The role of voltage dependence of the NMDA receptor in cellular and network oscillation

European Journal of Neuroscience

Volumn 36, Issue 2, 2012, Pages 2121-2136

  Martell, Amber L ^a   Ramirez, Jan Marino ^b   Lasky, Robert E ^c   Dwyer, Jennifer E ^a   Kohrman, Michael ^a   Van Drongelen, Wim ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Bursting; Compartmental model; Mouse; Neocortex; Pacemaker

Indexed keywords

MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TETRODOTOXIN; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ACTIVITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CELL STRUCTURE; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; MOUSE; NEOCORTEX; NERVE POTENTIAL; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SPIKE; WHOLE CELL;

EID: 84984584156     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08083.x     Document Type: Article

References (83)

1. Ashcroft, F.M. (2000) Ion Channels and Disease: Channelopathies. Academic Press, San Diego, CA.
2. Bayreuther, C., Bourg, V., Dellamonica, J., Borg, M., Bernardin, G. & Thomas, P. (2009) Complex partial status epilepticus revealing anti-NMDA receptor encephalitis. Epileptic Disord., 11, 261-265.
3. Ben Ari, Y. (2001) Developing networks play a similar melody. Trends Neurosci., 24, 353-360.
4. Benayoun, M., Cowan, J.D., van Drongelen, W. & Wallace, E. (2010) Avalanches in a Stochastic Model of Spiking Neurons. PLoS Comput. Biol., 6, 1000846.
5. Bonansco, C., González de la Vega, A., González Alegre, P., Borde, M., Garcá-Segura, L.M. & Buño, W. (2002) Tetanic stimulation of schaffer collaterals induces rhythmic bursts via NMDA receptor activation in rat CA1 pyramidal neurons. Hippocampus, 12, 434-446.
6. Bryk, A.S. & Raudenbush, S.W. (1992) Hierarchical Linear Models. Sage Publications, Newbury Park.
7. Buzsáki, G. (2006) Rhythms of the Brain. Oxford University Press, Oxford.
8. Chagnac-Amitai, Y. & Connors, B.W. (1989) Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex. J. Neurophysiol., 62, 1149-1162.
9. Chagnac-Amitai, Y., Luhmann, H.J. & Prince, D.A. (1990) Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J. Comp. Neurol., 296, 598-613.
10. 2+ channels controls pain sensory gating in the thalamus. J. Neurosci., 28, 13331-13340.
11. Christophe, E., Doerflinger, N., Lavery, D., Molnár, Z., Charpak, S. & Audinat, E. (2005) Two populations of layer V pyramidal cells of the mouse neocortex: development and sensitivity to anesthetics. J. Neurophysiol., 94, 3357-3367.
12. Chu, H.Y. & Zhen, X. (2010) Hyperpolarization-activated, cyclic nucleotide-gated (HCN) channels in the regulation of midbrain dopamine systems. Acta Pharmacol. Sin., 31, 1036-1043.
13. Crino, P.B., Duhaime, A. & Baltuch, G. (2001) Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia. Neurology, 56, 906-913.
14. Cull-Candy, S., Brickley, S. & Farrant, M. (2001) NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol., 11, 327-335.
15. +-dependent mechanism. J. Neurosci., 21, 759-770.
16. Del Negro, C.A., Pace, R.W. & Hayes, J.A. (2008) What role do pacemakers play in the generation of respiratory rhythm? Adv. Exp. Med. Biol., 605, 88-93.
17. Deschenes, M., Labelle, A. & Landry, P. (1979) Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Res., 178, 251-274.
18. van Drongelen, W., Koch, H., Marcuccilli, C., Pena, F. & Ramirez, J.M. (2003) Synchrony levels during evoked seizure-like bursts in mouse neocortical slices. J. Neurophysiol., 90, 1571-1580.
19. van Drongelen, W., Lee, H.C., Koch Hereld, M., Elsen, F., Chen, Z. & Stevens, R.L. (2005) Emergent epileptiform activity in neural networks with weak excitatory synapses. IEEE Trans. Neural. Syst. Rehabil. Eng., 13, 236-241.
20. van Drongelen, W., Koch, H., Elsen, F.P., Lee, H.C., Mrejeru, A., Doren, E., Marcuccilli, C.J., Hereld, M., Stevens, R.L. & Ramirez, J.M. (2006) The role of persistent sodium current in bursting activity of mouse neocortical networks in vitro. J. Neurophysiol., 96, 2564-2577.
21. Frick, A., Zieglgänsberger, W. & Dodt, H.U. (2001) Glutamate receptors form hot spots on apical dendrites of neocortical pyramidal neurons. J. Neurophysiol., 86, 1412-1421.
22. Games, K.D. & Winter, J.A. (1988) LayerV in rat auditory cortex: projections to inferior colliculus and contralateral cortex. Hear. Res., 34, 1-25.
23. Gao, W.J. & Zheng, Z.H. (2004) Target-specific differences in somatodendritic morphology of layerV pyramidal neurons in rat motor cortex. J. Comp. Neurol., 476, 174-185.
24. Glitsch, M.D. (2008) Calcium influx through N-methyl-D-aspartate receptors triggers GABA release at interneuron-Purkinje cell synapse in rat cerebellum. Neuroscience, 151, 403-409.
25. Gola, M. (1974) Neurones h ondes-salves des mollusques-Variations cycliques lentes des conductances ioniques. Pflügers Arch., 352, 17-36.
26. Golomb, D. & Amitai, Y. (1997) Propagating neuronal discharge in neocortical slices: computational and experimental study. J. Neurophysiol., 78, 1199-1211.
27. Hattox, A.M. & Nelson, S.B. (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J. Neurophysiol., 98, 3330-3340.
28. Hill, A.A. & Upadhyaya, R. (2009) The effect of prenatal nicotine exposure on the postnatal development of an in vitro respiratory rhythm. Abstract no. 270.15. Society for Neuroscience Annual Meeting 2009.
29. Hodgkin, A.L. (1948) The local electric changes associated with repetitive action in a nonmedulated axon. J. Physiol., 107, 165-181.
30. Hodgkin, A.L. & Huxley, A.F. (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol., 117, 500-544.
31. Hox, J.J. (1995) Applied Multi-Level Analysis, 2nd Edn. TT-Publikaties, Amsterdam.
32. Hull, C., Isaacson, J.S. & Scanziani, M. (2009) Postsynaptic mechanisms govern the differential excitation of cortical neurons by thalamic inputs. J. Neurosci., 29, 9127-9136.
33. Huss, M., Wang, D., Trané, C., Wikström, M. & Hellgren Kotaleski, J. (2008) An experimentally constrained computational model of NMDA oscillations in lamprey CPG neurons. J. Comput. Neurosci., 25, 108-121.
34. Izhikevich, E. (2007) Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting. MIT Press, Cambridge.
35. Jahr, C.E. & Stevens, C.F. (1990) A quantitative description of NMDA receptor-channel kinetic behavior. J. Neurosci., 10, 1830-1837.
36. Kalia, L.V., Kalia, S.K. & Salter, M.W. (2008) NMDA receptors in clinical neurology: excitatory times ahead. Lancet Neurol., 7, 742-755.
37. Kang, J., Huguenard, J.R. & Prince, D.A. (2000) Voltage-gated potassium channels activated during action potentials in layerV neocortical pyramidal neurons. J. Neurophysiol., 83, 70-80.
38. Kasper, E.M., Larkman, A.U., Lübke, J. & Blakemore, C. (1994) Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology and electrophysiological properties. J. Comp. Neurol., 339, 495-518.
39. Keefer, E.W., Gramowski, A. & Gross, G.W. (2001) NMDA receptor-dependent periodic oscillations in cultured spinal cord networks. J. Neurophysiol., 86, 3030-3042.
40. Kobayashi, T., Nagao, T., Fukuda, H., Hicks, T.P. & Oka, J.I. (1993) NMDA receptors mediate neuronal burst firing in rat somatosensory cortex in vivo. NeuroReport, 4, 735-738.
41. Kotsopoulos, I.A., van Merode, T., Kessels, F.G., de From, M.C. & Knottnerus, J.A. (2002) Systematic review and meta-analysis of incidence studies of epilepsy and unprovoked seizures. Epilepsia, 43, 1402-1409.
42. Larkum, M.E., Nevian, T., Sandler, M., Polsky, A. & Schiller, J. (2009) Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science, 325, 756-760.
43. Lerma, J., Herranz, A.S., Herreras, O., Abraira, V. & Martin del Rio, R. (1986) In vivo determination of extracellular concentration of amino acids in the rat hippocampus. A method based on brain dialysis and computerized analysis. Brain Res., 384, 145-155.
44. Liu, X.B., Murray, K.D. & Jones, E.G. (2004) Switching of NMDA receptor 2A and 2B subunits at thalamic and cortical synapses during early postnatal development. J. Neurosci., 24, 8885-8895.
45. MacLean, J.N. & Schmidt, B.J. (2001) Voltage-sensitivity of motoneuron NMDA receptor channels is modulated by serotonin in the neonatal rat spinal cord. J. Neurophysiol., 86, 1131-1138.
46. Mainen, Z.F. & Sejnowski, T.J. (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature, 382, 363-366.
47. Marcantoni, A., Baldelli, P., Hernandez-Guijo, J.M., Comunanza, V., Carabelli, V. & Carbone, E. (2007) L-type calcium channels in adrenal chromaffin cells: role in pace-making and secretion. Cell Calcium, 42, 397-408.
48. Marcuccilli, C.J., Tryba, A.K., van Drongelen, W., Koch, H., Viemari, J.C., Peña-Ortega, F., Doren, E.L., Pytel, P., Chevalier, M., Mrejeru, A., Kohrman, M.H., Lasky, R.E., Lew, S.M., Frim, D.M. & Ramirez, J.M. (2010) Neuronal bursting properties in focal and parafocal regions in pediatric neocortical epilepsy stratified by histology. J. Clin. Neurophysiol., 27, 387-397.
49. Mayer, M.L., Vyklicky, L. Jr. & Westbrook, G.L. (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J. Physiol., 415, 329-350.
50. 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.
51. Mitchell, B.D. & Macklis, J.D. (2005) Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice. J. Comp. Neurol., 482, 17-32.
52. Molnár, Z. & Cheung, A.F. (2006) Towards the classification of subpopulations of layerV pyramidal projection neurons. Neurosci. Res., 55, 105-115.
53. Mrejeru, A., Wei, A. & Ramirez, J.M. (2011) Calcium-activated non-selective cation currents are involved in generation of tonic and bursting activity in dopamine neurons of the substantia nigra pars compacta. J. Physiol., 589, 2497-2514.
54. Najm, I., Ying, Z., Babb, T., Crino, P.B., Macdonald, R., Mathern, G.W. & Spreafico, R. (2004) Mechanisms of epileptogenicity in cortical dysplasias. Neurology, 62, S9-S13.
55. Nicoll, R.A. (2003) Expression mechanisms underlying long-term potentiation: a postsynaptic view. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, 721-726.
56. Nishizawa, Y., Morii, H. & Durlach, J. (2007) New Perspectives in Magnesium Research. Springer, London.
57. Ohara, S., Ikeda, A., Kunieda, T., Yazawa, S., Taki, J., Nagamine, T., Taki, W., Miyamoto, S., Hashimoto, N. & Shibasaki, H. (2004) Propagation of tonic posturing in supplementary motor area (SMA) seizures. Epilepsy Res., 62, 179-187.
58. Pikovsky, A., Rosenblum, M. & Kurths, J. (2001) Synchronization - A Universal Concept in Nonlinear Sciences. Cambridge University Press, Cambridge.
59. Polsky, A., Mel, B. & Schiller, J. (2009) Encoding and decoding bursts by NMDA spikes in basal dendrites of layer5 pyramidal neurons. J. Neurosci., 29, 11891-11903.
60. Purvis, L.K., Smith, J.C., Koizumi, H. & Butera, R.J. (2007) Intrinsic bursters increase the robustness of rhythm generation in an excitatory network. J. Neurophysiol., 97, 1515-1526.
61. Raol, Y.H., Lynch, D.R. & Brooks-Kayal, A.R. (2001) Role of excitatory amino acids in developmental epilepsies. Ment. Retard. Dev. Disabil. Res. Rev., 7, 254-260.
62. Rhodes, P. (2006) The properties and implications of NMDA spikes in neocortical pyramidal cells. J. Neurosci., 26, 6704-6715.
63. Rioult-Pedotti, M.S. (1997) Intrinsic NMDA-induced oscillations in motoneurons of an adult vertebrate spinal cord are masked by inhibition. J. Neurophysiol., 77, 717-730.
64. Sah, P., S Hestrin, S. & Nicoll, R.A. (1989) Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science, 246, 815-818.
65. Schiller, J. & Schiller, Y. (2001) NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr. Opin. Neurobiol., 11, 343-348.
66. Schiller, J., Major, G., Koester, H.J. & Schiller, Y. (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature, 404, 285-289.
67. Schmidt, B.J., Hochman, S. & MacLean, J.N. (1998) NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann. N. Y. Acad. Sci., 860, 189-202.
68. Schubert, D., Kötter, R., Luhmann, H.J. & Staiger, J.F. (2006) Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layerva in the primary somatosensory cortex. Cereb. Cortex, 16, 223-236.
69. Schwartzkroin, P.A. (1993) Epilepsy: Models, Mechanisms, and Concepts. Cambridge University Press, Cambridge.
70. Schwarz, G.E. (1978) Estimating the dimension of a model. Ann. Stat., 6.2, 461-464.
71. Sherwin, A.L. (1999) Neuroactive amino acids in focally epileptic human brain: a review. Neurochem. Res., 24, 1387-1395.
72. Sherwin, A., Robitaille, Y., Quesney, F., Olivier, A., Villemure, J., Leblanc, R., Feindel, W., Andermann, E., Gotman, J., Andermann, F., Ethier, R. & Kish, S. (1988) Excitatory amino acids are elevated in human epileptic cerebral cortex. Neurology, 38, 920-923.
73. Spires, T.L., Molnár, Z., Kind, P.C., Cordery, P.M., Upton, A.L., Blakemore, C. & Hannan, A.J. (2005) Activity-dependent regulation of synapse and dendritic spine morphology in developing barrel cortex requires phospholipase C-beta1 signalling. Cereb. Cortex, 15, 385-393.
74. Spreafico, R., Battaglia, G., Arcelli, P., Andermann, F., Dubeau, F., Palmini, A., Olivier, A., Villemure, J.G., Tampieri, D., Avanzini, G. & Avoli, M. (1998) Cortical dysplasia: an immunocytochemical study of three patients. Neurology, 50, 27-36.
75. Strogatz, S.H. (1994) Nonlinear Dynamics and Chaos. Perseus Books, Cambridge.
76. Takekawa, T., Aoyagi, T. & Fukai, T. (2007) Synchronous and asynchronous bursting states: role of intrinsic neural dynamics. J. Comput. Neurosci., 23, 189-200.
77. Tohidi, V. & Nadim, F. (2009) Membrane resonance in bursting pacemaker neurons of an oscillatory network is correlated with network frequency. J. Neurosci., 29, 6427-6435.
78. + conductance or by blocking BK channels. J. Neurophysiol., 89, 909-921.
79. Trevelyan, A.J., Sussillo, D., Watson, B.O. & Yuste, R. (2006) Modular propagation of epileptiform activity: evidence for an inhibitory veto in neocortex. J. Neurosci., 26, 12447-12455.
80. Trevelyan, A.J., Baldeweg, T., van Drongelen, W., Yuste, R. & Whittington, M. (2007) The source of afterdischarge activity in neocortical tonic-clonic epilepsy. J. Neurosci., 27, 13513-13519.
81. Walther, H., Lambert, J.D., Jones, R.S., Heinemann, U. & Hamon, B. (1986) Epileptiform activity in combined slices of the hippocampus, subiculum and entorhinal cortex during perfusion with low magnesium medium. Neurosci. Lett., 69, 156-161.
82. White, E.L., Weinfeld, L. & Lev, D.L. (1997) A survey of morphogenesis during the early postnatal period in PMBSF barrels of mouse SmI cortex with emphasis on barrel D4. Somatosens. Mot. Res., 14, 34-55.
83. Ying, Z., Babb, T.L., Comair, Y.G., Bingaman, W., Bushey, M. & Touhalisky, K. (1998) Induced expression of NMDAR2 proteins and differential expression of NMDAR1 splice variants in dysplastic neurons of human epileptic cortex. J. Neuropathol. Exp. Neurol., 57, 47-62.