Shortest loops are pacemakers in random networks of electrically coupled axons

Frontiers in Computational Neuroscience

Volumn , Issue MARCH 2012, 2012, Pages 1-23

  Vladimirov, Nikita ^a   Tu, Yuhai ^a   Traub, Roger D ^a  

^a IBM T J WATSON RESEARCH CENTER   (United States)

Author keywords

Axon; Gap junction; Loop; Network; Pacemaker; Pyramidal neuron

Indexed keywords

AXON; BRAIN ACTIVITY; CA1 PYRAMIDAL NEURON; CELLULAR AUTOMATON MODELS; CONTROL LOOP; COUPLED CELLS; FREQUENCY OF OSCILLATION; GAP JUNCTIONS; HIGH FREQUENCY OSCILLATIONS; KEY FACTORS; LOOP; LOOP STATISTICS; NETWORK CONNECTIVITY; NETWORK OSCILLATIONS; NETWORK SIZE; OSCILLATION PERIODS; PYRAMIDAL NEURON; RANDOM NETWORK; SPIKE PROPAGATION; TYPE II;

CELLULAR AUTOMATA; NETWORKS (CIRCUITS); PACEMAKERS;

COMPUTER SIMULATION;

ARTICLE; CONTROLLED STUDY; DENDRITE; ELECTROENCEPHALOGRAM; GAP JUNCTION; HIGH FREQUENCY OSCILLATION; HIPPOCAMPAL CA1 REGION; NERVE FIBER; PYRAMIDAL NERVE CELL; SIMULATION;

EID: 84859030638     PISSN: 16625188     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncom.2012.00017     Document Type: Article

References (55)

1. Engel Jr, J., Bragin, A., Staba, R., and Mody, I.: High-frequency oscillations: What is normal and what is not? Epilepsia 50, 598-604 (2009)
2. Bragin, A., Engel Jr, J., and Staba, R.: High-frequency oscillations in epileptic brain. Current Opinion in Neurology 23, 151 (2010)
3. Girardeau, G. and Zugaro, M.: Hippocampal ripples and memory consolidation. Current Opinion in Neurobiology (2011)
4. Buzsaki, G., Horvath, Z., Urioste, R., Hetke, J., and Wise, K.: High-frequency network oscillation in the hippocampus. Science 256, 1025 (1992)
5. Ylinen, A., Bragin, A., Nadasdy, Z., Jando, G., Szabo, I., Sik, A., and Buzsaki, G.: Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. The Journal of Neuroscience 15, 30-46 (1995)
6. Chrobak, J. and Buzsaki, G.: High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. The Journal of Neuroscience 16, 3056-3066 (1996)
7. Skaggs, W., McNaughton, B., Permenter, M., Archibeque, M., Vogt, J., Amaral, D., and Barnes, C.: EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. Journal of Neurophysiology 98, 898-910 (2007)
8. Maier, N., Nimmrich, V., and Draguhn, A.: Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. The Journal of Physiology 550, 873-887 (2003)
9. Buzsáki, G.: Memory consolidation during sleep: a neurophysiological perspective. Journal of Sleep Research 7, 17-23 (1998)
10. Axmacher, N., Elger, C., and Fell, J.: Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131, 1806 (2008)
11. Bragin, A., Engel, J., Wilson, C. L., Fried, I., and Buzski, G.: High-frequency oscillations in human brain. Hippocampus 9, 137-142 (1999)
12. Bragin, A., Mody, I., Wilson, C. L., and Engel, J.: Local Generation of Fast Ripples in Epileptic Brain. The Journal of Neuroscience 22, 2012-2021 (2002)
13. Draguhn, A., Traub, R., Schmitz, D., and Jefferys, J.: Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394, 189-192 (1998)
14. Traub, R. D., Schmitz, D., Jefferys, J. G. R., and 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)
15. Traub, R. and Bibbig, A.: A model of high-frequency ripples in the hippocampus based on synaptic coupling plus axon-axon gap junctions between pyramidal neurons. The Journal of Neuroscience 20, 2086 (2000)
16. Traub, R., Duncan, R., Russell, A., Baldeweg, T., Tu, Y., Cunningham, M., and Whittington, M.: 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)
17. Traub, R., Cunningham, M., and Whittington, M.: 2011 Special Issue: Chemical synaptic and gap junctional interactions between principal neurons: Partners in epileptogenesis. Neural Networks 24, 515-525 (2011)
18. Traub, R. and Whittington, M.: Cortical oscillations in health and disease. Oxford University Press (2010). ISBN 0195342798
19. Traub, R., Whittington, M., Buhl, E., LeBeau, F., Bibbig, A., Boyd, S., Cross, H., and 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)
20. Traub, R., Draguhn, A., Whittington, M., Baldeweg, T., Bibbig, A., Buhl, E., and Schmitz, D.: Axonal gap junctions between principal neurons: a novel source of network oscillations, and perhaps epileptogenesis. Reviews in the Neurosciences 13, 1-30 (2002)
21. Roopun, A. K., Simonotto, J. D., Pierce, M. L., Jenkins, A., Nicholson, C., Schofield, I. S., Whittaker, R. G., Kaiser, M., Whittington, M. A., Traub, R. D., and Cunningham, M. O.: A nonsynaptic mechanism underlying interictal discharges in human epileptic neocortex. Proceedings of the National Academy of Sciences 107, 338-343 (2010)
22. Söhl, G., Maxeiner, S., and Willecke, K.: Expression and functions of neuronal gap junctions. Nature Reviews Neuroscience 6, 191-200 (2005)
23. Dere, E. and Zlomuzica, A.: The role of gap junctions in the brain in health and disease. Neuroscience & Biobehavioral Reviews 36, 206-217 (2011)
24. Phelan, P., Goulding, L., Tam, J., Allen, M., Dawber, R., Davies, J., and Bacon, J.: Molecular mechanism of rectification at identified electrical synapses in the Drosophila giant fiber system. Current Biology 18, 1955-1960 (2008)
25. Lewis, T. J. and Rinzel, J.: Self-organized synchronous oscillations in a network of excitable cells coupled by gap junctions. Network: Computation in Neural Systems 11, 299-320 (2000)
26. Vladimirov, N., Traub, R., and Tu, Y.: Wave Speed in Excitable Random Networks with Spatially Constrained Connections. PloS One 6, e20536 (2011)
27. Munro, E. and Boergers, C.: Mechanisms of very fast oscillations in networks of axons coupled by gap junctions. Journal of Computational Neuroscience 28, 539-555 (2010). 10.1007/s10827-010-0235-6
28. Tseng, S., Tsai, L., and Yeh, S.: Induction of high-frequency oscillations in a junction-coupled network. The Journal of Neuroscience 28, 7165 (2008)
