Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Nov 29;353(1377):1829–1840. doi: 10.1098/rstb.1998.0335

Consciousness and the structure of neuronal representations.

W Singer 1
PMCID: PMC1692413  PMID: 9854255

Abstract

The hypothesis is defended that brains expressing phenomenal awareness are capable of generating metarepresentations of their cognitive processes, these metarepresentations resulting from an iteration of self-similar cortical operations. Search for the neuronal substrate of awareness therefore converges with the search for the nature of neuronal representations. It is proposed that evolved brains use two complementary representational strategies. One consists of the generation of neurons responding selectively to a particular constellation of features and is based on selective recombination of inputs in hierarchically structured feedforward architectures. The other relies on the dynamic association of feature-specific cells into functionally coherent cell assemblies that, as a whole, represent the constellation of features defining a particular perceptual object. Arguments are presented that favour the notion that the metarepresentations supporting awareness are established in accordance with the second strategy. Experimental data are reviewed that are compatible with the hypothesis that evolved brains use assembly codes for the representation of contents and that these assemblies become organized through transient synchronization of the discharges of associated neurons. It is argued that central states favouring the formation of assembly-based representations are similar to those favouring awareness.

Full Text

The Full Text of this article is available as a PDF (239.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abeles M. Role of the cortical neuron: integrator or coincidence detector? Isr J Med Sci. 1982 Jan;18(1):83–92. [PubMed] [Google Scholar]
  2. Brecht M., Singer W., Engel A. K. Correlation analysis of corticotectal interactions in the cat visual system. J Neurophysiol. 1998 May;79(5):2394–2407. doi: 10.1152/jn.1998.79.5.2394. [DOI] [PubMed] [Google Scholar]
  3. Buzsáki G., Chrobak J. J. Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol. 1995 Aug;5(4):504–510. doi: 10.1016/0959-4388(95)80012-3. [DOI] [PubMed] [Google Scholar]
  4. Carr C. E. Processing of temporal information in the brain. Annu Rev Neurosci. 1993;16:223–243. doi: 10.1146/annurev.ne.16.030193.001255. [DOI] [PubMed] [Google Scholar]
  5. Eggermont J. J. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation, and age. J Neurophysiol. 1992 Oct;68(4):1216–1228. doi: 10.1152/jn.1992.68.4.1216. [DOI] [PubMed] [Google Scholar]
  6. Engel A. K., Kreiter A. K., König P., Singer W. Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6048–6052. doi: 10.1073/pnas.88.14.6048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Engel A. K., König P., Kreiter A. K., Singer W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science. 1991 May 24;252(5009):1177–1179. doi: 10.1126/science.252.5009.1177. [DOI] [PubMed] [Google Scholar]
  8. Engel A. K., König P., Singer W. Direct physiological evidence for scene segmentation by temporal coding. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9136–9140. doi: 10.1073/pnas.88.20.9136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Freiwald W. A., Kreiter A. K., Singer W. Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. Neuroreport. 1995 Nov 27;6(17):2348–2352. doi: 10.1097/00001756-199511270-00018. [DOI] [PubMed] [Google Scholar]
  10. Fries P., Roelfsema P. R., Engel A. K., König P., Singer W. Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12699–12704. doi: 10.1073/pnas.94.23.12699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gray C. M., König P., Engel A. K., Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature. 1989 Mar 23;338(6213):334–337. doi: 10.1038/338334a0. [DOI] [PubMed] [Google Scholar]
  12. Gray C. M., Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A. 1989 Mar;86(5):1698–1702. doi: 10.1073/pnas.86.5.1698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grillner S., Wallén P., Brodin L., Lansner A. Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. Annu Rev Neurosci. 1991;14:169–199. doi: 10.1146/annurev.ne.14.030191.001125. [DOI] [PubMed] [Google Scholar]
  14. Joliot M., Ribary U., Llinás R. Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11748–11751. doi: 10.1073/pnas.91.24.11748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kiper D. C., Gegenfurtner K. R., Movshon J. A. Cortical oscillatory responses do not affect visual segmentation. Vision Res. 1996 Feb;36(4):539–544. doi: 10.1016/0042-6989(95)00135-2. [DOI] [PubMed] [Google Scholar]
  16. Kreiter A. K., Singer W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J Neurosci. 1996 Apr 1;16(7):2381–2396. doi: 10.1523/JNEUROSCI.16-07-02381.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kristeva-Feige R., Feige B., Makeig S., Ross B., Elbert T. Oscillatory brain activity during a motor task. Neuroreport. 1993 Sep 30;4(12):1291–1294. doi: 10.1097/00001756-199309150-00001. [DOI] [PubMed] [Google Scholar]
  18. König P., Engel A. K., Löwel S., Singer W. Squint affects synchronization of oscillatory responses in cat visual cortex. Eur J Neurosci. 1993 May 1;5(5):501–508. doi: 10.1111/j.1460-9568.1993.tb00516.x. [DOI] [PubMed] [Google Scholar]
  19. König P., Engel A. K., Singer W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 1996 Apr;19(4):130–137. doi: 10.1016/s0166-2236(96)80019-1. [DOI] [PubMed] [Google Scholar]
