Skip to main content
NCBI home page
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):1729–1737. doi: 10.1098/rstb.2002.1157

Spike timing and visual processing in the retinogeniculocortical pathway.

W Martin Usrey 1
PMCID: PMC1693071  PMID: 12626007

Abstract

Although the visual response properties of neurons along the retinogeniculocortical pathway have been studied for decades, relatively few studies have examined how individual neurons along the pathway communicate with each other. Recent studies in the cat (Felis domestica) now show that the strength of these connections is very dynamic and spike timing plays an important part in determining whether action potentials will be transferred from pre- to postsynaptic cells. This review explores recent progress in our understanding of what role spike timing has in establishing different patterns of geniculate activity and how these patterns ultimately drive the cortex.

Full Text

The Full Text of this article is available as a PDF (660.8 KB).

Selected References

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

  1. Alonso J. M., Usrey W. M., Reid R. C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature. 1996 Oct 31;383(6603):815–819. doi: 10.1038/383815a0. [DOI] [PubMed] [Google Scholar]
  2. Alonso J. M., Usrey W. M., Reid R. C. Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J Neurosci. 2001 Jun 1;21(11):4002–4015. doi: 10.1523/JNEUROSCI.21-11-04002.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Azouz R., Gray C. M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8110–8115. doi: 10.1073/pnas.130200797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brody C. D. Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. J Neurophysiol. 1998 Dec;80(6):3345–3351. doi: 10.1152/jn.1998.80.6.3345. [DOI] [PubMed] [Google Scholar]
  5. Chen Chinfei, Blitz Dawn M., Regehr Wade G. Contributions of receptor desensitization and saturation to plasticity at the retinogeniculate synapse. Neuron. 2002 Feb 28;33(5):779–788. doi: 10.1016/s0896-6273(02)00611-6. [DOI] [PubMed] [Google Scholar]
  6. Chung Sooyoung, Li Xiangrui, Nelson Sacha B. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron. 2002 Apr 25;34(3):437–446. doi: 10.1016/s0896-6273(02)00659-1. [DOI] [PubMed] [Google Scholar]
  7. Crunelli V., Haby M., Jassik-Gerschenfeld D., Leresche N., Pirchio M. Cl- - and K+-dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. J Physiol. 1988 May;399:153–176. doi: 10.1113/jphysiol.1988.sp017073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dan Y., Alonso J. M., Usrey W. M., Reid R. C. Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat Neurosci. 1998 Oct;1(6):501–507. doi: 10.1038/2217. [DOI] [PubMed] [Google Scholar]
  9. Dobrunz L. E., Stevens C. F. Response of hippocampal synapses to natural stimulation patterns. Neuron. 1999 Jan;22(1):157–166. doi: 10.1016/s0896-6273(00)80687-x. [DOI] [PubMed] [Google Scholar]
  10. Erişir A., Van Horn S. C., Bickford M. E., Sherman S. M. Immunocytochemistry and distribution of parabrachial terminals in the lateral geniculate nucleus of the cat: a comparison with corticogeniculate terminals. J Comp Neurol. 1997 Jan 27;377(4):535–549. [PubMed] [Google Scholar]
  11. Erişir A., Van Horn S. C., Sherman S. M. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1517–1520. doi: 10.1073/pnas.94.4.1517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ferster D., Chung S., Wheat H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature. 1996 Mar 21;380(6571):249–252. doi: 10.1038/380249a0. [DOI] [PubMed] [Google Scholar]
  13. Fitzpatrick D., Usrey W. M., Schofield B. R., Einstein G. The sublaminar organization of corticogeniculate neurons in layer 6 of macaque striate cortex. Vis Neurosci. 1994 Mar-Apr;11(2):307–315. doi: 10.1017/s0952523800001656. [DOI] [PubMed] [Google Scholar]
  14. Funke K., Nelle E., Li B., Wörgötter F. Corticofugal feedback improves the timing of retino-geniculate signal transmission. Neuroreport. 1996 Sep 2;7(13):2130–2134. doi: 10.1097/00001756-199609020-00013. [DOI] [PubMed] [Google Scholar]
  15. Gil Z., Connors B. W., Amitai Y. Efficacy of thalamocortical and intracortical synaptic connections: quanta, innervation, and reliability. Neuron. 1999 Jun;23(2):385–397. doi: 10.1016/s0896-6273(00)80788-6. [DOI] [PubMed] [Google Scholar]
  16. Gilbert C. D., Kelly J. P. The projections of cells in different layers of the cat's visual cortex. J Comp Neurol. 1975 Sep;163(1):81–105. doi: 10.1002/cne.901630106. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Guido W., Weyand T. Burst responses in thalamic relay cells of the awake behaving cat. J Neurophysiol. 1995 Oct;74(4):1782–1786. doi: 10.1152/jn.1995.74.4.1782. [DOI] [PubMed] [Google Scholar]
  19. Gulyás B., Lagae L., Eysel U., Orban G. A. Corticofugal feedback influences the responses of geniculate neurons to moving stimuli. Exp Brain Res. 1990;79(2):441–446. doi: 10.1007/BF00608257. [DOI] [PubMed] [Google Scholar]
  20. HUBEL D. H., WIESEL T. N. Integrative action in the cat's lateral geniculate body. J Physiol. 1961 Feb;155:385–398. doi: 10.1113/jphysiol.1961.sp006635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Hendrickson A. E., Wilson J. R., Ogren M. P. The neuroanatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. J Comp Neurol. 1978 Nov 1;182(1):123–136. doi: 10.1002/cne.901820108. [DOI] [PubMed] [Google Scholar]
  23. Hirsch J. A., Alonso J. M., Reid R. C. Visually evoked calcium action potentials in cat striate cortex. Nature. 1995 Dec 7;378(6557):612–616. doi: 10.1038/378612a0. [DOI] [PubMed] [Google Scholar]
  24. Huguenard J. R., McCormick D. A. Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol. 1992 Oct;68(4):1373–1383. doi: 10.1152/jn.1992.68.4.1373. [DOI] [PubMed] [Google Scholar]
  25. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jahnsen H., Llinás R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol. 1984 Apr;349:227–247. doi: 10.1113/jphysiol.1984.sp015154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jones E. G. The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 2001 Oct;24(10):595–601. doi: 10.1016/s0166-2236(00)01922-6. [DOI] [PubMed] [Google Scholar]
  28. Kaplan E., Purpura K., Shapley R. M. Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. J Physiol. 1987 Oct;391:267–288. doi: 10.1113/jphysiol.1987.sp016737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kara P., Reinagel P., Reid R. C. Low response variability in simultaneously recorded retinal, thalamic, and cortical neurons. Neuron. 2000 Sep;27(3):635–646. doi: 10.1016/s0896-6273(00)00072-6. [DOI] [PubMed] [Google Scholar]
  30. Katz L. C. Local circuitry of identified projection neurons in cat visual cortex brain slices. J Neurosci. 1987 Apr;7(4):1223–1249. doi: 10.1523/JNEUROSCI.07-04-01223.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kralik J. D., Dimitrov D. F., Krupa D. J., Katz D. B., Cohen D., Nicolelis M. A. Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods. 2001 Oct;25(2):121–150. doi: 10.1006/meth.2001.1231. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]
  34. Levine M. W., Cleland B. G. An analysis of the effect of retinal ganglion cell impulses upon the firing probability of neurons in the dorsal lateral geniculate nucleus of the cat. Brain Res. 2001 Jun 1;902(2):244–254. doi: 10.1016/s0006-8993(01)02411-8. [DOI] [PubMed] [Google Scholar]
