sutton, “Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury,” Journal of Neuropathology and Experimental Neurology, vol. 69, no. 2, pp. 139–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  115. S. Y. Kim, V. V. Senatorov Jr, C. S. Morrissey et al., “TGFβ signaling is associated with changes in inflammatory gene expression and perineuronal net degradation around inhibitory neurons following various neurological insults,” Scientific Reports, vol. 7, no. 1, p. 7711, 2017. View at Publisher · View at Google Scholar
  116. H. Pantazopoulos and S. Berretta, “In sickness and in health: perineuronal nets and synaptic plasticity in psychiatric disorders,” Neural Plasticity, vol. 2016, Article ID 9847696, 23 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  117. H. Pantazopoulos, M. Markota, F. Jaquet et al., “Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala,” Translational Psychiatry, vol. 5, no. 1, article e496, 2015. View at Publisher · View at Google Scholar · View at Scopus
  118. S. Sabunciyan, R. Yolken, C. M. Ragan et al., “Polymorphisms in the homeobox gene OTX2 may be a risk factor for bipolar disorder,” American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, vol. 144B, no. 8, pp. 1083–1086, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. X. Miró, S. Meier, M. L. Dreisow et al., “Studies in humans and mice implicate neurocan in the etiology of mania,” The American Journal of Psychiatry, vol. 169, no. 9, pp. 982–990, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. K. Ohira, R. Takeuchi, T. Iwanaga, and T. Miyakawa, “Chronic fluoxetine treatment reduces parvalbumin expression and perineuronal nets in gamma-aminobutyric acidergic interneurons of the frontal cortex in adult mice,” Molecular Brain, vol. 6, no. 1, p. 43, 2013. View at Publisher · View at Google Scholar · View at Scopus
  121. J. Umemori, F. Winkel, E. Castren, and N. N. Karpova, “Distinct effects of perinatal exposure to fluoxetine or methylmercury on parvalbumin and perineuronal nets, the markers of critical periods in brain development,” International Journal of Developmental Neuroscience, vol. 44, pp. 55–64, 2015. View at Publisher · View at Google Scholar · View at Scopus
  122. Y. Li, J. Partridge, C. Berger, A. Sepulveda-Rodriguez, S. Vicini, and K. Conant, “Dopamine increases NMDA-stimulated calcium flux in striatopallidal neurons through a matrix metalloproteinase-dependent mechanism,” The European Journal of Neuroscience, vol. 43, no. 2, pp. 194–203, 2016. View at Publisher · View at Google Scholar · View at Scopus
  123. E. V. Yang, A. K. Sood, M. Chen et al., “Norepinephrine up-regulates the expression of vascular endothelial growth factor, matrix metalloproteinase (MMP)-2, and MMP-9 in nasopharyngeal carcinoma tumor cells,” Cancer Research, vol. 66, no. 21, pp. 10357–10364, 2006. View at Publisher · View at Google Scholar · View at Scopus
  124. L. W. Yick, K. F. So, P. T. Cheung, and W. T. Wu, “Lithium chloride reinforces the regeneration-promoting effect of chondroitinase ABC on rubrospinal neurons after spinal cord injury,” Journal of Neurotrauma, vol. 21, no. 7, pp. 932–943, 2004. View at Publisher · View at Google Scholar · View at Scopus
  125. J. P. Frederick, A. T. Tafari, S. M. Wu et al., “A role for a lithium-inhibited Golgi nucleotidase in skeletal development and sulfation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 33, pp. 11605–11612, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. E. Favuzzi, A. Marques-Smith, R. Deogracias et al., “Activity-dependent gating of parvalbumin interneuron function by the perineuronal net protein brevican,” Neuron, vol. 95, no. 3, pp. 639–655.e10, 2017. View at Publisher · View at Google Scholar