  20. König P., Engel A. K., Singer W. Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):290–294. doi: 10.1073/pnas.92.1.290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Laurent G. Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci. 1996 Nov;19(11):489–496. doi: 10.1016/S0166-2236(96)10054-0. [DOI] [PubMed] [Google Scholar]
  22. Leonards U., Singer W., Fahle M. The influence of temporal phase differences on texture segmentation. Vision Res. 1996 Sep;36(17):2689–2697. doi: 10.1016/0042-6989(96)86829-5. [DOI] [PubMed] [Google Scholar]
  23. Leonards U., Singer W. Selective temporal interactions between processing streams with differential sensitivity for colour and luminance contrast. Vision Res. 1997 May;37(9):1129–1140. doi: 10.1016/s0042-6989(96)00264-7. [DOI] [PubMed] [Google Scholar]
  24. Leonards U., Singer W. Two segmentation mechanisms with differential sensitivity for colour and luminance contrast. Vision Res. 1998 Jan;38(1):101–109. doi: 10.1016/s0042-6989(97)00148-x. [DOI] [PubMed] [Google Scholar]
  25. Logothetis N. K., Leopold D. A., Sheinberg D. L. What is rivalling during binocular rivalry? Nature. 1996 Apr 18;380(6575):621–624. doi: 10.1038/380621a0. [DOI] [PubMed] [Google Scholar]
  26. Löwel S., Singer W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science. 1992 Jan 10;255(5041):209–212. doi: 10.1126/science.1372754. [DOI] [PubMed] [Google Scholar]
  27. Munk M. H., Roelfsema P. R., König P., Engel A. K., Singer W. Role of reticular activation in the modulation of intracortical synchronization. Science. 1996 Apr 12;272(5259):271–274. doi: 10.1126/science.272.5259.271. [DOI] [PubMed] [Google Scholar]
  28. Murthy V. N., Fetz E. E. Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. J Neurophysiol. 1996 Dec;76(6):3968–3982. doi: 10.1152/jn.1996.76.6.3968. [DOI] [PubMed] [Google Scholar]
  29. Neuenschwander S., Singer W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature. 1996 Feb 22;379(6567):728–732. doi: 10.1038/379728a0. [DOI] [PubMed] [Google Scholar]
  30. Nowak L. G., Munk M. H., Nelson J. I., James A. C., Bullier J. Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. J Neurophysiol. 1995 Dec;74(6):2379–2400. doi: 10.1152/jn.1995.74.6.2379. [DOI] [PubMed] [Google Scholar]
  31. Riehle A., Grün S., Diesmann M., Aertsen A. Spike synchronization and rate modulation differentially involved in motor cortical function. Science. 1997 Dec 12;278(5345):1950–1953. doi: 10.1126/science.278.5345.1950. [DOI] [PubMed] [Google Scholar]
  32. Roelfsema P. R., Engel A. K., König P., Singer W. Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature. 1997 Jan 9;385(6612):157–161. doi: 10.1038/385157a0. [DOI] [PubMed] [Google Scholar]
  33. Roelfsema P. R., König P., Engel A. K., Sireteanu R., Singer W. Reduced synchronization in the visual cortex of cats with strabismic amblyopia. Eur J Neurosci. 1994 Nov 1;6(11):1645–1655. doi: 10.1111/j.1460-9568.1994.tb00556.x. [DOI] [PubMed] [Google Scholar]
  34. Sanes J. N., Donoghue J. P. Oscillations in local field potentials of the primate motor cortex during voluntary movement. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4470–4474. doi: 10.1073/pnas.90.10.4470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schmidt K. E., Goebel R., Löwel S., Singer W. The perceptual grouping criterion of colinearity is reflected by anisotropies of connections in the primary visual cortex. Eur J Neurosci. 1997 May;9(5):1083–1089. doi: 10.1111/j.1460-9568.1997.tb01459.x. [DOI] [PubMed] [Google Scholar]
  36. Shadlen M. N., Newsome W. T. Noise, neural codes and cortical organization. Curr Opin Neurobiol. 1994 Aug;4(4):569–579. doi: 10.1016/0959-4388(94)90059-0. [DOI] [PubMed] [Google Scholar]
  37. Singer W. Development and plasticity of cortical processing architectures. Science. 1995 Nov 3;270(5237):758–764. doi: 10.1126/science.270.5237.758. [DOI] [PubMed] [Google Scholar]
  38. Singer W., Gray C. M. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 1995;18:555–586. doi: 10.1146/annurev.ne.18.030195.003011. [DOI] [PubMed] [Google Scholar]
  39. Softky W. Sub-millisecond coincidence detection in active dendritic trees. Neuroscience. 1994 Jan;58(1):13–41. doi: 10.1016/0306-4522(94)90154-6. [DOI] [PubMed] [Google Scholar]
  40. Steriade M., Amzica F., Contreras D. Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci. 1996 Jan;16(1):392–417. doi: 10.1523/JNEUROSCI.16-01-00392.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Tallon-Baudry C., Bertrand O., Delpuech C., Pernier J. Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human. J Neurosci. 1996 Jul 1;16(13):4240–4249. doi: 10.1523/JNEUROSCI.16-13-04240.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Vaadia E., Haalman I., Abeles M., Bergman H., Prut Y., Slovin H., Aertsen A. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature. 1995 Feb 9;373(6514):515–518. doi: 10.1038/373515a0. [DOI] [PubMed] [Google Scholar]
  43. Volgushev M., Chistiakova M., Singer W. Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential. Neuroscience. 1998 Mar;83(1):15–25. doi: 10.1016/s0306-4522(97)00380-1. [DOI] [PubMed] [Google Scholar]
  44. deCharms R. C., Merzenich M. M. Primary cortical representation of sounds by the coordination of action-potential timing. Nature. 1996 Jun 13;381(6583):610–613. doi: 10.1038/381610a0. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES