Communication through Resonance in Spiking Neuronal Networks

PLoS Computational Biology

Volumn 10, Issue 8, 2014, Pages

  Hahn, Gerald ^a   Bujan, Alejandro F ^b   Frégnac, Yves ^a   Aertsen, Ad ^b   Kumar, Arvind ^b  

^a Unite de Neurosciences Integratives et Computationnelles   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; LOCKS (FASTENERS); NEURAL NETWORKS; NEURONS;

BRAIN AREAS; CONNECTED NETWORKS; CORTEXES; CORTICAL REGIONS; DISTRIBUTED NETWORKS; LOCAL OSCILLATION; NEURONAL ACTIVITIES; ROUTING MODEL; SPIKING NEURONAL NETWORKS; STRONGLY CONNECTED;

RESONANCE;

ALGORITHM; ARTICLE; BRAIN CORTEX; MATHEMATICAL ANALYSIS; MATHEMATICAL MODEL; NERVE CELL NETWORK; NERVE PROJECTION; NEUROMODULATION; NEUROTRANSMISSION; OSCILLATION; PERIODICITY; PROBABILITY; SPIKE WAVE; SYNAPSE; ACTION POTENTIAL; BIOLOGICAL MODEL; BIOLOGY; FEEDBACK SYSTEM; NERVE CELL; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; COMPUTATIONAL BIOLOGY; FEEDBACK; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; SYNAPTIC TRANSMISSION;

EID: 84918780978     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003811     Document Type: Article

References (70)