  127. S. M. Thompson, A. J. Kallarackal, M. D. Kvarta, A. M. Van Dyke, T. A. LeGates, and X. Cai, “An excitatory synapse hypothesis of depression,” Trends in Neurosciences, vol. 38, no. 5, pp. 279–294, 2015. View at Publisher · View at Google Scholar · View at Scopus
  128. M. Morawski, T. Reinert, W. Meyer-Klaucke et al., “Ion exchanger in the brain: quantitative analysis of perineuronally fixed anionic binding sites suggests diffusion barriers with ion sorting properties,” Scientific Reports, vol. 5, no. 1, article 16471, 2015. View at Publisher · View at Google Scholar · View at Scopus
  129. T. S. Balmer, “Perineuronal nets enhance the excitability of fast-spiking neurons,” eNeuro, vol. 3, no. 4, article ENEURO.0112-16.2016, 2016. View at Publisher · View at Google Scholar
  130. W. Hartig, A. Derouiche, K. Welt et al., “Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations,” Brain Research, vol. 842, no. 1, pp. 15–29, 1999. View at Publisher · View at Google Scholar · View at Scopus
  131. G. Bruckner, K. Brauer, W. Hartig et al., “Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain,” Glia, vol. 8, no. 3, pp. 183–200, 1993. View at Publisher · View at Google Scholar · View at Scopus
  132. M. Morawski, M. K. Bruckner, P. Riederer, G. Bruckner, and T. Arendt, “Perineuronal nets potentially protect against oxidative stress,” Experimental Neurology, vol. 188, no. 2, pp. 309–315, 2004. View at Publisher · View at Google Scholar · View at Scopus
  133. N. Canas, T. Valero, M. Villarroya et al., “Chondroitin sulfate protects SH-SY5Y cells from oxidative stress by inducing heme oxygenase-1 via phosphatidylinositol 3-kinase/Akt,” The Journal of Pharmacology and Experimental Therapeutics, vol. 323, no. 3, pp. 946–953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. N. G. Harris, M. S. M. Nogueira, D. R. Verley, and R. L. Sutton, “Chondroitinase enhances cortical map plasticity and increases functionally active sprouting axons after brain injury,” Journal of Neurotrauma, vol. 30, no. 14, pp. 1257–1269, 2013. View at Publisher · View at Google Scholar · View at Scopus
  135. J. M. Massey, C. H. Hubscher, M. R. Wagoner et al., “Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury,” The Journal of Neuroscience, vol. 26, no. 16, pp. 4406–4414, 2006. View at Publisher · View at Google Scholar · View at Scopus
  136. M. Blosa, C. Bursch, S. Weigel et al., “Reorganization of synaptic connections and perineuronal nets in the deep cerebellar nuclei of Purkinje cell degeneration mutant mice,” Neural Plasticity, vol. 2016, Article ID 2828536, 17 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  137. F. Donato, S. B. Rompani, and P. Caroni, “Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning,” Nature, vol. 504, no. 7479, pp. 272–276, 2013. View at Publisher · View at Google Scholar · View at Scopus
  138. J. J. Letzkus, S. B. E. Wolff, and A. Lüthi, “Disinhibition, a circuit mechanism for associative learning and memory,” Neuron, vol. 88, no. 2, pp. 264–276, 2015. View at Publisher · View at Google Scholar · View at Scopus
  139. R. Frischknecht, M. Heine, D. Perrais, C. I. Seidenbecher, D. Choquet, and E. D. Gundelfinger, “Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity,” Nature Neuroscience, vol. 12, no. 7, pp. 897–904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  140. M. Slaker, L. Churchill, R. P. Todd et al., “Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory,” The Journal of Neuroscience, vol. 35, no. 10, pp. 4190–4202, 2015. View at Publisher · View at Google Scholar · View at Scopus
  141. F. Morellini, E. Sivukhina, L. Stoenica et al., “Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus,” Cerebral Cortex, vol. 20, no. 11, pp. 2712–2727, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. D. Carulli, T. Pizzorusso, J. C. F. Kwok et al., “Animals lacking link protein have attenuated perineuronal nets and persistent plasticity,” Brain, vol. 133, no. 8, pp. 2331–2347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  143. M. F. K. Happel, H. Niekisch, L. L. Castiblanco Rivera, F. W. Ohl, M. Deliano, and R. Frischknecht, “Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 7, pp. 2800–2805, 2014. View at Publisher · View at Google Scholar · View at Scopus
  144. G. Buzsaki and A. Draguhn, “Neuronal oscillations in cortical networks,” Science, vol. 304, no. 5679, pp. 1926–1929, 2004. View at Publisher · View at Google Scholar · View at Scopus
  145. T. F. Freund and I. Katona, “Perisomatic inhibition,” Neuron, vol. 56, no. 1, pp. 33–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  146. T. Klausberger and P. Somogyi, “Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations,” Science, vol. 321, no. 5885, pp. 53–57, 2008. View at Publisher · View at Google Scholar · View at Scopus
  147. A. Racz, A. A. Ponomarenko, E. C. Fuchs, and H. Monyer, “Augmented hippocampal ripple oscillations in mice with reduced fast excitation onto parvalbumin-positive cells,” The Journal of Neuroscience, vol. 29, no. 8, pp. 2563–2568, 2009. View at Publisher · View at Google Scholar · View at Scopus
  148. G. Buzsaki, “Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning,” Hippocampus, vol. 25, no. 10, pp. 1073–1188, 2015. View at Publisher · View at Google Scholar · View at Scopus
  149. M. Bartos, I. Vida, and P. Jonas, “Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks,” Nature Reviews. Neuroscience, vol. 8, no. 1, pp. 45–56, 2007. View at Publisher · View at Google Scholar · View at Scopus
  150. T. Korotkova, E. C. Fuchs, A. Ponomarenko, J. von Engelhardt, and H. Monyer, “NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory,” Neuron, vol. 68, no. 3, pp. 557–569, 2010. View at Publisher · View at Google Scholar · View at Scopus
  151. A. Khalid, B. S. Kim, B. A. Seo et al., “Gamma oscillation in functional brain networks is involved in the spontaneous remission of depressive behavior induced by chronic restraint stress in mice,” BMC Neuroscience, vol. 17, no. 1, p. 4, 2016. View at Publisher · View at Google Scholar · View at Scopus
  152. M. Wilson and B. McNaughton, “Reactivation of hippocampal ensemble memories during sleep,” Science, vol. 265, no. 5172, pp. 676–679, 1994. View at Publisher · View at Google Scholar
  153. G. Buzsaki, “Hippocampal sharp waves: their origin and significance,” Brain Research, vol. 398, no. 2, pp. 242–252, 1986. View at Publisher · View at Google Scholar · View at Scopus
  154. J. O'Keefe and J. Dostrovsky, “The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat,” Brain Research, vol. 34, no. 1, pp. 171–175, 1971. View at Publisher · View at Google Scholar · View at Scopus
  155. O. Eschenko, W. Ramadan, M. Molle, J. Born, and S. J. Sara, “Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning,” Learning & Memory, vol. 15, no. 4, pp. 222–228, 2008. View at Publisher · View at Google Scholar · View at Scopus
  156. V. Ego-Stengel and M. A. Wilson, “Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat,” Hippocampus, vol. 20, no. 1, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. A. Bikbaev, R. Frischknecht, and M. Heine, “Brain extracellular matrix retains connectivity in neuronal networks,” Scientific Reports, vol. 5, no. 1, article 14527, 2015. View at Publisher · View at Google Scholar · View at Scopus
  158. M. Vedunova, T. Sakharnova, E. Mitroshina et al., “Seizure-like activity in hyaluronidase-treated dissociated hippocampal cultures,” Frontiers in Cellular Neuroscience, vol. 7, p. 149, 2013. View at Publisher · View at Google Scholar · View at Scopus