Neuronal Synchronization, Attention Orienting, and Primary Consciousness

  • Lawrence M. WardEmail author


How does the brain implement cognitive processes? Part of the answer is specialization of function in particular regions. But complex cognitive processes involved in attention, memory, and consciousness require the coordinated activity of several or many of these specialized regions. Moreover, the specialized regions often (always?) exhibit different functions depending on the particular subset of other regions with which they are interacting. Finally, because cognitive tasks vary dramatically over timescales of hundreds of milliseconds to seconds, the functionally relevant regional networks must form and dissolve over these short timescales, which are too short to accommodate mechanisms such as synaptic modification via spike-timing dependent plasticity. It has been suggested that oscillatory synchronization of neural activity provides a mechanism whereby networks of functionally specialized brain regions could function transiently on such timescales. This chapter begins to make the case that for attention and consciousness, at least, this mechanism is deeply involved in implementing the required functional networks. It also briefly considers the implications of the role of oscillatory neural synchronization in cognition for the global workspace.


Inferior Frontal Gyrus Gamma Band Binocular Rivalry Alpha Power Target Interval 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This chapter and much of the research described were sponsored by Discovery Grant A9958 from the Natural Sciences and Engineering Research Council (NSERC) of Canada. I thank the coauthors of the various papers emanating from the laboratories of myself and my collaborators whose results I describe here for their vital contributions to this research program.


  1. Akam T, Kullman DM (2014) Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat Rev Neurosci 15:111–122CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aru J, Aru J, Priesemann V, Wibral M, Lana L, Pipa G, Singer W, Vicente R (2015) Untangling cross-frequency coupling in neuroscience. Curr Opin Neurobiol 31:51–61CrossRefPubMedGoogle Scholar
  3. Azouz R, Gray CM (2000) Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci USA 97:8110–8115CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baars BJ (1997) In the theatre of consciousness. J Conscious Stud 4(4):521–535Google Scholar
  5. Bastos AM, Vezoli J, Fries P (2015) Communication through coherence with inter-areal delays. Curr Opin Neurobiol 31:173–180CrossRefPubMedGoogle Scholar
  6. Bedo N, Ribary U, Ward LM (2014) Fast dynamics of cortical effective connectivity during word reading. PLoS One 9(2), e88940 (1–13)CrossRefPubMedPubMedCentralGoogle Scholar
  7. Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403:309–312CrossRefPubMedGoogle Scholar
  8. Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput 11:1621–1671CrossRefPubMedGoogle Scholar
  9. Buzsáki G (2006) Rhythms of the brain. Oxford University Press, New YorkCrossRefGoogle Scholar
  10. Buzsáki G, Schomberg EW (2015) What does gamma coherence tell us about inter-regional neural communication? Nat Neurosci 18:1–7CrossRefGoogle Scholar
  11. Buzsáki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225CrossRefPubMedPubMedCentralGoogle Scholar
  12. Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506–515CrossRefPubMedPubMedCentralGoogle Scholar
  13. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626CrossRefPubMedPubMedCentralGoogle Scholar
  14. Corbetta M, Shulman GL (2002) Control of goal-driven and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215CrossRefPubMedGoogle Scholar
  15. Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:308–324CrossRefGoogle Scholar
  16. Cosmelli D, David O, Lachaux JP, Martinerie J, Garnero L et al (2004) Waves of consciousness: ongoing cortical patterns during binocular rivalry. Neuroimage 23:128–140CrossRefPubMedGoogle Scholar
  17. Dehaene S, Cohen L (2011) The unique role of the visual word form area in reading. Trends Cogn Sci 15:254–262CrossRefPubMedGoogle Scholar
  18. Dehaene S, Naccache J (2001) Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 79:1–37CrossRefPubMedGoogle Scholar
  19. Doesburg SM, Ward LM (2007) Long-distance alpha-band MEG synchronization maintains selective visual attention. Int Congr Ser 1300:551–554CrossRefGoogle Scholar
  20. Doesburg SM, Ward LM (2009) Synchronization between sources: emerging methods for understanding large-scale functional networks in the human brain. In: Perez-Velazquez J-L, Wennberg R (eds) Coordinated activity in the brain. Springer, New York, pp 25–42CrossRefGoogle Scholar
  21. Doesburg SM, Kitajo K, Ward LM (2005) Increased gamma-band synchrony precedes switching of conscious perceptual objects in binocular rivalry. Neuroreport 2:229–239Google Scholar
  22. Doesburg SM, Herdman A, Ward LM (2007) MEG reveals synchronous neural network for visuospatial attention. Poster presented at CNS Meeting, New York CityGoogle Scholar
  23. Doesburg SM, Roggeveen AB, Kitajo K, Ward LM (2008) Large-scale gamma-band phase synchronization and selective attention. Cereb Cortex 18(2):386–396. doi: 10.1093/cercor/bhm073 CrossRefPubMedGoogle Scholar
  24. Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009a) From local inhibition to long-range integration: a functional dissociation of alpha-band synchronization across cortical scales in visuospatial attention. Brain Res 1303C:97–110. doi: 10.1016/j.brainres.2009.09.069 CrossRefGoogle Scholar
  25. Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009b) Rhythms of consciousness: binocular rivalry reveals large-scale oscillatory network dynamics mediating visual perception. PLoS One 7, e6142 (1–14)CrossRefGoogle Scholar
  26. Doesburg SM, Green JJ, McDonald JJ, Ward LM (2012) Theta modulation of inter-regional gamma synchronization during auditory attention control. Brain Res 1431:77–85CrossRefPubMedGoogle Scholar
  27. Doesburg SM, Bedo N, Ward LM (2016) Top-down alpha oscillatory network interactions during visuospatial attention orienting. NeuroImage 132:512–519Google Scholar
  28. Drewes AM, Sami SAK, Dimcevski G, Nielsen KD, Funch-Jensen P, Valeriani M, Arendt-Nielsen L (2006) Cerebral processing of painful oesophageal stimulation: a study based on independent component analysis of the EEG. Gut 55:619–629CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480CrossRefPubMedGoogle Scholar
  30. Fries P, Roelfsema PR, Engel AK, Königl P, Singer W (1997) Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc Natl Acad Sci USA 94:12699–12704CrossRefPubMedPubMedCentralGoogle Scholar
  31. Green JJ, McDonald JJ (2008) Electrical neuroimaging reveals timing of attentional control activity in human brain. PLoS Biol 6(4), e81CrossRefPubMedCentralGoogle Scholar
  32. Green JJ, McDonald JJ (2009) A practical guide to beamformer source reconstruction for EEG. In: Handy TC (ed) Brain signal analysis: advances in neuroelectric and neuromagnetic methods. The MIT Press, Cambridge, MA, pp 79–98CrossRefGoogle Scholar
  33. Green JJ, Doesburg SM, Ward LM, McDonald JJ (2011) Electrical neuroimaging of voluntary audio-spatial attention: evidence for a supramodal attention control network. J Neurosci 31:3560–3564CrossRefPubMedGoogle Scholar
  34. Greenwood PE, McDonnell MD, Ward LM (2015) Dynamics of gamma bursts in local field potentials. Neural Comput 27:74–103CrossRefPubMedGoogle Scholar
