Cellular mechanisms of subplate-driven and cholinergic input-dependent network activity in the neonatal rat somatosensory cortex

Cerebral Cortex

Volumn 19, Issue 1, 2009, Pages 89-105

  Hanganu, Ileana L ^a   Okabe, Akihito ^a,b   Lessmann, Volkmar ^a,c   Luhmann, Heiko J ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b HYOGO COLLEGE OF MEDICINE   (Japan)

^c OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Calcium transients; Development; Gap junctions; m1 m5 muscarinic receptors; Tonic GABA; Up state

Indexed keywords

4 AMINOBUTYRIC ACID; MUSCARINIC RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; DEPOLARIZATION; ELECTRICAL SYNAPSE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION;

ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CALCIUM SIGNALING; CELLS, CULTURED; GAMMA-AMINOBUTYRIC ACID; NERVE NET; NEURONS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION;

EID: 57749196754     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhn061     Document Type: Article

References (85)

1. Albrecht J, Hanganu IL, Heck N, Luhmann HJ. 2005. Oxygen and glucose deprivation induces major dysfunction in the somatosensory cortex of the newborn rat. Eur J Neurosci. 22:2295-2305.
2. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci. 17:185-218.
3. Arumugam H, Liu X, Colombo PJ, Corriveau RA, Belousov AB. 2005. NMDA receptors regulate developmental gap junction uncoupling via CREB signaling. Nat Neurosci. 8:1720-1726.
4. Borden LA, Murali Dhar TG, Smith KE, Weinshank RL, Branchek TA, Gluchowski C. 1994. Tiagabine, SK&F 89976-A, CI-966, and NNC-711 are selective for the cloned GABA transporter GAT-1. Eur J Pharmacol. 269:219-224.
5. Bunney BG, Potkin SG, Bunney WE. 1997. Neuropathological studies of brain tissue in schizophrenia. J Psychiatr Res. 31:159-173.
6. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G. 1998. Endogenous ACh enhances striatal NMDA-responses via M1-like muscarinic receptors and PKC activation. Eur J Neurosci. 10:2887-2895.
7. Calarco CA, Robertson RT. 1995. Development of basal forebrain projections to visual cortex: DiI studies in rat. J Comp Neurol. 354:608-626.
8. Calderon DP, Leverkova N, Peinado A. 2005. Gq/11-induced and spontaneous waves of coordinated network activation in developing frontal cortex. J Neurosci. 25:1737-1749.
9. Catalano SM, Shatz CJ. 1998. Activity-dependent cortical target selection by thalamic axons. Science. 281:559-562.
10. Cobb SR, Davies CH. 2005. Cholinergic modulation of hippocampal cells and circuits. J Physiol. 562:81-88.
11. Corlew R, Bosma MM, Moody WJ. 2004. Spontaneous, synchronous electrical activity in neonatal mouse cortical neurons. J Physiol. 560:377-390.
12. Cruikshank SJ, Hopperstad M, Younger M, Connors BW, Spray DC, Srinivas M. 2004. Potent block of Cx36 and Cx50 gap junction channels by mefloquine. Proc Natl Acad Sci USA. 101:12364-12369.
13. Del Rio JA, Soriano E, Ferrer I. 1992. Development of GABA-immunoreactivity in the neocortex of the mouse. J Comp Neurol. 326:501-526.
14. Demarque M, Represa A, Becq H, Khalilov I, Ben-Ari Y, Aniksztejn L. 2002. Paracrine intercellular communication by a Ca2+- and SNARE-independent release of GABA and glutamate prior to synapse formation. Neuron. 36:1051-1061.
15. Dodt H-U, Zieglgänsberger W. 1990. Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res. 537:333-336.
16. Dupont E, Hanganu IL, Kilb W, Hirsch S, Luhmann HJ. 2006. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature. 439:79-83.
17. Egorov AV, Angelova PR, Heinemann U, Muller W. 2003. Ca2+-independent muscarinic excitation of rat medial entorhinal cortex layer V neurons. Eur J Neurosci. 18:3343-3351.
18. Farrant M, Nusser Z. 2005. Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci. 6:215-229.
19. Feller MB, Scanziani M. 2005. A precritical period for plasticity in visual cortex. Curr Opin Neurobiol. 15:94-100.
20. Flint AC, Dammerman RS, Kriegstein AR. 1999. Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc Natl Acad Sci USA. 96:12144-12149.
21. Fox K, Schlaggar BL, Glazewski S, O'Leary DD. 1996. Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex. Proc Natl Acad Sci USA. 93:5584-5589.
22. Friauf E, McConnell SK, Shatz CJ. 1990. Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex. J Neurosci. 10:2601-2613.
23. Garaschuk O, Linn J, Eilers J, Konnerth A. 2000. Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci. 3:452-459.
24. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature. 439:589-593.
25. Ghosh A, Antonini A, McConnell SK, Shatz CJ. 1990. Requirements of subplate neurons in the formation of thalamocortical connections. Nature. 347:179-181.
26. Gloveli T, Egorov AV, Schmitz D, Heinemann U, Muller W. 1999. Carbachol-induced changes in excitability and [Ca2+]i signalling in projection cells of medial entorhinal cortex layers II and III. Eur J Neurosci. 11:3626-3636.
27. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci. 26:4535-4545.
28. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. 1981. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100.
29. Hanganu IL, Kilb W, Luhmann HJ. 2001. Spontaneous synaptic activity of subplate neurons in neonatal rat somatosensory cortex. Cereb Cortex. 11:400-410.
30. Hanganu IL, Kilb W, Luhmann HJ. 2002. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci. 22:7165-7176.
31. Hanganu IL, Ben-Ari Y, Khazipov R. 2006. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J Neurosci. 26:6728-6736.
32. 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.
33. Heinemann U, Lux HD. 1977. Ceiling of stimulus induced rises in extracellular potassium concentration in the cerebral cortex of cat. Brain Res. 120:231-249.
34. Higashi S, Molnár Z, Kurotani T, Toyama K. 2002. Prenatal development of neural excitation in rat thalamocortical projections studied by optical recording. Neuroscience. 115:1231-1246.
35. Johnston MV, McKinney M, Coyle JT. 1979. Evidence for a cholinergic projection to neocortex from neurons in basal forebrain. Proc Natl Acad Sci USA. 76:5392-5396.
36. Jones EG. 1995. Cortical development and neuropathology in schizophrenia. Ciba Found Symp. 193:277-295.
37. Kanold PO, Kara P, Reid RC, Shatz CJ. 2003. Role of subplate neurons in functional maturation of visual cortical columns. Science. 301:521-525.
38. Kasyanov AM, Safiulina VF, Voronin LL, Cherubini E. 2004. GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci USA. 101:3967-3972.
39. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsaki G. 2004. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature. 432:758-761.
40. Khazipov R, Luhmann HJ. 2006. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 29:414-418.
41. Kilb W, Luhmann HJ. 2000. Characterization of a hyperpolarization- activated inward current in Cajal-Retzius cells in rat neonatal neocortex. J Neurophysiol. 84:1681-1691.
42. Kilb W, Luhmann HJ. 2003. Carbachol-induced network oscillations in the intact cerebral cortex of the newborn rat. Cereb Cortex. 13:409-421.
43. Klink R, Alonso A. 1997. Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol. 77:1829-1843.
44. Kostovic I. 1986. Prenatal development of nucleus basalis complex and related fiber systems in man: a histochemical study. Neuroscience. 17:1047-1077.
45. Kostovic I, Judas M. 2002. The role of the subplate zone in the structural plasticity of the developing human cerebral cortex. Neuroembryology. 1:145-153.
46. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW. 2002. Electrical synapses in the thalamic reticular nucleus. J Neurosci. 22:1002-1009.
47. Lein ES, Finney EM, McQuillen PS, Shatz CJ. 1999. Subplate neuron ablation alters neurotrophin expression and ocular dominance column formation. Proc Natl Acad Sci USA. 96:13491-13495.
48. Liu SQ, Kaczmarek LK. 1998. Depolarization selectively increases the expression of the Kv3.1 potassium channel in developing inferior colliculus neurons. J Neurosci. 18:8758-8769.
49. Long MA, Landisman CE, Connors BW. 2004. Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J Neurosci. 24:341-349.
50. Lucas-Meunier E, Fossier P, Baux G, Amar M. 2003. Cholinergic modulation of the cortical neuronal network. Pflugers Arch. 446:17-29.
51. Luhmann HJ, Hanganu I, Kilb W. 2003. Cellular physiology of the neonatal rat cerebral cortex. Brain Res Bull. 60:345-353.
52. Marchionni I, Omrani A, Cherubini E. 2007. In the developing rat hippocampus a tonic GABAA-mediated conductance selectively enhances the glutamatergic drive of principal cells. J Physiol. 581:515-528.
53. Mao BQ, Hamzei-Sichani F, Aronov D, Froemke RC, Yuste R. 2001. Dynamics of spontaneous activity in neocortical slices. Neuron. 32:883-898.
54. McCormick DA. 1993. Actions of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog Brain Res. 98:303-308.