1. Azouz R, Gray CM, (2000) Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci U S A 97: 8110–8115.
2. Lger JF, Stern EA, Aertsen A, Heck D, (2005) Synaptic integration in rat frontal cortex shaped by network activity. J Neurophysiol 93: 281–293.
3. Bruno RM, Sakmann B, (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312: 1622–1627.
4. Rossant C, Leijon S, Magnusson AK, Brette R, (2011) Sensitivity of noisy neurons to coincident inputs. J Neurosci 31: 17193–17206.
5. Abeles M, (1982) Role of the cortical neuron: integrator or coincidence detector? Isr J Med Sci 18: 83–92.
6. Abeles M (1991) Corticonics: Neural Circuits of the Cerebral Cortex. Cambridge University Press, first edition.
7. Diesmann M, Gewaltig MO, Aertsen A, (1999) Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529–533.
8. Reyes AD, (2003) Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci 6: 593–599.
9. Kumar A, Rotter S, Aertsen A, (2008) Conditions for propagating synchronous spiking and asynchronous firing rates in a cortical network model. J Neurosci 28: 5268–5280.
10. Rosenbaum R, Trousdale J, Josic K, (2010) Pooling and correlated neural activity. Front Comput Neurosci 4: 9 doi: 10.3389/fncom.2010.00009
11. Braitenberg V, Schüz A (1998) Cortex: Statistics and Geometry of Neuronal Connectivity. Heidelberg, Germany: Springer-Verlag, second edition, 249 pp.
12. Matsumura M, Chen Df, Sawaguchi T, Kubota K, Fetz EE, (1996) Synaptic interactions between primate precentral cortex neurons revealed by spike-triggered averaging of intracellular membrane potentials in vivo. J Neurosci 16: 7757–7767.
13. Schrader S, Grüen S, Diesmann M, Gerstein GL, (2008) Detecting synfire chain activity using massively parallel spike train recording. J Neurophysiol 100: 2165–2176.
14. Kumar A, Rotter S, Aertsen A, (2010) Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci 11: 615–627.
15. Fries P, (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32: 209–224.
16. Engel AK, Fries P, Singer W, (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2: 704–716.
17. Fries P, (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9: 474–480.
18. Womelsdorf T, Fries P, (2007) The role of neuronal synchronization in selective attention. Curr Opin Neurobiol 17: 154–160.
19. Uhlhaas PJ, Pipa G, Lima B, Melloni L, Neuenschwander S, et al. (2009) Neural synchrony in cortical networks: history, concept and current status. Front Integr Neurosci 3: 17.
20. Ledoux E, Brunel N, (2011) Dynamics of networks of excitatory and inhibitory neurons in response to time-dependent inputs. Front Comput Neurosci 5: 25.
21. Gerstner W, Kistler WM (2002) Spiking Neuron Models: Single Neurons, Populations, Plasticity. 494 pp.
22. Gewaltig MO, Diesmann M, (2007) Nest (neural simulation tool). Scholarpedia 2: 1430.
23. Eppler JM, Helias M, Muller E, Diesmann M, Gewaltig MO, (2008) Pynest: A convenient interface to the nest simulator. Front Neuroinform 2: 12.
24. Hunter JD, (2007) Matplotlib: A 2d graphics environment. Comput Sci Eng 9: 90–95.
25. van Vreeswijk C, Sompolinsky H, (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274: 1724–1726.
26. Brunel N, (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8: 183–208.
27. Softky WR, Koch C, (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random epsps. J Neurosci 13: 334–350.
28. Barth AL, Poulet JFA, (2012) Experimental evidence for sparse firing in the neocortex. Trends Neurosci 35: 345–355.
29. Ecker AS, Berens P, Keliris GA, Bethge M, Logothetis NK, et al. (2010) Decorrelated neuronal firing in cortical microcircuits. Science 327: 584–587.
30. Harris KD, Thiele A, (2011) Cortical state and attention. Nat Rev Neurosci 12: 509–523.
31. Borg-Graham LJ, Monier C, Fregnac Y, (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393: 369–373.
32. Vida I, Bartos M, Jonas P, (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49: 107–117.
33. Bartos M, Vida I, Jonas P, (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8: 45–56.
34. Brunel N, Wang XJ, (2003) What determines the frequency of fast network oscillations with irregular neural discharges? i. synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90: 415–430.
35. Wang XJ, (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90: 1195–1268.
36. Gray CM, König P, Engel AK, Singer W, et al. (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334–337.
37. Burns SP, Xing D, Shapley RM, (2011) Is gamma-band activity in the local field potential of v1 cortex a “clock” or filtered noise? J Neurosci 31: 9658–9664.
38. Xing D, Shen Y, Burns S, Yeh CI, Shapley R, et al. (2012) Stochastic generation of gamma-band activity in primary visual cortex of awake and anesthetized monkeys. J Neurosci 32: 13873–13880a.
39. Nikoli D, Fries P, Singer W, (2013) Gamma oscillations: precise temporal coordination without a metronome. Trends Cogn Sci 17: 54–55.
40. Kumar A, Schrader S, Aertsen A, Rotter S, (2008) The high-conductance state of cortical networks. Neural Comput 20: 1–43.
41. Steriade M, Timofeev I, Grenier F, (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969–1985.
42. Mehring C, Hehl U, Kubo M, Diesmann M, Aertsen A, (2003) Activity dynamics and propagation of synchronous spiking in locally connected random networks. Biol Cybern 88: 395–408.
43. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, et al. (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663–667.
44. Uhlhaas P, Singer W, (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52: 155–168.
45. Llinás RR, (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654–1664.
46. Steriade M, (2000) Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101: 243–276.
47. Dwyer J, Lee H, Martell A, van Drongelen W, (2012) Resonance in neocortical neurons and networks. Eur J Neurosci 36: 3698–3708.
48. Izhikevich EM, (2001) Resonate-and-fire neurons. Neural Netw 14: 883–894.
49. Moca VV, Nikolić D, Singer W, Mureşan RC, (2014) Membrane resonance enables stable and robust gamma oscillations. Cerebral Cortex 24: 119–142.
50. Lepousez G, Lledo PM, (2013) Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 80: 1010–1024.
51. Akam T, Kullmann DM, (2010) Oscillations and filtering networks support flexible routing of information. Neuron 67: 308–320.
52. Gewaltig MO, Diesmann M, Aertsen A, (2001) Propagation of cortical synfire activity: survival probability in single trials and stability in the mean. Neural Netw 14: 657–673.
53. Kremkow J, Aertsen A, Kumar A, (2010) Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition. J Neurosci 30: 15760–15768.
54. van Rossum MCW, Turrigiano GG, Nelson SB, (2002) Fast propagation of firing rates through layered networks of noisy neurons. J Neurosci 22: 1956–1966.
55. Vogels TP, Abbott LF, (2005) Signal propagation and logic gating in networks of integrate-and-fire neurons. J Neurosci 25: 10786–10795.
56. Varela F, Lachaux JP, Rodriguez E, Martinerie J, (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2: 229–239.
57. Tallon-Baudry C, (2009) The roles of gamma-band oscillatory synchrony in human visual cognition. Front Biosci 14: 321–332.
58. Vinck M, Womelsdorf T, Fries P (2013) Gamma-band synchronization and information transmission. In: Principles of Neural Coding, CRC Press Taylor & Francis. pp. 449–469.
59. Buzsáki G, Wang XJ, (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35: 203–225.
60. Gregoriou GG, Gotts SJ, Zhou H, Desimone R, (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324: 1207–1210.
61. Bosman CA, Schoffelen J, Brunet N, Oostenveld R, Bastos AM, et al. (2012) Attentional stimulus selection through selective synchronization between monkey visual areas. Neuron 75: 875–888.
62. Roberts MJ, Lowet E, Brunet NM, Ter Wal M, Tiesinga P, et al. (2013) Robust gamma coherence between macaque v1 and v2 by dynamic frequency matching. Neuron 78: 523–536.
63. Ahissar E, Arieli A, (2012) Seeing via miniature eye movements: A dynamic hypothesis for vision. Front Comput Neurosci 6: 89 doi: 10.3389/fncom.2012.00089
64. Landau AN, Fries P, (2012) Attention samples stimuli rhythmically. Curr Biol 22: 1000–1004.
65. Fell J, Axmacher N, (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12: 105–118.
66. Waldert S, Pistohl T, Braun C, Ball T, Aertsen A, et al. (2009) A review on directional information in neural signals for brain-machine interfaces. J Physiol (Paris) 103: 244–254.
67. Akam TE, Kullmann DM, (2012) Efficient communication through coherence requires oscillations structured to minimize interference between signals. PLoS Comput Biol 8: e1002760 doi: 10.1371/journal.pcbi.1002760
68. Munk MH, Roelfsema PR, Knig P, Engel AK, Singer W, (1996) Role of reticular activation in the modulation of intracortical synchronization. Science 272: 271–274.
69. Herculano-Houzel S, Munk MH, Neuenschwander S, Singer W, (1999) Precisely synchronized oscillatory firing patterns require electroencephalographic activation. J Neurosci 19: 3992–4010.
70. Cannon J, McCarthy MM, Lee S, Lee J, Börgers C, et al. (2013) Neurosystems: brain rhythms and cognitive processing. Eur J Neurosci 39: 705–19 doi: 10.1111/ejn.12453