  35. Gregoriou GG, Paneria S, Sapountzis P (2015) Oscillatory synchrony as a mechanism of attentional processing. Brain Res 1626:165–182CrossRefPubMedGoogle Scholar
  36. Gross J, Schmitz F, Schnitzler I, Kessler K, Shapiro K et al (2004) Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. Proc Natl Acad Sci USA 101:13050–13055CrossRefPubMedPubMedCentralGoogle Scholar
  37. Grossberg S (2000) The complementary brain: unifying brain dynamics and modularity. Trends Cogn Sci 4:233–246CrossRefPubMedGoogle Scholar
  38. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595–601CrossRefPubMedGoogle Scholar
  39. Kang K, Shelley M, Henrie JA, Shapley R (2010) LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback. J Comput Neurosci 29:495–507CrossRefPubMedGoogle Scholar
  40. Kanwisher N (2006) What’s in a face? Science 311:617–618CrossRefPubMedGoogle Scholar
  41. Koch C, Tsuchiya N (2006) Attention and consciousness: two distinct brain processes. Trends Cogn Sci 11:16–22CrossRefPubMedGoogle Scholar
  42. Lamme VAF (2003) Why visual attention and awareness are different. Trends Cogn Sci 7:12–18CrossRefPubMedGoogle Scholar
  43. Lamme VAF, Roelfsema PR (2000) The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci 23:571–579CrossRefPubMedGoogle Scholar
  44. Llinás R, Ribary U, Contreras D, Pedroarena C (1998) The neuronal basis for consciousness. Philos Trans R Soc London Ser B 353:1841–1849CrossRefGoogle Scholar
  45. Logothetis N, Schall JD (1989) Neuronal correlates of subjective visual perception. Science 245:761–763CrossRefPubMedGoogle Scholar
  46. Lumer ED, Edelman GM, Tononi G (1997) Neural dynamics in a model of the thalamocortical system. I. Layers, loops and the emergence of fast synchronous rhythms. Cereb Cortex 7:207–227CrossRefPubMedGoogle Scholar
  47. McIntosh AR (2000) Towards a network theory of cognition. Neural Netw 13:861–870CrossRefPubMedGoogle Scholar
  48. Niebur E, Hsiao SS, Johnson KO (2002) Synchrony: a neuronal mechanism for attentional selection? Curr Opin Neurobiol 12:190–194CrossRefPubMedGoogle Scholar
  49. Palva S, Palva JM (2007) New vistas for alpha-frequency band oscillations. Trends Neurosci 30:150–158CrossRefPubMedGoogle Scholar
  50. Pessoa L (2014) Understanding brain networks and brain organization. Phys Life Rev 11:400–435CrossRefPubMedPubMedCentralGoogle Scholar
  51. Popescu AT, Popa D, Paré D (2009) Coherent gamma oscillations couple the amygdala and striatum during learning. Nat Neurosci 12:801–807CrossRefPubMedPubMedCentralGoogle Scholar
  52. Rolls ET, Treves A (2011) The neuronal encoding of information in the brain. Prog Neurobiol 95:448–490CrossRefPubMedGoogle Scholar
  53. Salinas E, Sejnowski TJ (2001) Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci 2:539–550CrossRefPubMedPubMedCentralGoogle Scholar
  54. Scherg M, Ille N, Bornfleth H, Berg P (2002) Advanced tools for digital EEG review: virtual source montages, whole-head mapping, correlation, and phase analysis. J Clin Neurophysiol 19:91–112CrossRefPubMedGoogle Scholar
  55. Simons DJ, Rensink RA (2005) Change blindness: past present and future. Trends Cogn Sci 9:16–20CrossRefPubMedGoogle Scholar
  56. Somers D, Kopell N (1993) Rapid synchrony through fast threshold modulation. Biol Cybern 68:393–407CrossRefPubMedGoogle Scholar
  57. Srinivasan R, Russell DP, Edelman GM, Tononi G (1999) Increased synchronization of neuromagnetic responses during conscious perception. J Neurosci 19:5435–5448PubMedGoogle Scholar
  58. Supp GG, Schlögl A, Trujillo-Barreto N, Müller M, Gruber T (2007) Directed cortical information flow during human object recognition: analyzing induced EEG gamma-band responses in brain’s source space. PLoS One 2(8), e648CrossRefGoogle Scholar
  59. Taylor JG (2007) CODAM model: through attention to consciousness. Scholarpedia 2(11):1598CrossRefGoogle Scholar
  60. Tononi G, Edelman GM (1998) Consciousness and complexity. Science 282:1846–1851CrossRefPubMedGoogle Scholar
  61. Varela F, Lachaux JP, Rodriguez E, Martinerie J (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229–239CrossRefPubMedGoogle Scholar
  62. Volgushev M, Chistiakova M, Singer W (1998) Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience 83:15–25CrossRefPubMedGoogle Scholar
  63. von Stein A, Sarnthein J (2000) Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. Int J Psychophysiol 38:301–313CrossRefGoogle Scholar
  64. Ward LM (2003) Synchronous neural oscillations and cognitive processes. Trends Cogn Sci 17:553–559CrossRefGoogle Scholar
  65. Ward LM (2004) Oscillations and synchrony in cognition. In: Jirsa V, Kelso JAS (eds) Coordination dynamics: issues and trends. Springer, New York, pp 217–242CrossRefGoogle Scholar
  66. Ward LM (2011) The thalamic dynamic core theory of conscious experience. Conscious Cogn 20:464–486CrossRefPubMedGoogle Scholar
  67. Ward LM, Doesburg SM (2009) Synchronization analysis in EEG and MEG. In: Handy TC (ed) Brain signal analysis: advances in neuroelectric and neuromagnetic methods. MIT Press, Cambridge, MA, pp 171–204CrossRefGoogle Scholar
  68. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12:1–24CrossRefPubMedPubMedCentralGoogle Scholar
  69. Worden MS, Foxe JJ, Wang N, Simpson GV (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific α-band electroencephalography increases over occipital cortex. J Neurosci 20(63):1–6Google Scholar
  70. Wright RD, Ward LM (2008) Orienting of attention. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Psychology and The Brain Research CentreThe University of British ColumbiaVancouverCanada

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