29. Tamamaki, N. and Nojyo, Y.: Crossing fiber arrays in the rat hippocampus as demonstrated by three-dimensional reconstruction. The Journal of Comparative Neurology 303, 435-442 (1991)
30. Scorcioni, R. and Ascoli, G.: Algorithmic reconstruction of complete axonal ar- borizations in rat hippocampal neurons. Neurocomputing 65, 15-22 (2005)
31. Traub, R., Contreras, D., Cunningham, M., Murray, H., LeBeau, F., Roopun, A., Bibbig, A., Wilent, W., Higley, M., and Whittington, M.: Single-column thalamo- cortical network model exhibiting gamma oscillations, sleep spindles, and epilepto- genic bursts. Journal of Neurophysiology 93, 2194 (2005)
32. Carnevale, N. and Hines, M.: The NEURON book. Cambridge University Press (2006)
33. Cuntz, H., Forstner, F., Borst, A., and Hausser, M.: One rule to grow them all: a general theory of neuronal branching and its practical application. PLoS computa- tional biology 6, e1000877 (2010)
34. Strogatz, S.: Exploring complex networks. Nature 410, 268-276 (2001)
35. Dorogovtsev, S. N., Goltsev, A. V., and Mendes, J. F. F.: Critical phenomena in complex networks. Rev Mod Phys 80, 1275-1335 (2008)
36. Johnson, D.: Finding all the elementary circuits of a directed graph. Siam J Comput 4, 77-84 (1975)
37. Raastad, M. and Shepherd, G. M. G.: Single-axon action potentials in the rat hippocampal cortex. The Journal of Physiology 548, 745-752 (2003)
38. Popovic, M., Foust, A., McCormick, D., and Zecevic, D.: The spatio-temporal characteristics of action potential initiation in layer 5 pyramidal neurons: a voltage imaging study. The Journal of Physiology 589, 4167-4187 (2011)
39. Traub, R., Bibbig, A., Fisahn, A., LeBeau, F., Whittington, M., and Buhl, E.: A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. European Journal of Neuroscience 12, 4093-4106 (2000)
40. Huang, X., Troy, W., Yang, Q., Ma, H., Laing, C., Schiff, S., and Wu, J.: Spiral waves in disinhibited mammalian neocortex. The Journal of Neuroscience 24, 9897 (2004)
41. Huang, X., Xu, W., Liang, J., Takagaki, K., Gao, X., and Wu, J.: Spiral wave dynamics in neocortex. Neuron 68, 978-990 (2010)
42. Viventi, J., Kim, D., Vigeland, L., Frechette, E., Blanco, J., Kim, Y., Avrin, A., Tiruvadi, V., Hwang, S., Vanleer, A., et al.: Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity in vivo. Nature Neuroscience 1599-1605 (2011)
43. Sheikh, F., Ross, R., and Chen, J.: Cell-Cell Connection to Cardiac Disease. Trends in Cardiovascular Medicine 19, 182-190 (2009)
44. Weingart, R. and Maurer, P.: Action potential transfer in cell pairs isolated from adult rat and guinea pig ventricles. Circulation Research 63, 72-80 (1988)
45. Bub, G., Shrier, A., and Glass, L.: Global organization of dynamics in oscillatory heterogeneous excitable media. Physical Review Letters 94, 28105 (2005)
46. Whittington, M., Traub, R., Jefferys, J., et al.: Synchronized oscillations in in- terneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612-615 (1995)
47. Traub, R., Whittington, M., Stanfords, I., and Jefferys, J.: A mechanism for gen- eration of long-range synchronous fast oscillations in the cortex. Nature 383, 17 (1996)
48. Jones, M. and Barth, D.: Effects of bicuculline methiodide on fast (> 200 Hz) electrical oscillations in rat somatosensory cortex. Journal of Neurophysiology 88, 1016 (2002)
49. Nimmrich, V., Maier, N., Schmitz, D., and Draguhn, A.: Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. The Journal of Physiology 563, 663-670 (2005)
50. Maier, N., Tejero-Cantero, A., Dorrn, A., Winterer, J., Beed, P., Morris, G., Kempter, R., Poulet, J., Leibold, C., and Schmitz, D.: Coherent Phasic Excitation during Hippocampal Ripples. Neuron 72, 137-152 (2011)
51. Hamzei-Sichani, F., Kamasawa, N., Janssen, W., Yasumura, T., Davidson, K., Hof, P., Wearne, S., Stewart, M., Young, S., Whittington, M., et al.: Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze-fracture replica immunogold labeling. Proceedings of the National Academy of Sciences 104, 12548 (2007)
52. Schmitz, D., Schuchmann, S., Fisahn, A., Draguhn, A., Buhl, E., Petrasch-Parwez, E., Dermietzel, R., Heinemann, U., and Traub, R.: Axo-Axonal Coupling: A Novel Mechanism for Ultrafast Neuronal Communication. Neuron 31, 831-840 (2001)
53. Memmesheimer, R.: Quantitative prediction of intermittent high-frequency oscillations in neural networks with supralinear dendritic interactions. Proceedings of the National Academy of Sciences 107, 11092 (2010)
54. Foffani, G., Uzcategui, Y., Gal, B., and Menendez de la Prida, L.: Reduced spike- timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron 55, 930-941 (2007)
55. Ibarz, J., Foffani, G., Cid, E., Inostroza, M., and de la Prida, L.: Emergent dy- namics of fast ripples in the epileptic hippocampus. The Journal of Neuroscience 16249-16261 (2010)