Subthreshold somatic voltage in neocortical pyramidal cells can control whether spikes propagate from the axonal plexus to axon terminals: A model study

Journal of Neurophysiology

Volumn 107, Issue 10, 2012, Pages 2833-2852

  Munro, Erin ^a,b   Kopell, Nancy ^b  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b USA   (United States)

Author keywords

Epilepsy; Gap junction; Neocortex; Pyramidal cell; Very fast oscillation

Indexed keywords

ANESTHESIA; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; GAP JUNCTION; HYPERPOLARIZATION; IN VIVO STUDY; MEMBRANE DEPOLARIZATION; NEOCORTEX; NERVE ENDING; NERVE FIBER; NERVE POTENTIAL; NERVE SPROUTING; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIMULATION; SOMATOSENSORY CORTEX; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; AXONS; COMPUTER SIMULATION; GAP JUNCTIONS; MODELS, NEUROLOGICAL; NERVE NET; PYRAMIDAL CELLS; RATS;

EID: 84861138491     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00709.2011     Document Type: Article

References (116)

1. Acker CD, Antic SD. Quantitative assessment of the distributions of membrane conductances involved in action potential backpropagation along basal dendrites. J Neurophysiol 101: 1524-1541, 2009.
2. Ascoli GA, Donohue DE, Halavi Neuro Morpho M. Org: A central resource for neuronal morphologies. J Neurosci 27: 9247-9251, 2007.
3. Beaulieu C. Numerical data on neocortical neurons in adult rat, with special reference to the GABA population. Brain Res 609: 284-292, 1993.
4. Bertram E. The relevance of kindling for human epilepsy. Epilepsia 48, Suppl 2: 65-74, 2007.
5. Boiko T, Wart AV, Caldwell JH, Levinson SR, Trimmer JS, Matthews G. Functional specialization of the axon initial segment by isoform-specific sodium channel targeting. J Neurosci 23: 2306-2313, 2003.
6. Bragin A, Mody I, Wilson CL, Engel J Jr. Local generation of fast ripples in epileptic brain. J Neurosci 22: 2012-2021, 2002.
7. Bragin A, Wilson CL, Almajano J, Mody I, Engel J Jr. High-frequency oscillations after status epilepticus: epileptogenesis and seizure genesis. Epilepsia 45: 1017-1023, 2004.
8. Brecht M, Sakmann B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol 543: 49-70, 2002.
9. Brosch M, Budinger E, Scheich H. Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol 87: 2715-2725, 2002.
10. Brovelli A, Lachaux JP, Kahane P, Boussaoud D. High gamma frequency oscillatory activity dissociates attention from intention in the human pre-motor cortex. Neuroimage 28: 154-164, 2005.
11. Buhl DL, Harris KD, Hormuzdi SG, Monyer H, Buzsáki G. Selective impairment of hippocampal gamma oscillations in connexin-36 knock-out mouse in vivo. J Neurosci 23: 1013-1018, 2003.
12. Buxhoeveden DP, Casanova MF. The minicolumn hypothesis in neurosci-ence. Brain 125: 935-951, 2002.
13. Canolty RT, Soltani M, Dalal SS, Edwards E, Dronkers NF, Nagarajan SS, Kirsch HE, Barbaro NM, Knight RT. Spatiotemporal dynamics of word processing in the human brain. Front Neurosci 1: 185-196, 2007.
14. Carnevale NT, Hines ML. The NEURON Book. Cambridge, UK: Cambridge University Press, 2006.
15. Chang BS, Lowenstein DH. Epilepsy. N Engl J Med 349: 1257-1266, 2003.
16. Chevassus-au-Louis N, Baraban SC, Gäiarsa JL, Ben-Ari Y. Cortical malformations and epilepsy: new insights from animal models. Epilepsia 40: 811-821, 1999.
17. Cheyne D, Bells S, Ferrari P, Gaetz W, Bostan AC. Self-paced movements induce high-frequency gamma oscillations in primary motor cortex. Neuro-image 42: 332-342, 2008.
18. Chung F, Lu L. Connected components in random graphs with given expected degree sequences. Ann Comb 6: 125-145, 2002.
19. Cox CL, Denk W, Tank DW, Svoboda K. Action potentials reliably invade axonal arbors of rat neocortical neurons. Proc Natl Acad Sci USA 97: 9724-9728, 2000.
20. Crochet S, Petersen CCH. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat Neurosci 9: 608-610, 2006.
21. Crone NE, Sinai A, Korzeniewska A. High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res 159: 275-295, 2006.
22. Cunningham MO, Halliday DM, Davies CH, Traub RD, Buhl EH, Whit-tington MA. Coexistence of gamma and high-frequency oscillations in rat medial entorhinal cortex in vitro. J Physiol 559: 347-353, 2004.
23. Cvapp. Cvapp (Online). http://www.compneuro.org/CDROM/docs/cvapp.html.
24. Debanne D. Information processing in the axon. Nat Rev Neurosci 5: 304-316, 2004.
25. + conductance in hippocampus. Nature 389: 286-289, 1997.
26. Draguhn A, Traub RD, Schmitz D, Jefferys JG. Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394: 189-192, 1998.
27. Edwards E, Soltani M, Deouell LY, Berger MS, Knight RT. High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. J Neurophysiol 94: 4269-4280, 2005.
28. Edwards E, Soltani M, Kim W, Dalal SS, Nagarajan SS, Berger MS, Knight RT. Comparison of timefrequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol 102: 377-386, 2009.
29. Engel J Jr. Introduction to temporal lobe epilepsy. Epilepsy Res 26: 141-150, 1996.
30. Engel J Jr, Bragin A, Staba R, Mody I. High-frequency oscillations: what is normal and what is not? Epilepsia 50: 598-604, 2009.
31. Erdos P, Rényi A. On the evolution of random graphs. Publ Math Inst Hung Acad Sci 5: 17-61, 1960.
32. Feldman ML, Peters A. A study of barrels and pyramidal dendritic clusters in the cerebral cortex. Brain Res 77: 55-76, 1974.
33. Gansert J, Golowasch J, Nadim F. Sustained rhythmic activity in gap-junctionally coupled networks of model neurons depends on the diameter of coupled dendrites. J Neurophysiol 98: 3450-3460, 2007.
34. Gaona CM, Sharma M, Freudenburg ZV, Breshears JD, Bundy DT, Roland J, Barbour DL, Schalk G, Leuthardt EC. Nonuniform high-gamma (60-500 Hz) power changes dissociate cognitive task and anatomy in human cortex. J Neurosci 31: 2091-2100, 2011.
35. Goldstein SS, Rall W. Changes of action potential shape and velocity for changing core conductor geometry. Biophys J 14: 731-757, 1974.
36. Goodenough DA, Paul DL. Gap junctions. Cold Spring Harb Perspect Biol 1: a002576, 2009.
37. Grenier F, Timofeev I, Steriade M. Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. J Neurophysiol 86: 1884-1898, 2001.
38. Grenier F, Timofeev I, Steriade M. Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. J Neurophysiol 89: 841-852, 2003.
39. Gutnick MJ, Lobel-Yaakov R, Rimon G. Incidence of neuronal dye-coupling in neocortical slices depends on the plane of section. Neuroscience 15: 659-666, 1985.
40. Gutnick MJ, Prince DA. Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice. Science 211: 67-70, 1981.
41. Hamzei-Sichani F, Kamasawa N, Janssen WGM, Yasumura T, Davidson KGV, Hof PR, Wearne SL, Stewart MG, Young SR, Whittington MA, Rash JE, Traub RD. Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze fracture replica immunogold labeling. Proc Natl Acad Sci USA 104: 12548-12553, 2007.
42. Hines ML, Morse T, Migliore M, Carenvale NT, Shepherd GM. ModelDB: A database to support computational neuroscience. J Comput Neurosci 17: 7-11, 2004.
43. Hormuzdi SG, Pais I, LeBeau FE, Towers SK, Rozov A, Buhl EH, Whittington MA, Monyer H. Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31: 487-495, 2001.
44. Hromádka T, Zador A. Representations in auditory cortex. Curr Opin Neurobiol 19: 430-433, 2009.
45. Jacobs J, Kahana MJ. Neural representations of individual stimuli in humans revealed by gamma-band electrocorticographic activity. J Neurosci 29: 10203-10214, 2009.
46. Jones MS, Barth DS. Spatiotemporal organization of fast (>200 Hz) electrical oscillations in rat vibrissa/barrel cortex. J Neurophysiol 82: 1599-1609, 1999.
47. Jones MS, MacDonald KD, Choi B, Dudek FE, Barth DS. Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. J Neurophysiol 84: 1505-1518, 2000.
48. Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, Carandini M. Local origin of field potentials in visual cortex. Neuron 61: 35-41, 2009.
49. Koester HJ, Sakmann B. Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. J Physiol 529: 625-646, 2000.
50. Kole MHP, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11: 178-186, 2008.
51. Lewis TJ, Rinzel J. Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions. Network 11: 299-320, 2000.
52. Lewis TJ, Rinzel J. Topological target patterns and population oscillations in a network with random gap junctional coupling. Neurocomputing 38-40: 763-768, 2001.
53. Lorincz A, Nusser Z. Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28: 14329-14340, 2008.
54. Maier N, Güldenagel M, Söhl G, Siegmund H, Willecke K, Draguhn A. Reduction of high-frequency network oscillations (ripples) and pathological network discharges in hippocampal slices from connexin 36-deficient mice. J Physiol 541: 521-528, 2002.
55. Margrie TW, Brecht M, Sakmann B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflügers Arch 444: 491-498, 2002.
56. MathWorks. MATLAB (Online). http://www.mathworks.com/products/matlab/.
57. Mercer A, Bannister AP, Thomson AM. Electrical coupling between pyramidal cells in adult cortical regions. Brain Cell Biol 35: 13-27, 2006.
58. Milojkovic BA, Wuskell JP, Loew LM, Antic SD. Initiation of sodium spikelets in basal dendrites of neocortical pyramidal neurons. J Membr Biol 208: 155-169, 2005.
59. Mountcastle VB. The columnar organization of the neocortex. Brain 120: 701-722, 1997.
60. Mountcastle VB. Introduction: computation in cortical columns. Cereb Cortex 13: 2-4, 2003.
61. Munro E, Börgers C. Mechanisms of very fast oscillations in networks of axons coupled by gap junctions. J Comput Neurosci 28: 539-555, 2010.
62. Murakami S, Zhang T, Hirose A, Okada YC. Physiological origins of evoked magnetic fields and extracellular field potentials produced by guinea-pig CA3 hippocampal slices. J Physiol 544: 237-251, 2002.
63. Nadim F, Golowasch J. Signal transmission between gap-junctionally coupled passive cables is most effective at an optimal diameter. J Neurophysiol 95: 3831-3843, 2006.
64. NeuroMorphoOrg. http://NeuroMorpho.org.
65. NEURON. http://www.neuron.yale.edu/neuron/.
66. Newman ME. Random graphs as models of networks. In: Handbook of Graphs and Networks: From the Genome to the Internet, edited by Born-holdt S, Schuster HG. Weinheim, Germany: Wiley-VCH Verlag, chapt 2, pp. 35-68. 2003.
67. Nimmrich V, Maier N, Schmitz D, Draguhn A. Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J Physiol 563: 663-670, 2005.
68. Palmer LM, Stuart GJ. Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26: 1854-1863, 2006.
69. Parker PRL, Cruikshank SJ, Connors BW. Stability of electrical coupling despite massive developmental changes of intrinsic neuronal physiology. J Neurosci 29: 9761-970, 2009.
70. Pei X, Leuthardt EC, Gaona CM, Brunner P, Wolpaw JR, Schalk G. Spatiotemporal dynamics of electrocorticographic high gamma activity during overt and covert word repetition. Neuroimage 54: 2960-2972, 2011.
71. Pitkänen A, McIntosh TK. Animal models of post-traumatic epilepsy. J Neurotrauma 23: 241-261, 2006.
72. Rakic P. Confusing cortical columns. Proc Natl Acad Sci USA 105: 12099-12100, 2008.
73. Rockland KS, Ichinohe N. Some thoughts on cortical minicolumns. Exp Brain Res 158: 265-277, 2004.
74. Roland J, Brunner P, Johnston J, Schalk G, Leuthardt EC. Passive real-time identification of speech and motor cortex during an awake craniotomy. Epilepsy Behav 18: 123-128, 2010.
75. Roopun AK, Simonotto JD, Pierce ML, Jenkins A, Nicholson C, Schofield IS, Whittaker RG, Kaiser M, Whittington MA, Traub RD, Cunningham MO. A nonsynaptic mechanism underlying interictal discharges in human epileptic neocortex. Proc Natl Acad Sci USA 107: 338-343, 2010.
76. Salazar AM, Jabbari B, Vance SC, Grafman J, Amin D, Dillon JD. Epilepsy after penetrating head injury. I. Clinical correlates: a report of the vietnam head injury study. Neurology 35: 1406-1414, 1985.
77. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15: 8234-8245, 1995.
78. Scharfman HE. The neurobiology of epilepsy. Curr Neurol Neurosci Rep 7: 1849-1857, 2008.
79. Schmidt-Heiber C, Jonas P, Bischofberger J. Action Potential initiation and propagation in hippocampal mossy fibre axons. J Physiol 586: 1849-1857, 2008.
80. Schmitz D, Schuchmann S, Fisahn A, Draguhn A, Buhl EH, Petrasch-Parwez E, Dermietzel R, Heinemann U, Traub RD. Axo-axonal coupling: A novel mechanism for ultrafast neuronal communication. Neuron 31: 831-840, 2001.
81. Schubert D, Kötter R, Luhmann HJ, Staiger JF. Morphology, electrophys-iology and functional input connectivity of pyramidal neurons characterizes a genuine layer Va in the primary somatosensory cortex. Cereb Cortex 16: 223-236, 2006.
82. Scorcioni R, Polavaram S, Axcoli GA. L-measure: a web-accessible tool for the analysis, comparison and search of digital reconstructions of neuronal morphologies. Nat Protoc 3: 866-876, 2008.
83. Shepherd GMG, Svoboda K. Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25: 5670-5679, 2005.
84. Shu Y, Duque A, Yu Y, Haider B, McCormick DA. Properties of action-potential initiation in neocortical pyramidal cells: Evidence from whole cell axon recordings. J Neurophysiol 97: 746-760, 2007a.
85. Shu Y, Hasenstaub A, Duque A, Yu Y, McCormick DA. Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441: 761-765, 2006.
86. + current. Proc Natl Acad Sci USA 104: 11453-11458, 2007b.
87. Skoglund TS, Pascher R, Berthold CH. Heterogeneity in the columnar number of neurons in different neocortical areas in the rat. Neurosci Lett 208: 97-100, 1996.
88. Sloper JJ, Powell TP. A study of the axon initial segment and proximal axon of neurons in the primate motor and somatic sensory cortices. Philos Trans R Soc Lond B Biol Sci 285: 173-197, 1979.
89. Staba RJ, Bergmann PC, Barth DS. Dissociation of slow waves and fast oscillations above 200 Hz during GABA application in rat somatosensory cortex. J Physiol 561: 205-214, 2004a.
90. Staba RJ, Wilson CL, Bragin A, Jhung D, Fried I, Engel J Jr. High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann Neurol 56: 108-115, 2004b.
91. Stacey WC, Lazarewicz MT, Litt B. Synaptic noise and physiological coupling generate high-frequency oscillations in a hippocampal computational model. J Neurophysiol 102: 2342-2357, 2009.
92. Staiger JF, Flagmeyer I, Schubert D, Zillis K, Kotter R, Luhmann H. Functional diversity of layer IV spiny neurons in rat somatosensory cortex: Quantitative morphology of electrophysiologically characterized and biocy- tin labeled cells. Cereb Cortex 14: 690-701, 2004.
93. Steriade M, Nuñez A, Amzica F. A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252-3265, 1993.
94. Steriade M, Timofeev I, Grenier F. Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969-1985, 2001.
95. Sutor B, Hagerty T. Involvement of gap junctions in the development of the neocortex. Biochim Biophys Acta 1719: 59-68, 2005.
96. Teskey GC, Valentine PA. Post-activation potentiation in the neocortex of awake freely moving rats. Neurosci Biobehav Rev 22: 195-207, 1998.
97. Timofeev I, Grenier F, Steriade M. Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc Natl Acad Sci USA 98: 1924-1929, 2001.
98. Traub R. Fast oscillations and epilepsy. Epilepsy Curr 3: 77-79, 2003.
99. Traub RD, Contreras D, Cunningham MO, Murray H, LeBeau FE, Roopun A, Bibbig A, Wilent WB, Higley MJ, Whittington MA. Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. J Neurophysiol 93: 2194-2232, 2005a.
100. Traub RD, Contreras D, Whittington MA. Combined experimental/simulation studies of cellular and network mechanisms of epileptogenesis in vitro and in vivo. J Clin Neurophysiol 22: 330-342, 2005b.
101. Traub RD, Cunningham MO, Gloveli T, LeBeau FE, Bibbig A, Buhl EH, Whittington MA. GABAenhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations. Proc Natl Acad Sci USA 100: 11047-11052, 2003a.
102. Traub RD, Duncan R, Russell AJC, Baldeweg T, Tu Y, Cunningham MO, Whittington MA. Spatiotemporal patterns of electrocorticographic very fast oscillations (>80 Hz) consistent with a network model based on electrical coupling between principal neurons. Epilepsia 51: 1587-1597, 2010.
103. Traub RD, Pais I, Bibbig A, LeBeau FE, Buhl EH, Hormuzdi SG, Monyer H, Whittington MA. Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations. Proc Natl Acad Sci USA 100: 1370-1374, 2003b.
104. Traub RD, Schmitz D, Jefferys JG, Draguhn A. High-frequency population oscillations are predicted to occur in hippocampal pyramidal neuronal networks interconnected by axoaxonal gap junctions. Neuroscience 92: 407-426, 1999.
105. Traub RD, Whittington MA, Buhl EH, LeBeau FE, Bibbig A, Boyd S, Cross H, Baldeweg T. A possible role for gap junctions in generation of very fast EEG oscillations preceding the onset of, and perhaps initiating, seizures. Epilepsia 42: 153-170, 2001.
106. Tsumoto T. Long-term potentiation and depression in the cerebral neocortex. Jpn J Physiol 40: 573-593, 1990.
107. Tuckwell HC. Introduction to Theoretical Neurobiology: Volume 1, Linear Cable Theory and Dendritic Structure. Cambridge, UK: Cambridge University Press, 1988.
108. Urrestarazu E, Chander R, Dubeau F, Gotman J. Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. Brain 130: 2354-2366, 2007.
109. Wang W, Degenhart AD, Collinger JL, Vinjamuri R, Sudre GP, Adel-son PD, Holder DL, Leuthardt EC, Moran DW, Boninger ML, Schwartz AB, Crammond DJ, Tyler-Kabara EC, Weber DJ. Human motor cortical activity recorded with micro-ECoG electrodes, during individual finger movements. Conf Proc IEEE Eng Med Biol Soc 2009: 586-589, 2009a.
110. Wang Y, Barakat A, Zhou H. Electrotonic coupling between pyramidal neurons in the neocortex. PLos One 5: e10253, 2010.
111. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H. Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12: 395-410, 2002.
112. Wang Y, Zhang G, Zhou H, Barakat A, Querfurth H. Opposite effects of low and high doses of A /342 on electrical network and neuronal excitability in the rat prefrontal cortex. PLos One 4: e8366, 2009b.
113. Waxman SG, Kocsis JD, Stys PK. The Axon: Structure, Function, Pathophysiology. Oxford, UK: Oxford University Press, 1995.
114. Worrell GA, Gardner AB, Stead SM, Hu S, Goerss S, Cascino GJ, Meyer FB, Marsh R, Litt B. High frequency oscillations in human temporal lobe: Simultaneous microwire and clinical macroelectrode recordings. Brain 131: 928-937, 2008.
115. Worrell GA, Parish L, Cranstoun SD, Jonas R, Baltuch G, Litt B. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127: 1496-1506, 2004.
116. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15: 30-46, 1995.