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Far in Space and Yet in Synchrony: Neuronal Mechanisms for Zero-Lag Long-Range Synchronization

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Coherent Behavior in Neuronal Networks

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 3))

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Abstract

Distant neuronal populations are observed to synchronize their activity patterns at zero-lag during certain stages of cognitive acts. This chapter provides an overview of the problem of large-scale synchrony and some of the solutions that have been proposed for attaining long-range coherence in the nervous system despite long conduction delays. We also review in detail the synchronizing properties of a canonical neuronal microcircuit that naturally enhances the isochronous discharge of remote neuronal resources. The basic idea behind this mechanism is that when two neuronal populations relay their activities onto a third mediating population, the redistribution of the dynamics performed by the latter leads to a self-organized and lag-free synchronization among the pools of neurons being relayed. Exploring the physiological relevance of this mechanism, we discuss the role of associative thalamic nuclei and their bidirectional interaction with the neocortex as a relevant physiological structure in which the network module under study is densely embedded. These results are further supported by the recently proposed role of thalamocortical interactions as a substrate for the trans-areal cortical coordination.

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References

  1. Nicolelis M, Ribeiro S (2002) Multielectrode recordings: the next steps. Curr. Opin. Neurobio. 12:602–606

    Article  CAS  Google Scholar 

  2. Singer W, Engel AK, Kreiter AK, Munk MHJ, Neuenschwander S, Roelfsema PR (1997) Neuronal assemblies: necessity, signature and detectability. Trends Cogn. Sci. 1:252–260

    Article  PubMed  CAS  Google Scholar 

  3. Singer W (1999) Neuronal Synchrony: A Versatile Code for the Definition of Relations. Neuron 24:49–65

    Article  PubMed  CAS  Google Scholar 

  4. Varela FJ, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci. 2:299–230

    Article  Google Scholar 

  5. Milner PM (1974) A model for visual shape recognition. Psychol. Rev. 81:521–535

    Article  PubMed  CAS  Google Scholar 

  6. von der Malsburg, C (1981) The correlation theory of brain function. Intern. Rep. 81-2, Dept. of Neurobiology, Max-Planck-Institute for Biophysical Chemistry, Gottingen, Germany

    Google Scholar 

  7. Gray CM, Konig P, Engel AK, Singer W (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338:334–337

    Article  PubMed  CAS  Google Scholar 

  8. Gray CM (1999) The temporal correlation hypothesis of visual feature integration. Neuron 24:31–47

    Article  PubMed  CAS  Google Scholar 

  9. Salinas E, Sejnowski TJ (2000) Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20:6193–6209

    PubMed  CAS  Google Scholar 

  10. Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neuronal information. Nat. Rev. Neurosci. 2:539–550

    Article  PubMed  CAS  Google Scholar 

  11. Castelo-Branco M, Goebel R, Neuenschwander S, Singer W (2000) Neuronal synchrony correlates with surface segregation rules. Nature 405:685–689

    Article  PubMed  CAS  Google Scholar 

  12. Fries P, Roelfsema PR, Engel AK, Konig P, Singer W (1997) Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc. Natl. Acad. Sci. 94:12699–12704

    Article  PubMed  CAS  Google Scholar 

  13. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563

    Article  PubMed  CAS  Google Scholar 

  14. Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A (1998) Synchronization between prefrontal and posterior association cortex during human working memory. Proc. Natl. Acad. Sci. 95:7092–7096

    Article  PubMed  CAS  Google Scholar 

  15. Roelfsema PR, Engel AK, Konig P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157–161

    Article  PubMed  CAS  Google Scholar 

  16. Rodriguez E et al. (1999) Perception’s shadow: long-distance synchronization of human brain activity. Nature 397:430–433

    Article  PubMed  CAS  Google Scholar 

  17. Mima T, Oluwatimilehin T, Hiraoka T, Hallett M (2001) Transient Interhemispheric Neuronal Synchrony Correlates with Object Recognition. J. Neurosci. 21:3942–3948

