Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Kaufman, Maya ^a   Corner, Michael A ^b   Ziv, Noam E ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CHOLINERGIC SYSTEM; CHOLINERGIC TONE; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITIC SPINE; ELECTROPHYSIOLOGY; HOMEOSTASIS; HUMAN; HUMAN CELL; NERVE EXCITABILITY; NERVOUS SYSTEM PARAMETERS; NEUROMODULATION; NONHUMAN; RAT; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC POTENTIAL; SYNAPTIC REMODELING; SYNAPTIC TRANSMISSION; SYNCHRONOUS BURSTING;

ANIMALS; CARBACHOL; CELLS, CULTURED; CHOLINERGIC AGONISTS; NERVE NET; NEURONS; RATS; SYNAPSES;

EID: 84864194547     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040980     Document Type: Article

References (80)

1. Hasselmo ME, (2006) The Role of Acetylcholine in Learning and Memory. Curr Opin Neurobiol 16: 710-715.
2. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, et al. (2007) Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity. Neuron 55: 919-929.
3. Froemke RC, Merzenich MM, Schreiner CE, (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450: 425-429.
4. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR, (2010) Facilitation of long-term potentiation by muscarinic M(1) receptors is mediated by inhibition of SK channels. Neuron 68: 948-963.
5. Gu Z, Yakel JL, (2011) Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71: 155-165.
6. Metherate R, Cox CL, Ashe JH, (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12: 4701-4711.
7. Steriade M, Amzica F, Nuñez A, (1993) Cholinergic and noradrenergic modulation of the slow (approximately 0.3 Hz) oscillation in neocortical cells. J Neurophysiol 70: 1385-1400.
8. Jones BE, (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26: 578-586.
9. Platt B, Riedel G, (2011) The cholinergic system, EEG and sleep. Behav Brain Res 221: 499-504.
10. Shaffery JP, Roffwarg H, (2009) The Ontogenetic Hypothesis of Rapid Eye Movement Sleep Function Revisited. In: Marcos G Frank, editors. pp. 177-216 editor. Current Advances in Sleep Biology. Nova Science Publishers, Inc.
11. Diekelmann S, Born J, (2010) The memory function of sleep. Nat Rev Neurosci 11: 114-126.
12. Hohmann CF, Berger-Sweeney J, (1998) Cholinergic regulation of cortical development and plasticity. New twists to an old story. Perspect Dev Neurobiol 5: 401-425.
13. Gu Q, (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111: 815-835.
14. Ramanathan D, Tuszynski MH, Conner JM, (2009) The basal forebrain cholinergic system is required specifically for behaviorally mediated cortical map plasticity. J Neurosci 29: 5992-6000.
15. Barnes CA, McNaughton BL, Goddard GV, Douglas RM, Adamec R, (1977) Circadian rhythm of synaptic excitability in rat and monkey central nervous system. Science 197: 91-92.
16. Birtoli B, Ulrich D, (2004) Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J Neurosci 24: 4935-4940.
17. Vyazovskiy VV, Cirelli C, Pfister-Genskow M, Faraguna U, Tononi G, (2008) Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep. Nat Neurosci 11: 200-208.
18. Liu ZW, Faraguna U, Cirelli C, Tononi G, Gao XB, (2010) Direct evidence for wake-related increases and sleep-related decreases in synaptic strength in rodent cortex. J Neurosci 30: 8671-8675.
19. Maret S, Faraguna U, Nelson AB, Cirelli C, Tononi G, (2011) Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat Neurosci 14: 1418-1420.
20. Lanté F, Toledo-Salas JC, Ondrejcak T, Rowan MJ, Ulrich D, (2011) Removal of synaptic Ca2+-permeable AMPA receptors during sleep. J Neurosci 31: 3953-3961.
21. Yang G, Gan WB, (2011) Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex. Dev Neurobiol doi:10.1002/dneu.20996.
22. Appelbaum L, Wang G, Yokogawa T, Skariah GM, Smith SJ, et al. (2010) Circadian and homeostatic regulation of structural synaptic plasticity in hypocretin neurons. Neuron 68: 87-98.
23. Gilestro GF, Tononi G, Cirelli C, (2009) Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 324: 109-112.
24. Donlea JM, Ramanan N, Shaw PJ, (2009) Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324: 105-108.
25. Bushey D, Tononi G, Cirelli C, (2011) Sleep and synaptic homeostasis: structural evidence in Drosophila. Science 332: 1576-1581.
