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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2002 Dec 29;357(1428):1869–1876. doi: 10.1098/rstb.2002.1172

Feed-forward synchronization: propagation of temporal patterns along the retinothalamocortical pathway.

Sergio Neuenschwander 1, Miguel Castelo-Branco 1, Jerome Baron 1, Wolf Singer 1
PMCID: PMC1693079  PMID: 12626020

Abstract

Visual responses in the cortex and lateral geniculate nucleus (LGN) are often associated with synchronous oscillatory patterning. In this short review, we examine the possible relationships between subcortical and cortical synchronization mechanisms. Our results obtained from simultaneous multi-unit recordings show strong synchronization of oscillatory responses between retina, LGN and cortex, indicating that cortical neurons can be synchronized by oscillatory activity relayed through the LGN. This feed-forward synchronization mechanism operating in the 60 to 120 Hz frequency range was observed mostly for static stimuli. In response to moving stimuli, by contrast, cortical synchronization was independent of oscillatory inputs from the LGN, with oscillation frequency in the range of 30 to 60 Hz. The functional implications of synchronization of activity from parallel channels are discussed, in particular its significance for signal transmission and cortical integration processes.

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Selected References

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  1. Adrian E. D., Matthews R. The action of light on the eye: Part III. The interaction of retinal neurones. J Physiol. 1928 Jun 24;65(3):273–298. doi: 10.1113/jphysiol.1928.sp002475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ariel M., Daw N. W., Rader R. K. Rhythmicity in rabbit retinal ganglion cell responses. Vision Res. 1983;23(12):1485–1493. doi: 10.1016/0042-6989(83)90160-8. [DOI] [PubMed] [Google Scholar]
  3. Arnett D. W. Correlation analysis of units recorded in the cat dorsal lateral geniculate nucleus. Exp Brain Res. 1975 Dec 22;24(2):111–130. doi: 10.1007/BF00234058. [DOI] [PubMed] [Google Scholar]
  4. Arnett D. W. Statistical dependence between neighboring retinal ganglion cells in goldfish. Exp Brain Res. 1978 May 12;32(1):49–53. doi: 10.1007/BF00237389. [DOI] [PubMed] [Google Scholar]
  5. Arnett D., Spraker T. E. Cross-correlation analysis of the maintained discharge of rabbit retinal ganglion cells. J Physiol. 1981 Aug;317:29–47. doi: 10.1113/jphysiol.1981.sp013812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. BISHOP P. O., LEVICK W. R., WILLIAMS W. O. STATISTICAL ANALYSIS OF THE DARK DISCHARGE OF LATERAL GENICULATE NEURONES. J Physiol. 1964 Apr;170:598–612. doi: 10.1113/jphysiol.1964.sp007352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brivanlou I. H., Warland D. K., Meister M. Mechanisms of concerted firing among retinal ganglion cells. Neuron. 1998 Mar;20(3):527–539. doi: 10.1016/s0896-6273(00)80992-7. [DOI] [PubMed] [Google Scholar]
  8. Brody CD. Correlations without synchrony. Neural Comput. 1999 Oct 1;11(7):1537–1551. doi: 10.1162/089976699300016133. [DOI] [PubMed] [Google Scholar]
  9. Brody CD. Disambiguating different covariation types. Neural Comput. 1999 Oct 1;11(7):1527–1535. doi: 10.1162/089976699300016124. [DOI] [PubMed] [Google Scholar]
  10. Castelo-Branco M., Neuenschwander S., Singer W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J Neurosci. 1998 Aug 15;18(16):6395–6410. doi: 10.1523/JNEUROSCI.18-16-06395.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DOTY R. W., KIMURA D. S. OSCILLATORY POTENTIALS IN THE VISUAL SYSTEM OF CATS AND MONKEYS. J Physiol. 1963 Aug;168:205–218. doi: 10.1113/jphysiol.1963.sp007187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Diesmann M., Gewaltig M. O., Aertsen A. Stable propagation of synchronous spiking in cortical neural networks. Nature. 1999 Dec 2;402(6761):529–533. doi: 10.1038/990101. [DOI] [PubMed] [Google Scholar]
  13. Engel A. K., Fries P., Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci. 2001 Oct;2(10):704–716. doi: 10.1038/35094565. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Fries P., Reynolds J. H., Rorie A. E., Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science. 2001 Feb 23;291(5508):1560–1563. doi: 10.1126/science.1055465. [DOI] [PubMed] [Google Scholar]
  16. Fries Pascal, Schröder Jan-Hinrich, Roelfsema Pieter R., Singer Wolf, Engel Andreas K. Oscillatory neuronal synchronization in primary visual cortex as a correlate of stimulus selection. J Neurosci. 2002 May 1;22(9):3739–3754. doi: 10.1523/JNEUROSCI.22-09-03739.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ghose G. M., Freeman R. D. Oscillatory discharge in the visual system: does it have a functional role? J Neurophysiol. 1992 Nov;68(5):1558–1574. doi: 10.1152/jn.1992.68.5.1558. [DOI] [PubMed] [Google Scholar]
  18. Granit R. The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. J Physiol. 1933 Feb 8;77(3):207–239. doi: 10.1113/jphysiol.1933.sp002964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Gray C. M. The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron. 1999 Sep;24(1):31-47, 111-25. doi: 10.1016/s0896-6273(00)80820-x. [DOI] [PubMed] [Google Scholar]
  22. Gruber T., Müller M. M., Keil A., Elbert T. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin Neurophysiol. 1999 Dec;110(12):2074–2085. doi: 10.1016/s1388-2457(99)00176-5. [DOI] [PubMed] [Google Scholar]
  23. HUBEL D. H., WIESEL T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962 Jan;160:106–154. doi: 10.1113/jphysiol.1962.sp006837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Herculano-Houzel S., Munk M. H., Neuenschwander S., Singer W. Precisely synchronized oscillatory firing patterns require electroencephalographic activation. J Neurosci. 1999 May 15;19(10):3992–4010. doi: 10.1523/JNEUROSCI.19-10-03992.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kilner J. M., Baker S. N., Salenius S., Hari R., Lemon R. N. Human cortical muscle coherence is directly related to specific motor parameters. J Neurosci. 2000 Dec 1;20(23):8838–8845. doi: 10.1523/JNEUROSCI.20-23-08838.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Laufer M., Verzeano M. Periodic activity in the visual system of the cat. Vision Res. 1967 Mar;7(3):215–229. doi: 10.1016/0042-6989(67)90086-7. [DOI] [PubMed] [Google Scholar]
  28. Levick W. R., Cleland B. G., Dubin M. W. Lateral geniculate neurons of cat: retinal inputs and physiology. Invest Ophthalmol. 1972 May;11(5):302–311. [PubMed] [Google Scholar]
  29. Mastronarde D. N. Correlated firing of retinal ganglion cells. Trends Neurosci. 1989 Feb;12(2):75–80. doi: 10.1016/0166-2236(89)90140-9. [DOI] [PubMed] [Google Scholar]
  30. Maynard E. M., Hatsopoulos N. G., Ojakangas C. L., Acuna B. D., Sanes J. N., Normann R. A., Donoghue J. P. Neuronal interactions improve cortical population coding of movement direction. J Neurosci. 1999 Sep 15;19(18):8083–8093. doi: 10.1523/JNEUROSCI.19-18-08083.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Meister M., Lagnado L., Baylor D. A. Concerted signaling by retinal ganglion cells. Science. 1995 Nov 17;270(5239):1207–1210. doi: 10.1126/science.270.5239.1207. [DOI] [PubMed] [Google Scholar]
  32. Miltner W. H., Braun C., Arnold M., Witte H., Taub E. Coherence of gamma-band EEG activity as a basis for associative learning. Nature. 1999 Feb 4;397(6718):434–436. doi: 10.1038/17126. [DOI] [PubMed] [Google Scholar]
  33. Neuenschwander S., Castelo-Branco M., Singer W. Synchronous oscillations in the cat retina. Vision Res. 1999 Jul;39(15):2485–2497. doi: 10.1016/s0042-6989(99)00042-5. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Przybyszewski A. W., Lankheet M. J., van de Grind W. A. Nonlinearity and oscillations in X-type ganglion cells of the cat retina. Vision Res. 1993 May;33(7):861–875. doi: 10.1016/0042-6989(93)90069-9. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Rodieck R. W. Maintained activity of cat retinal ganglion cells. J Neurophysiol. 1967 Sep;30(5):1043–1071. doi: 10.1152/jn.1967.30.5.1043. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Sakai H. M., Naka K. I. Dissection of the neuron network in the catfish inner retina. V. Interactions between NA and NB amacrine cells. J Neurophysiol. 1990 Jan;63(1):120–130. doi: 10.1152/jn.1990.63.1.120. [DOI] [PubMed] [Google Scholar]
  40. Shadlen M. N., Movshon J. A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron. 1999 Sep;24(1):67-77, 111-25. doi: 10.1016/s0896-6273(00)80822-3. [DOI] [PubMed] [Google Scholar]
  41. Sillito A. M., Jones H. E., Gerstein G. L., West D. C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature. 1994 Jun 9;369(6480):479–482. doi: 10.1038/369479a0. [DOI] [PubMed] [Google Scholar]
  42. Singer W. Neuronal synchrony: a versatile code for the definition of relations? Neuron. 1999 Sep;24(1):49-65, 111-25. doi: 10.1016/s0896-6273(00)80821-1. [DOI] [PubMed] [Google Scholar]
  43. Singer W., Pöppel E., Creutzfeldt O. Inhibitory interaction in the cat's lateral geniculate nucleus. Exp Brain Res. 1972;14(2):210–226. doi: 10.1007/BF00234800. [DOI] [PubMed] [Google Scholar]
  44. Steinmetz P. N., Roy A., Fitzgerald P. J., Hsiao S. S., Johnson K. O., Niebur E. Attention modulates synchronized neuronal firing in primate somatosensory cortex. Nature. 2000 Mar 9;404(6774):187–190. doi: 10.1038/35004588. [DOI] [PubMed] [Google Scholar]
  45. Tallon-Baudry C, Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci. 1999 Apr;3(4):151–162. doi: 10.1016/s1364-6613(99)01299-1. [DOI] [PubMed] [Google Scholar]
  46. Usrey W. M., Reid R. C. Synchronous activity in the visual system. Annu Rev Physiol. 1999;61:435–456. doi: 10.1146/annurev.physiol.61.1.435. [DOI] [PubMed] [Google Scholar]
  47. Usrey W. Martin. Spike timing and visual processing in the retinogeniculocortical pathway. Philos Trans R Soc Lond B Biol Sci. 2002 Dec 29;357(1428):1729–1737. doi: 10.1098/rstb.2002.1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wörgötter F., Funke K. Fine structure analysis of temporal patterns in the light response of cells in the lateral geniculate nucleus of cat. Vis Neurosci. 1995 May-Jun;12(3):469–484. doi: 10.1017/s0952523800008373. [DOI] [PubMed] [Google Scholar]

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