Gq/11-Induced and spontaneous waves of coordinated network activation in developing frontal cortex

Journal of Neuroscience

Volumn 25, Issue 7, 2005, Pages 1737-1749

  Calderon, D Paola ^a   Leverkova, Natalya ^a   Peinado, Alejandro ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Calcium (Ca); Cortex; Development; Dopamine; Frontal; mGluR5; Muscarinic; Neurotensin; Spontaneous

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR 1; MUSCARINIC M1 RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CHOLINERGIC NERVE CELL; DOPAMINERGIC NERVE CELL; EMBRYO; FRONTAL CORTEX; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

(R)-2,3,4,5-TETRAHYDRO-8-CHLORO-3-METHYL-5-PHENYL-1H-3-BENZAZEPIN-7-OL; ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; DOPAMINE; FRONTAL LOBE; GLUTAMIC ACID; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; INDANS; MUSCARINE; NERVE TISSUE PROTEINS; NEUROTENSIN; OCCIPITAL LOBE; PARIETAL LOBE; PEPTIDE FRAGMENTS; PHENANTHRIDINES; PICROTOXIN; RATS; RATS, LONG-EVANS; RATS, WISTAR; RECEPTOR, MUSCARINIC M1; RECEPTOR, MUSCARINIC M3; RECEPTORS, DOPAMINE D1; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 14044254911     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2765-04.2005     Document Type: Article

References (76)

1. Aksay E, Gamkrelidze G, Seung HS, Baker R, Tank DW (2001) In vivo intracellular recording and perturbation of persistent activity in a neural integrator. Nat Neurosci 4:184-193.
2. 1-like receptor activation excites rat striatal large aspiny neurons in vitro. J Neurosci 18:5180-5190.
3. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
4. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
5. Bevilacqua JA, Downes CP, Lowenstein PR (1995) Transiently selective activation of phosphoinositide turnover in layer V pyramidal neurons after specific mGluRs stimulation in rat somatosensory cortex during early postnatal development. J Neurosci 15:7916-7928.
6. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC (2004) Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429:523-530.
7. Broersen LM, Heinsbroek RP, de Bruin JP, Joosten RN, van Hest A, Olivier B (1994) Effects of local application of dopaminergic drugs into the dorsal part of the medial prefrontal cortex of rats in a delayed matching to position task: comparison with local cholinergic blockade. Brain Res 645:113-122.
8. Chub N, O'Donovan MJ (1998) Blockade and recovery of spontaneous rhythmic activity after application of neurotransmitter antagonists to spinal networks of the chick embryo. J Neurosci 18:294-306.
9. Crair MC (1999) Neuronal activity during development: permissive or instructive? Curr Opin Neurobiol 9:88-93.
10. Dale LB, Babwah AV, Bhattacharya M, Kelvin DJ, Ferguson SS (2001) Spatial-temporal patterning of metabotropic glutamate receptor-mediated inositol 1,4,5-triphosphate, calcium, and protein kinase C oscillations: protein kinase C-dependent receptor phosphorylation is not required. J Biol Chem 38:35900-35908.
11. De Felipe J, Marco P, Fairen A, Jones EG (1997) Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb Cortex 7:619-634.
12. Descarries L, Lemay B, Doucet G, Berger B (1987) Regional and laminar density of the dopamine innervation in adult rat cerebral cortex. Neuroscience 21:807-824.
13. Divac I, Bjorklund A, Lindvall O, Passingham RE (1978) Converging projections from the mediodorsal thalamic nucleus and mesencephalic dopaminergic neurons to the neocortex in three species. J Comp Neurol 180:59-71.
14. Dudek SM, Bowen WD, Bear MF (1989) Postnatal changes in glutamate stimulated phosphoinositide turnover in rat neocortical synaptoneurosomes. Dev Brain Res 47:123-128.
15. Durstewitz D, Seamans JK, Sejnowski TJ (2000) Neurocomputational models of working memory. Nat Neurosci [Suppl] 3:1184-1191.
16. Egorov AV, Hamam BN, Fransen E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178.
17. Feller MB (1999) Spontaneous correlated activity in developing neural circuits. Neuron 22:653-656.
18. 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.
19. Garaschuk O, Hanse E, Konnerth A (1998) Developmental profile and synaptic origin of early network oscillations in the CA1 region of rat neonatal hippocampus. J Physiol (Lond) 507:219-236.
20. Garaschuk O, Linn J, Eilers J, Konnerth A (2000) Large-scale oscillatory calcium waves in the immature cortex. Nat Neurosci 3:452-459.
21. Caspar P, Bloch B, Le Moine C (1995) D1 and D2 receptor gene expression in the rat frontal cortex: cellular localization in different classes of efferent neurons. Eur J Neurosci 7:1050-1063.
22. Ghosh A, Greenberg ME (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268:239-247.
23. Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14:477-485.
24. Goodman CS, Shatz CJ (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell [Suppl] 72:77-98.
25. 2+ transients. Nature 375:784-787.
26. Hara Y, Shiosaka S, Senba E, Sakanaka M, Inagaki S, Takagi H, Kawai Y, Takatsuki K, Matsuzaki T, Tohyama M (1982) Ontogeny of the neurotensin- containing neuron system of the rat: immunohistochemical analysis. I. Forebrain and diencephalon. J Comp Neurol 208:177-195.
27. Horton HL, Levitt P (1988) A unique membrane protein is expressed on early developing limbic system axons and cortical targets. J Neurosci 8:4653-4661.
28. Ihnatovych I, Novotny J, Haugvicova R, Bourova L, Mares P, Svoboda P (2002) Ontogenetic development of the G protein-mediated adenylyl cyclase signalling in rat brain. Brain Res Dev Brain Res 133:69-75.
29. Kalsbeek A, Voorn P, Buijs RM, Pool CW, Uylings HB (1988) Development of the dopaminergic innervation in the prefrontal cortex of the rat. J Comp Neurol 269:58-72.
30. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
31. Kilb W, Luhmann HJ (2003) Carbachol-induced network oscillations in the intact cerebral cortex of the newborn rat. Cereb Cortex 13:409-421.
32. Leinekugel X, Khazipov R, Cannon R, Hirase H, Ben-Ari Y, Buzsaki G (2002) Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296:2049-2052.
33. Lepee-Lorgeoux I, Betancur C, Rostene W, Pelaprat D (1999) Differential ontogenetic patterns of levocabastine-sensitive neurotensin NT2 receptors and of NT1 receptors in the rat brain revealed by in situ hybridization. Brain Res Dev Brain Res 113:115-131.
34. Lezcano N, Mrzljak L, Eubanks S, Levenson R, Goldman-Rakic P, Bergson C (2000) Dual signaling regulated by calcyon, a D1 dopamine receptor interacting protein. Science 287:1660-1664.
35. Lopez-Bendito G, Shigemoto R, Fairen A, Lujan R (2002) Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb Cortex 12:625-638.
36. Luhmann HJ, Prince DA (1991) Postnatal maturation of the GABAergic system in rat neocortex. J Neurophysiol 65:247-263.
37. MacGregor DG, Chesler M, Rice ME (2001) HEPES prevents edema in rat brain slices. Neurosci Lett 303:141-144.
38. Marder E, Abbott LF, Turrigiano GG, Liu Z, Golowasch J (1996) Memory from the dynamics of intrinsic membrane currents. Proc Natl Acad Sci USA 93:13481-13486.
39. Meister M, Wong RO, Baylor DA, Shatz CJ (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252:939-943.
40. Milner LD, Landmesser LT (1999) Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19:3007-3022.
41. Moroni F, Lombardi G, Thomsen C, Leonardi P, Attucci S, Peruginelli F, Torregrossa SA, Pellegrini-Giampietro DE, Luneia R, Pellicciari R (1997) Pharmacological characterization of 1-aminoindan-1,5-dicarboxylic acid, a potent mGluR1 antagonist. J Pharmacol Exp Ther 281:721-729,
42. O'Donovan MJ (1999) The origin of spontaneous activity in developing networks of the vertebrate nervous system. Curr Opin Neurobiol 9:94-104.
43. Ongur D, Price JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and man. Cereb Cortex 10:206-219.
44. Owens DF, Boyce LH, Davis MB, Kriegstein AR (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J Neurosci 16:6414-6423.
45. Palacios JM, Pazos A, Dietl MM, Schlumpf M, Lichtensteiger W (1988) The ontogeny of brain neurotensin receptors studied by autoradiography. Neuroscience 25:307-317.
46. 2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci 4:803-812.
47. Paxinos G, Tork I, Tecott LH, Valentine KL (1991) Atlas of the developing rat brain. New York: Academic.
48. Peinado A (2000) Traveling slow waves of neural activity: a novel form of network activity in developing neocortex. J Neurosci 20:RC54(1-6).
49. Peinado A (2001) Immature neocortical neurons exist as extensive syncitial networks linked by dendrodendritic electrical connections. J Neurophysiol 85:620-629.
50. Peinado A, Calderon DP (2002) Hyperactivation of developing cortical circuits by acetylcholine and the ontogeny of abnormal cognition and emotion: findings and hypothesis. Prog Brain Res 145:131-142.
51. Penn AA, Riquelme PA, Feller MB, Shatz CJ (1998) Competition in retinogeniculate patterning driven by spontaneous activity. Science 279:2108-2112.
52. Pimenta AF, Reinoso BS, Levitt P (1996) Expression of the mRNAs encoding the limbic system-associated membrane protein (LAMP): II. Fetal rat brain. J Comp Neurol 375:289-302.
53. Reid SN, Daw NW, Gregory DS, Flavin H (1996) cAMP levels increased by activation of metabotropic glutamate receptors correlate with visual plasticity. J Neurosci 16:7619-7626.
54. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 10:1027-1034.
55. Sawaguchi T, Goldman-Rakic PS (1991) D1 dopamine receptors in prefrontal cortex: involvement in working memory. Science 251:947-950.
56. Schmidt RH, Bjorklund A, Lindvall O, Loren I (1982) Prefrontal cortex: dense dopaminergic input in the newborn rat. Brain Res 281:222-228.
57. Shatz CJ (1996) Emergence of order in visual system development. Proc Natl Acad Sci USA 93:602-608.
58. Spitzer NC (2002) Activity-dependent neuronal differentiation prior to synapse formation: the functions of calcium transients. J Physiol (Paris) 96:73-80.
59. Spitzer NC, Debaca RC, Allen KA, Holliday J (1993) Calcium dependence of differentiation of GABA immunoreactivity in spinal neurons. J Comp Neurol 337:168-175.
60. Stead JDH, Neal CR, Evans SJ, Watson SJ, Akil H (2003) Variation in gene expression in the developing rat brain. Soc Neurosci Abstr 29:149.6.
61. Stellwagen D, Shatz CJ (2002) An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33:357-367.
62. Sur M, Angelucci A, Sharma J (1999) Rewiring cortex: the role of patterned activity in development and plasticity of neocortical circuits. J Neurobiol 41:33-43.
63. Undie AS, Friedman E (1990) Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain. J Pharmacol Exp Ther 253:987-992.
64. Verney C, Berger B, Adrien J, Vigny A, Gay M (1982) Development of the dopaminergic innervation of the rat cerebral cortex. A light microscopic immunocytochemical study using anti-tyrosine hydroxylase antibodies. Brain Res 281:41-52.
65. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
66. Vincent JP, Mazella J, Kitabgi P (1999) Neurotensin and neurotensin receptors. Trends Pharmacol Sci 20:302-309.
67. Wang HY, Undie AS, Friedman E (1995) Evidence for the coupling of Gq protein to D1-like dopamine sites in rat striatum: possible role in dopamine-mediated inositol phosphate formation. Mol Pharmacol 48:988-994.
68. Watt SD, Gu X, Smith RD, Spitzer NC (2000) Specific frequencies of spontaneous Ca2+ transients upregulate GAD 67 transcripts in embryonic spinal neurons. Mol Cell Neurosci 16:376-387.
69. Weliky M, Katz LC (1999) Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo. Science 285: 599-604.
70. Wiesel TN (1982) Postnatal development of the visual cortex and the influence of environment. Nature 299:583-591.
71. Wong RO (1999) Retinal waves and visual system development. Annu Rev Neurosci 22:29-47.
72. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566.
73. Yuste R, Peinado A, Katz LC (1992) Neuronal domains in developing neocortex. Science 257:665-669.
74. Zhang LI, Poo MM (2001) Electrical activity and development of neural circuits. Nat Neurosci [Suppl] 4:1207-1214.
75. Zilles K (1985) The cortex of the rat: a stereotaxic atlas. New York: Springer.
76. Zilles K, Wree A (1995) Cortex: areal and laminar structure. In: The rat nervous system (Paxinos G, ed), pp 649-685. San Diego: Academic.