    PubMed  CAS  Google Scholar 

  18. Uhlhaas PJ et al. (2006) Dysfunctional long-range coordination of neural activity during Gestalt perception in schizofrenia. J. Neurosci. 26:8168–8175

    Article  PubMed  CAS  Google Scholar 

  19. Soteropoulus DS, Baker S (2006) Cortico-cerebellar coherence during a precision grip task in the monkey. J. Neurophysiol. 95:1194–1206

    Article  Google Scholar 

  20. Witham CL, Wang M, Baker S (2007) Cells in somatosensory areas show synchrony with beta oscillations in monkey motor cortex. Eur. J. Neurosci. 26:2677–2686

    Article  PubMed  Google Scholar 

  21. Swadlow HA, Rosene DL, Waxman SG (1978) Characteristics of interhemispheric impulse conduction between the prelunate gyri of the rhesus monkey. Exp. Brain Res. 33:455–467

    Article  PubMed  CAS  Google Scholar 

  22. Swadlow HA (1985) Physiological properties of individual cerebral axons studied in vivo for as long as one year. J. Neurophysiol. 54:1346–1362

    PubMed  CAS  Google Scholar 

  23. Swadlow HA (1994) Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs. J. Neurophysiol. 71:437–453

    PubMed  CAS  Google Scholar 

  24. Miller R (2000) Time and the brain. Harwood Press, Switzerland

    Book  Google Scholar 

  25. Wen Q, Chkolvskii DB (2005) Seggregation of the brain into Gray and White matter: a design minimiying conduction delays. PLoS Comput. Biol. 1:e78

    Article  PubMed  Google Scholar 

  26. Ringo JL, Doty RW, Demeter S, Simard, PY (1994) Time is the essence: A conjecture that hemispheric specialization arises from interhemispheric conduction delay. Cereb. Cortex 4:331–343

    Article  PubMed  CAS  Google Scholar 

  27. Miller R (1996) Axonal conduction time and human cerebal laterality: a psychobiological theory, 1st edn. Harwood Academics Publisher, Amsterdam

    Google Scholar 

  28. Vicente R, Gollo LL, Mirasso CR, Fischer I, Pipa G (2008) Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays. Proc. Natl. Acad. Sci. 105:17157–17162

    Article  PubMed  CAS  Google Scholar 

  29. Fischer I, Vicente R, Buldu JM, Peil M, Mirasso CR, Torrent MC, Garcia-Ojalvo J (2006) Zero-lag long-range synchronization via dynamical relaying. Phys. Rev. Lett. 97:123902

    Article  PubMed  Google Scholar 

  30. Vicente R, Pipa G, Fischer I, Mirasso CR (2007) Zero-lag long range synchronization of neurons is enhanced by dynamical relaying. Lect. Notes Comp. Sci. 4688:904–913

    Article  Google Scholar 

  31. D’Huys O, Vicente R, Erneux T, Danckaert J, Fischer I (2008) Synchronization properties of network motifs: Influence of coupling delay and symmetry. Chaos 18:037116

    Article  PubMed  Google Scholar 

  32. Jones EG (2002) Thalamic circuitry and thalamocortical synchrony. Phil. Trans. R. Soc. Lond. B 357:1659–1673

    Article  Google Scholar 

  33. Shipp S (2003) The functional logic of cortico-pulvinar connections. Phil. Trans. R. Soc. Lond. B 358:1605–1624

    Article  CAS  Google Scholar 

  34. Honey CJ, Kotter R, Breakspear M, Sporns O (2007) Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc. Natl. Acad. Sci. 104:10240–10245

    Article  PubMed  CAS  Google Scholar 

  35. Soleng AF, Raastad M, Andersen P (1998) Conduction latency along CA3 hippocampal axons from the rat. Hippocampus 13:953–961

    Article  Google Scholar 

  36. Swadlow HA, Waxman SG (1975) Observations on impulse conduction along central axons. Proc. Natl. Acad. Sci. 72:5156–5159

    Article  PubMed  CAS  Google Scholar 

  37. Katz B, Miledi R (1965) The measurement of synaptic delay, and the time course of acetylcholine release at the neuromuscular junction. Proc. R. Soc. Lond. Series B, Biol. Sci. 161:483–495

    Article  CAS  Google Scholar 

  38. Shepherd GM (2004) The synaptic organization of the brain. Oxford University Press

    Google Scholar 

  39. Volgushev M, Chistiakova M, Singer W (1998) Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83:15–25

    Article  PubMed  CAS  Google Scholar 

  40. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Behav. Evol. 598:143–153

    CAS  Google Scholar 

  41. Dickson CT, Biella G, de Curtis M (2003) Slow periodic events and their transition to gamma oscillations in the entorhinal cortex of the isolated guinea pig brain. J. Neurophysiol. 900:39–46

    Article  Google Scholar 

  42. Rizzuto DS, Madsen JR, Bromfield EB, Schulze-Bonhage A, Seelig D, Aschenbrenner-Scheibe R, Kahana MJ (2003) Reset of human neocortical oscillations during a working memory task. Proc. Natl. Acad. Sci. 100:7931–7936

    Article  PubMed  CAS  Google Scholar 

  43. Mann EO, Paulsen O (2007) Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 30:343–349

    Article  PubMed  CAS  Google Scholar 

  44. Whittington MA, Doheny HC, Traub RD, LeBeau FEN, Buhl EH (2001) Differential expression of synaptic and nonsynaptic mechanisms underlying stimulus-induced gamma oscillations in vitro. J. Neurosci. 21:1727–1738

    PubMed  CAS  Google Scholar 

  45. Buzsaki G (2006) Rhythms of the brain. Oxford University Press

    Google Scholar 

  46. Bennet MVL, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495–511

    Article  Google Scholar 

  47. Caspar DLD, Goddenough DA, Makowski L, Phillips WC (1977) Gap junction structures. J. Cell Biol. 74:605–628

    Article  PubMed  CAS  Google Scholar 

  48. Draghun A, Traub RD, Schmitz D, Jefferys JGR (1998) Electrical coupling underlies high-frequency oscillations in the hippocampus in vitro. Nature 394:189–192

    Article  Google Scholar 

  49. Traub RD, Kopell N, Bibbig A, Buhl EH, Lebeau FEN, Whittington MA (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J. Neurosci. 21:9478–9486

    PubMed  CAS  Google Scholar 

  50. Kopell N, Ermentrout GB (2004) Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc. Natl. Acad. Sci. 101:15482–15487

    Article  PubMed  CAS  Google Scholar 

  51. Traub RD, Whittington MA, Stanford IM, Jefferys JGR (1996) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621–624

    Article  PubMed  CAS  Google Scholar 

  52. Bibbig A, Traub RD, Whittington MA (2002) Long-range synchronization of gamma and beta oscillations and the plasticity of excitatory and inhibitory synapses: a network model. J. Neurophysiol. 88:1634–1654

    PubMed  Google Scholar 

  53. Lowel S, Singer W (1992) Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science 255:209–212

    Article  PubMed  CAS  Google Scholar 

  54. Knoblauch A, Sommer FT (2003) Synaptic plasticity, conduction delays, and inter-areal phase relations of spike activity in a model of reciprocally connected areas. Neurocomputing 52–54:301–306

    Article  Google Scholar 

  55. Izhikevich E (2006) Polychronization: computation with spikes. Neural Comput. 18:245–282

    Article  PubMed  Google Scholar 

  56. Swindale NV (2003) Neural synchrony, axonal path lengths, and general anesthesia: a hipothesis. Neuroscientist 9:440–445

    Article  PubMed  Google Scholar 

  57. Sporns O, Kotter R (2004) Motifs in brain networks. PLoS Biol. 2:e369

    Google Scholar 

  58. Sporns O, Chialvo D, Kaiser M, Hiltetag CC (2004) Organization, development and function of complex brain networks. Trends Cogn. Sci. 8:418–425

    Article  PubMed  Google Scholar 

  59. Ermentrout, JB (1996) Type I membranes, phase resetting curves, and synchrony. Neural Comp. 8:979–1001

    Article  CAS  Google Scholar 

  60. Reyes AD, Fetz EE (1993) Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J. Neurophysiol. 69:1661–1672

    PubMed  CAS  Google Scholar 

  61. Douglas RJ, Martin KAC (2004) Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27:419–451

    Article  PubMed  CAS  Google Scholar 

  62. Pare D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J. Neurophysiol. 78:1450–1460

    Google Scholar 

  63. Arieli A, Sterkin A, Grinvald A, Aersten A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273:1868–1871

    Article  PubMed  CAS  Google Scholar 

  64. Llinas R, Pare D (1997) Coherent oscillations in specific and nonspecific thalamocortical networks and their role in cognition. In: Steriade M, Jones EG, McCormick DA (eds) Thalamus. Pergamon, New York.

    Google Scholar 

  65. Llinas R, Ribary U, Contreras D, Pedroarena C (1998) The neuronal basis for conciousness. Phil. Trans. R. Soc. Lond. B 353:1841–1849

    Article  CAS  Google Scholar 

  66. Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JPR, Lado F, Mogilner A, Llinas R (1991) Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc. Natl. Acad. Sci. 88:11037–11041

    Article  PubMed  CAS  Google Scholar 

  67. Sherman SM, Guillery, RW (2002) The role of the thalamus in the flow of information to the cortex. Phil. Trans. R. Soc. Lond. B 357:1695–1708

    Article  Google Scholar 

  68. Salami M, Itami C, Tsumoto T, Kimura F (2003) Change of conduction velocity by regional myelination yields to constant latency irrespective of distance between thalamus to cortex. Proc. Natl. Acad. Sci. 100:6174–6179

    Article  PubMed  CAS  Google Scholar 

  69. Engel AK, Kreiter AK, Koenig P, Singer W (1991) Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proc. Natl. Acad. Sci. 88:6048–6052

    Article  PubMed  CAS  Google Scholar 

  70. Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771–774

    Article  PubMed  CAS  Google Scholar 

  71. Fries P (2005) Neuronal communication through neuronal coherence. Trends Cogn. Sci. 9:474–480

    Article  PubMed  Google Scholar 

  72. Hodgkin AL, Huxley AF (1952) A quantitative description of the membrane current and its application to conduction and excitation in nerve. J. Physiol. 117:500–544

    PubMed  CAS  Google Scholar 

  73. Brunel N (2000) Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons. J. Comput. Neurosci. 8:183–208

    Article  PubMed  CAS  Google Scholar 

  74. Brette R, et al (2007) Simulation of networks of spiking neurons: A review of tools and strategies. J. Comput. Neurosci. 23:349–398

    Article  PubMed  Google Scholar 

  75. Pikovsky A, Rosenblum M, Kurths J (2002) Synchronization: A universal Concept in Nonlinear Science. Cambridge University Press

    Google Scholar 

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Acknowledgments

The authors would like to thank Wolf Singer, Carl van Vreeswijk, Christopher J. Honey, and Nancy Kopell for fruitful discussions. This work was partially supported by the Hertie Foundation, the European Commission Project GABA (FP6-NEST contract 043309), and the Spanish MCyT and Feder under Project FISICO (FIS-2004-00953). R.V. and G.P. are also with the Frankfurt Institute for Advanced Studies (FIAS).

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Vicente, R., Gollo, L.L., Mirasso, C.R., Fischer, I., Pipa, G. (2009). Far in Space and Yet in Synchrony: Neuronal Mechanisms for Zero-Lag Long-Range Synchronization. In: Josic, K., Rubin, J., Matias, M., Romo, R. (eds) Coherent Behavior in Neuronal Networks. Springer Series in Computational Neuroscience, vol 3. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0389-1_8

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