55. Mechawar N, Descarries L. 2001. The cholinergic innervation develops early and rapidly in the rat cerebral cortex: a quantitative immunocytochemical study. Neuroscience. 108:555-567.
56. A receptors by neurons of the subplate zone in developing primate occipital cortex: evidence for transient local circuits. J Comp Neurol. 317:91-101.
57. Minlebaev M, Ben-Ari Y, Khazipov R. 2007. Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol. 97:692-700.
58. Milh M, Kaminska A, Huong C, Lapillone C, Ben-Ari Y, Khazipov R. 2006. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb Cortex. 17:1582-1594.
59. Misson J-P, Takahashi T, Caviness VS, Jr. 1991. Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia. 4:138-148.
60. Moody WJ, Bosma MM. 2005. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev. 85:883-941.
61. Nusser Z, Mody I. 2002. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol. 87:2624-2628.
62. Peinado A. 2000. Traveling slow waves of neural activity: a novel form of network activity in developing neocortex. J Neurosci. 20:NIL1-NIL6.
63. Platel JC, Dupuis A, Boisseau S, Villaz M, Albrieux M, Brocard J. 2007. Synchrony of spontaneous calcium activity in mouse neocortex before synaptogenesis. Eur J Neurosci. 25:920-928.
64. Saint-Amant L, Drapeau P. 2000. Motoneuron activity patterns related to the earliest behavior of the zebrafish embryo. J Neurosci. 20:3964-3972.
65. Schröder R, Luhmann HJ. 1997. Morphology, electrophysiology and pathophysiology of supragranular neurons in rat primary somatosensory cortex. Eur J Neurosci. 9:163-176.
66. Semyanov A, Walker MC, Kullmann DM. 2003. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci. 6:484-490.
67. Semyanov A, Walker MC, Kullmann DM, Silver RA. 2004. Tonically active GABA-A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27:262-269.
68. A current in rat CA3 pyramidal neurons at birth. Eur J Neurosci. 25:717-722.
69. Somjen GG. 1979. Extracellular potassium in the mammalian central nervous system. Annu Rev Physiol. 41:159-177.
70. Sooksawate T, Isa T. 2006. Properties of cholinergic responses in neurons in the intermediate grey layer of rat superior colliculus. Eur J Neurosci. 24:3096-3108.
71. Stell BM, Mody I. 2002. Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. J Neurosci. 22:RC223.
72. Steriade M, Nuñez A, Amzica F. 1993. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci. 13:3252-3256.
73. Stuart GJ, Dodt H-U, Sakmann B. 1993. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch. 423:511-518.
74. Sun J-J, Luhmann HJ. 2007. Spatio-temporal dynamics of oscillatory network activity in the neonatal mouse cerebral cortex. Eur J Neurosci. 26:1995-2004.
75. Syed MM, Lee S, Zheng J, Zhou ZJ. 2004. Stage-dependent dynamics and modulation of spontaneous waves in the developing rabbit retina. J Physiol. 560:533-549.
76. Takayasu Y, Iino M, Furuya N, Ozawa S. 2003. Muscarine-induced increase in frequency of spontaneous EPSCs in Purkinje cells in the vestibulo-cerebellum of the rat. J Neurosci. 23:6200-6208.
77. Torborg CL, Feller MB. 2005. Spontaneous patterned retinal activity and the refinement of retinal projections. Prog Neurobiol. 76:213-235.
78. Vanhatalo S, Palva JM, Andersson S, Rivera C, Voipio J, Kaila K. 2005. Slow endogenous activity transients and developmental expression of K+-Cl- cotransporter 2 in the immature human cortex. Eur J Neurosci. 22:2799-2804.
79. Wagner J, Luhmann HJ. 2006. Activation of metabotropic glutamate receptors induces propagating network oscillations in the intact cerebral cortex of the newborn mouse. Neuropharmacology. 51:848-857.
80. Yan Z, Flores-Hernandez J, Surmeier DJ. 2001. Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons. Neuroscience. 103:1017-1024.
81. Yue C, Yaari Y. 2004. KCNQ/M channels control spike after depolarization and burst generation in hippocampal neurons. J Neurosci. 24:4614-4624.
82. Yuste R, Nelson DA, Rubin WW, Katz LC. 1995. Neuronal domains in developing neocortex: mechanisms of coactivation. Neuron. 14:7-17.
83. Yuste R, Peinado A, Katz LC. 1992. Neuronal domains in developing neocortex. Science. 257:665-669.
84. Zhang LI, Poo MM. 2001. Electrical activity and development of neural circuits. Nat Neurosci. 4:1207-1214.
85. Zheng JQ, He XP, Yang AZ, Liu CG. 1998. Neostigmine competitively inhibited nicotinic acetylcholine receptors in sympathetic neurons. Life Sci. 62:1171-1178.