Brain extracellular matrix retains connectivity in neuronal networks

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Bikbaev, Arthur ^a   Frischknecht, Renato ^a   Heine, Martin ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84942807120     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14527     Document Type: Article

References (60)

1. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138 (1996).
2. Ben-Ari, Y. Developing networks play a similar melody. Trends in neurosciences 24, 353-360 (2001).
3. Corner, M. A. Spontaneous neuronal burst discharges as dependent and independent variables in the maturation of cerebral cortex tissue cultured in vitro: A review of activity-dependent studies in live model systems for the development of intrinsically generated bioelectric slow-wave sleep patterns. Brain research reviews 59, 221-244 (2008).
4. Ben-Ari, Y. & Cherubini, E. Zinc and GABA in developing brain. Nature 353, 220 (1991).
5. Cancedda, L., Fiumelli, H., Chen, K. & Poo, M. M. Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. The Journal of neuroscience: The official journal of the Society for Neuroscience 27, 5224-5235 (2007).
6. Yuste, R. & Katz, L. C. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333-344 (1991).
7. Adelsberger, H., Garaschuk, O. & Konnerth, A. Cortical calcium waves in resting newborn mice. Nature neuroscience 8, 988-990 (2005).
8. Khazipov, R. et al. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432, 758-761 (2004).
9. Frischknecht, R. & Seidenbecher, C. I. The crosstalk of hyaluronan-based extracellular matrix and synapses. Neuron glia biology 4, 249-257 (2008).
10. Gundelfinger, E. D., Frischknecht, R., Choquet, D. & Heine, M. Converting juvenile into adult plasticity: A role for the brains extracellular matrix. The European journal of neuroscience 31, 2156-2165 (2010).
11. Celio, M. R. & Blumcke, I. Perineuronal nets-A specialized form of extracellular matrix in the adult nervous system. Brain research. Brain research reviews 19, 128-145 (1994).
12. Davies, S. J. et al. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 390, 680-683 (1997).
13. Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251 (2002).
14. Gogolla, N., Caroni, P., Luthi, A. & Herry, C. Perineuronal nets protect fear memories from erasure. Science 325, 1258-1261 (2009).
15. Happel, M. F. et al. 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 111, 2800-2805 (2014).
16. Carulli, D. et al. Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain: A journal of neurology 133, 2331-2347 (2010).
17. Tsien, R. Y. Very long-Term memories may be stored in the pattern of holes in the perineuronal net. Proceedings of the National Academy of Sciences of the United States of America 110, 12456-12461 (2013).
18. Wintergerst, E. S. et al. Temporal and spatial appearance of the membrane cytoskeleton and perineuronal nets in the rat neocortex. Neuroscience letters 209, 173-176 (1996).
19. Dityatev, A. et al. Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Developmental neurobiology 67, 570-588 (2007).
20. John, N. et al. Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Molecular and cellular neurosciences 31, 774-784 (2006).
21. Seeger, G., Brauer, K., Härtig, W. & Bröckner, G. Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry. Neuroscience 58, 371-388 (1994).
22. Bröckner, G., Bringmann, A., Köppe, G., Härtig, W. & Brauer, K. In vivo and in vitro labelling of perineuronal nets in rat brain. Brain research 720, 84-92 (1996).
23. Corner, M. A., van Pelt, J., Wolters, P. S., Baker, R. E. & Nuytinck, R. H. Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neuronal networks-An inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny. Neuroscience and biobehavioral reviews 26, 127-185 (2002).
24. Wagenaar, D. A., Madhavan, R., Pine, J. & Potter, S. M. Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. The Journal of neuroscience: The official journal of the Society for Neuroscience 25, 680-688 (2005).
25. Marom, S. & Shahaf, G. Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy. Quarterly reviews of biophysics 35, 63-87 (2002).
26. Habets, A. M., Van Dongen, A. M., Van Huizen, F. & Corner, M. A. Spontaneous neuronal firing patterns in fetal rat cortical networks during development in vitro: A quantitative analysis. Experimental brain research. Experimentelle Hirnforschung. Experimentation cerebrale 69, 43-52 (1987).
27. Opitz, T., De Lima, A. D. & Voigt, T. Spontaneous development of synchronous oscillatory activity during maturation of cortical networks in vitro. Journal of neurophysiology 88, 2196-2206 (2002).
28. Chiappalone, M., Bove, M., Vato, A., Tedesco, M. & Martinoia, S. Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development. Brain research 1093, 41-53 (2006).
29. van Huizen, F., Romijn, H. J. & Habets, A. M. Synaptogenesis in rat cerebral cortex cultures is affected during chronic blockade of spontaneous bioelectric activity by tetrodotoxin. Brain research 351, 67-80 (1985).
30. Voigt, T., Opitz, T. & de Lima, A. D. Activation of early silent synapses by spontaneous synchronous network activity limits the range of neocortical connections. The Journal of neuroscience: The official journal of the Society for Neuroscience 25, 4605-4615 (2005).
31. Canepari, M., Bove, M., Maeda, E., Cappello, M. & Kawana, A. Experimental analysis of neuronal dynamics in cultured cortical networks and transitions between different patterns of activity. Biological cybernetics 77, 153-162 (1997).
32. van Huizen, F., Romijn, H. J. & Corner, M. A. Indications for a critical period for synapse elimination in developing rat cerebral cortex cultures. Brain research 428, 1-6 (1987).
33. Swanwick, C. C., Murthy, N. R., Mtchedlishvili, Z., Sieghart, W. & Kapur, J. Development of gamma-Aminobutyric acidergic synapses in cultured hippocampal neurons. The Journal of comparative neurology 495, 497-510 (2006).
34. van Pelt, J., Wolters, P. S., Corner, M. A., Rutten, W. L. & Ramakers, G. J. Long-Term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE transactions on bio-medical engineering 51, 2051-2062 (2004).
35. Bettencourt, L. M., Stephens, G. J., Ham, M. I. & Gross, G. W. Functional structure of cortical neuronal networks grown in vitro. Physical review. E, Statistical, nonlinear, and soft matter physics 75, 021915 (2007).
36. Giamanco, K. A. & Matthews, R. T. Deconstructing the perineuronal net: Cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 218, 367-384 (2012).
37. Jarzylo, L. A. & Man, H. Y. Parasynaptic NMDA receptor signaling couples neuronal glutamate transporter function to AMPA receptor synaptic distribution and stability. The Journal of neuroscience: The official journal of the Society for Neuroscience 32, 2552-2563 (2012).
38. Kullmann, D. M., Min, M. Y., Asztely, F. & Rusakov, D. A. Extracellular glutamate diffusion determines the occupancy of glutamate receptors at CA1 synapses in the hippocampus. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 354, 395-402 (1999).
39. Stone, T. W. Development and therapeutic potential of kynurenic acid and kynurenine derivatives for neuroprotection. Trends in pharmacological sciences 21, 149-154 (2000).
40. Kamioka, H., Maeda, E., Jimbo, Y., Robinson, H. P. C. & Kawana, A. Spontaneous periodic synchronized bursting during formation of mature patterns of connections in cortical cultures. Neuroscience letters 206, 109-112 (1996).
41. Corner, M. A. & Ramakers, G. J. Spontaneous firing as an epigenetic factor in brain development-physiological consequences of chronic tetrodotoxin and picrotoxin exposure on cultured rat neocortex neurons. Brain research. Developmental brain research 65, 57-64 (1992).
42. van Huizen, F., Romijn, H. J., Habets, A. M. & van den Hooff, P. Accelerated neural network formation in rat cerebral cortex cultures chronically disinhibited with picrotoxin. Experimental neurology 97, 280-288 (1987).
43. McAllister, A. K., Katz, L. C. & Lo, D. C. Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064 (1996).
44. Vedunova, M. et al. Seizure-like activity in hyaluronidase-Treated dissociated hippocampal cultures. Frontiers in cellular neuroscience 7, 149 (2013).
45. Doischer, D. et al. Postnatal differentiation of basket cells from slow to fast signaling devices. The Journal of neuroscience: The official journal of the Society for Neuroscience 28, 12956-12968 (2008).
46. Dityatev, A., Schachner, M. & Sonderegger, P. The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nature reviews. Neuroscience 11, 735-746 (2010).
47. Savtchenko, L. P., Sylantyev, S. & Rusakov, D. A. Central synapses release a resource-efficient amount of glutamate. Nature neuroscience 16, 10-12 (2013).
48. Frischknecht, R. et al. Brain extracellular matrix affects AMPA receptor lateral mobility and short-Term synaptic plasticity. Nature neuroscience 12, 897-904 (2009).
49. Klueva, J., Gundelfinger, E. D., Frischknecht, R. R. & Heine, M. Intracellular Ca(2)(+ ) and not the extracellular matrix determines surface dynamics of AMPA-Type glutamate receptors on aspiny neurons. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 369, 20130605 (2014).
50. Kochlamazashvili, G. et al. The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-Type Ca(2+ ) channels. Neuron 67, 116-128 (2010).
51. Kullmann, D. M. Interneuron networks in the hippocampus. Current opinion in neurobiology 21, 709-716 (2011).
52. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78 (1995).
53. Geiger, J. R., Lubke, J., Roth, A., Frotscher, M. & Jonas, P. Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023 (1997).
54. Jinno, S. et al. Neuronal diversity in GABAergic long-range projections from the hippocampus. The Journal of neuroscience: The official journal of the Society for Neuroscience 27, 8790-8804 (2007).
55. Lahtinen, H. et al. Postnatal development of rat hippocampal gamma rhythm in vivo. Journal of neurophysiology 88, 1469-1474 (2002).
56. Gurevicius, K., Gureviciene, I., Valjakka, A., Schachner, M. & Tanila, H. Enhanced cortical and hippocampal neuronal excitability in mice deficient in the extracellular matrix glycoprotein tenascin-R. Molecular and cellular neurosciences 25, 515-523 (2004).
57. Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Annual review of neuroscience 35, 203-225 (2012).
58. Csicsvari, J., Jamieson, B., Wise, K. D. & Buzsaki, G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311-322 (2003).
59. Economo, M. N. & White, J. A. Membrane properties and the balance between excitation and inhibition control gammafrequency oscillations arising from feedback inhibition. PLoS computational biology 8, e1002354 (2012).
60. Kaech, S. & Banker, G. Culturing hippocampal neurons. Nat Protoc 1, 2406-2415 (2006).