26. Tateno T, Jimbo Y, Robinson HPC, (2005) Spatio-temporal cholinergic modulation in cultured networks of rat cortical neurons: spontaneous activity. Neuroscience 134: 425-437.
27. Chiappalone M, Vato A, Berdondini L, Koudelka-Hep M, Martinoia S, (2007) Network dynamics and synchronous activity in cultured cortical neurons. Int J Neural Syst 17: 87-103.
28. Chiappalone M, Corner M, Le Feber J, (2010) Persistent effects of cholinergic activation in developing cerebral cortex cultures: a model for the role of sleep activity patterns in early development? In: Stett A, editors. pp. 65-66 editor. Proceedings of the 7th International Meeting on Substrate-integrated Micro-electrodes: "MEA 2010." Stuttgart: BioPro BW.
29. Pasquale V, Massobrio P, Bologna LL, Chiappalone M, Martinoia S, (2008) Self-organization and neuronal avalanches in networks of dissociated cortical neurons. Neuroscience 153: 1354-1369.
30. Minerbi A, Kahana R, Goldfeld L, Kaufman M, Marom S, et al. (2009) Long-term relationships between synaptic tenacity, synaptic remodeling, and network activity. PLoS Biol 7(6), e1000136.
31. Holtmaat A, Svoboda K, (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 10: 647-658.
32. Keith D, El-Husseini A, (2008) Excitation Control: Balancing PSD-95 Function at the Synapse. Front Mol Neurosci 1: 4 DOI:10.3389/neuro.02.004.2008.
33. Bresler T, Ramati Y, Zamorano PL, Zhai R, Garner CC, et al. (2001) The dynamics of SAP90/PSD-95 recruitment to new synaptic junctions. Mol Cell Neurosci 18: 149-167.
34. Gray NW, Weimer RM, Bureau I, Svoboda K, (2006) Rapid redistribution of synaptic PSD-95 in the neocortex in vivo. PLoS Biol 4, e370.
35. Loewenstein Y, Kuras A, Rumpel S, (2011) Multiplicative dynamics underlie the emergence of the log-normal distribution of spine sizes in the neocortex in vivo. J Neurosci 31: 9481-9488.
36. Maeda E, Robinson HP, Kawana A, (1995) The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. J Neurosci 15: 6834-6845.
37. Segev R, Benveniste M, Hulata E, Cohen N, Palevski A, et al. (2002) Long term behavior of lithographically prepared in vitro neuronal networks. Phys Rev Lett 88(11), 118102.
38. van Pelt J, Wolters PS, Corner MA, Rutten WL, Ramakers GJ, (2004) Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE Trans Biomed Eng 51: 2051-2062.
39. Wagenaar DA, Madhavan R, Pine J, Potter SM, (2005) Controlling Bursting in Cortical Cultures with Closed-Loop Multi-Electrode Stimulation. J Neurosci 25: 680-688.
40. Wagenaar DA, Pine J, Potter SM, (2006) An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neurosci 7: 11 DOI:10.1186/1471-2202-7-11.
41. Eytan D, Marom S, (2006) Dynamics and effective topology underlying synchronization in networks of cortical neurons. J Neurosci 26: 8465-8476.
42. Corner MA, Baker RE, van Pelt J, (2008) Physiological consequences of selective suppression of synaptic transmission in developing cerebral cortical networks in vitro: differential effects on intrinsically generated bioelectric discharges in a living 'model' system for slow-wave sleep activity. Neurosci Biobehav Rev 32: 1569-1600.
43. Turrigiano GG, Nelson SB, (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5: 97-107.
44. Pozo K, Goda Y, (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66: 337-351.
45. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H, (2008) Principles of Long-Term Dynamics of Dendritic Spines. J Neurosci 28: 13592-13608.
46. Fisher-Lavie A, Zeidan A, Stern M, Garner CC, Ziv NE, (2011) Use dependence of presynaptic tenacity. J Neurosci 31: 16770-16780.
47. Lee MG, Hassani OK, Alonso A, Jones BE, (2005) Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25: 4365-4369.
48. McCormick DA, Prince DA, (1987) Actions of acetylcholine in the guinea-pig and cat medial and lateral geniculate nuclei, in vitro. J Physiol 392: 147-165.
49. Jasper HH, Tessier J, (1971) Acetylcholine liberation from cerebral cortex during paradoxical (REM) sleep. Science 172: 601-602.
50. Marrosu F, Portas C, Mascia MS, Casu MA, Fà M, et al. (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671: 329-332.
51. Vyazovskiy VV, Olcese U, Hanlon EC, Nir Y, Cirelli C, et al. (2011) Local sleep in awake rats. Nature 472: 443-447.
52. Steriade M, Nuñez A, Amzica F, (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252-3265.
53. Steriade M, Nuñez A, Amzica F, (1993) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13: 3266-3283.
54. Steriade M, Timofeev I, Grenier F, (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969-1985.
55. Destexhe A, Contreras D, Steriade M, (1999) Spatiotemporal analysis of local field potentials and unit discharges in cat cerebral cortex during natural wake and sleep states. J Neurosci 19: 4595-4608.
56. Timofeev I, Grenier F, Steriade M, (2001) Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci U S A 98: 1924-1929.
57. Amzica F, Steriade M, (2002) The functional significance of K-complexes. Sleep Med Rev 6: 139-149.
58. Volgushev M, Chauvette S, Mukovski M, Timofeev I, (2006) Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave oscillations. J Neurosci 26: 5665-5672.
59. Vyazovskiy VV, Olcese U, Lazimy YM, Faraguna U, Esser SK, et al. (2009) Cortical firing and sleep homeostasis. Neuron 63: 865-878.
60. Cash SS, Halgren E, Dehghani N, Rossetti AO, Thesen T, et al. (2009) The human K-complex represents an isolated cortical down-state. Science 324: 1084-1087.
61. Tononi G, Cirelli C, (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10: 49-62.
62. Corner MA, (2008) 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 Res Rev 59: 221-244.
63. Schätzle P, Ster J, Verbich D, McKinney RA, Gerber U, et al. (2011) Rapid and reversible formation of spine head filopodia in response to muscarinic receptor activation in CA1 pyramidal cells. J Physiol 589: 4353-4364.
64. Sanchez-Vives MV, McCormick DA, (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034.
65. Beggs JM, Plenz D, (2003) Neuronal avalanches in neocortical circuits. J Neurosci 23: 11167-11177.
66. Baker RE, Corner MA, van Pelt J, (2006) Spontaneous neuronal discharge patterns in developing organotypic mega-co-cultures of neonatal rat cerebral cortex. Brain Res 1101: 29-35.
67. Johnson HA, Buonomano DV, (2007) Development and plasticity of spontaneous activity and Up states in cortical organotypic slices. J Neurosci 27: 5915-5925.
68. Garaschuk O, Linn J, Eilers J, Konnerth A, (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3: 452-459.
69. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, et al. (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432: 758-761.
70. Hanganu IL, Staiger JF, Ben-Ari Y, Khazipov R, (2007) Cholinergic modulation of spindle bursts in the neonatal rat visual cortex in vivo. J Neurosci 27: 5694-5705.
71. Hanganu IL, Okabe A, Lessmann V, Luhmann HJ, (2009) Cellular mechanisms of subplate-driven and cholinergic input-dependent network activity in the neonatal rat somatosensory cortex. Cereb Cortex 19: 89-105.
72. Golshani P, Gonçalves JT, Khoshkhoo S, Mostany R, Smirnakis S, et al. (2009) Internally mediated developmental desynchronization of neocortical network activity. J Neurosci 29: 10890-10899.
73. Moore AR, Zhou WL, Jakovcevski I, Zecevic N, Antic SD, (2011) Spontaneous electrical activity in the human fetal cortex in vitro. J Neurosci 31: 2391-2398.
74. Constantinople CM, Bruno RM, (2011) Effects and mechanisms of wakefulness on local cortical networks. Neuron 69: 1061-1068.
75. Ben-Ari Y, (2001) Developing networks play a similar melody. Trends Neurosci 24: 353-360.
76. Fröhlich F, Bazhenov M, Sejnowski TJ, (2008) Pathological effect of homeostatic synaptic scaling on network dynamics in diseases of the cortex. J Neurosci 28: 1709-1720.
77. Hill S, Tononi G, (2005) Modeling sleep and wakefulness in the thalamocortical system. J Neurophysiol 93: 1671-1698.
78. Siegel JM, Rogawski MA, (1988) A function for REM sleep: regulation of noradrenergic receptor sensitivity. Brain Res 472: 213-233.
79. Corner MA, Baker RE, van Pelt J, Wolters PS, (2005) Compensatory physiological responses to chronic blockade of amino acid receptors during early development in spontaneously active organotypic cerebral cortex explants cultured in vitro. Prog Brain Res 147: 231-248.
80. Cohen D, Segal M, (2009) Homeostatic presynaptic suppression of neuronal network bursts. J Neurophysiol 101: 2077-2088.