  35. Lo F. S., Lu S. M., Sherman S. M. Intracellular and extracellular in vivo recording of different response modes for relay cells of the cat's lateral geniculate nucleus. Exp Brain Res. 1991;83(2):317–328. doi: 10.1007/BF00231155. [DOI] [PubMed] [Google Scholar]
  36. Lo Fu-Sun, Ziburkus Jokubas, Guido William. Synaptic mechanisms regulating the activation of a Ca(2+)-mediated plateau potential in developing relay cells of the LGN. J Neurophysiol. 2002 Mar;87(3):1175–1185. doi: 10.1152/jn.00715.1999. [DOI] [PubMed] [Google Scholar]
  37. Lund J. S., Lund R. D., Hendrickson A. E., Bunt A. H., Fuchs A. F. The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J Comp Neurol. 1975 Dec 1;164(3):287–303. doi: 10.1002/cne.901640303. [DOI] [PubMed] [Google Scholar]
  38. Mastronarde D. N. Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J Neurophysiol. 1987 Feb;57(2):381–413. doi: 10.1152/jn.1987.57.2.381. [DOI] [PubMed] [Google Scholar]
  39. McCormick D. A., Huguenard J. R. A model of the electrophysiological properties of thalamocortical relay neurons. J Neurophysiol. 1992 Oct;68(4):1384–1400. doi: 10.1152/jn.1992.68.4.1384. [DOI] [PubMed] [Google Scholar]
  40. Miller L. M., Escabí M. A., Read H. L., Schreiner C. E. Functional convergence of response properties in the auditory thalamocortical system. Neuron. 2001 Oct 11;32(1):151–160. doi: 10.1016/s0896-6273(01)00445-7. [DOI] [PubMed] [Google Scholar]
  41. Miller L. M., Escabí M. A., Schreiner C. E. Feature selectivity and interneuronal cooperation in the thalamocortical system. J Neurosci. 2001 Oct 15;21(20):8136–8144. doi: 10.1523/JNEUROSCI.21-20-08136.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Molotchnikoff S., Tremblay F., Lepore F. The role of the visual cortex in response properties of lateral geniculate cells in rats. Exp Brain Res. 1984;53(2):223–232. doi: 10.1007/BF00238152. [DOI] [PubMed] [Google Scholar]
  43. Murphy P. C., Sillito A. M. Functional morphology of the feedback pathway from area 17 of the cat visual cortex to the lateral geniculate nucleus. J Neurosci. 1996 Feb 1;16(3):1180–1192. doi: 10.1523/JNEUROSCI.16-03-01180.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Peters A., Payne B. R. Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex. 1993 Jan-Feb;3(1):69–78. doi: 10.1093/cercor/3.1.69. [DOI] [PubMed] [Google Scholar]
  45. Przybyszewski A. W., Gaska J. P., Foote W., Pollen D. A. Striate cortex increases contrast gain of macaque LGN neurons. Vis Neurosci. 2000 Jul-Aug;17(4):485–494. doi: 10.1017/s0952523800174012. [DOI] [PubMed] [Google Scholar]
  46. Ramcharan E. J., Gnadt J. W., Sherman S. M. Burst and tonic firing in thalamic cells of unanesthetized, behaving monkeys. Vis Neurosci. 2000 Jan-Feb;17(1):55–62. doi: 10.1017/s0952523800171056. [DOI] [PubMed] [Google Scholar]
  47. Rao R. P., Ballard D. H. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci. 1999 Jan;2(1):79–87. doi: 10.1038/4580. [DOI] [PubMed] [Google Scholar]
  48. Reid R. C., Alonso J. M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature. 1995 Nov 16;378(6554):281–284. doi: 10.1038/378281a0. [DOI] [PubMed] [Google Scholar]
  49. Reid R. C., Victor J. D., Shapley R. M. The use of m-sequences in the analysis of visual neurons: linear receptive field properties. Vis Neurosci. 1997 Nov-Dec;14(6):1015–1027. doi: 10.1017/s0952523800011743. [DOI] [PubMed] [Google Scholar]
  50. Reinagel P., Godwin D., Sherman S. M., Koch C. Encoding of visual information by LGN bursts. J Neurophysiol. 1999 May;81(5):2558–2569. doi: 10.1152/jn.1999.81.5.2558. [DOI] [PubMed] [Google Scholar]
  51. Rowe M. H., Fischer Q. Dynamic properties of retino-geniculate synapses in the cat. Vis Neurosci. 2001 Mar-Apr;18(2):219–231. doi: 10.1017/s0952523801182076. [DOI] [PubMed] [Google Scholar]
  52. Roy S. A., Alloway K. D. Coincidence detection or temporal integration? What the neurons in somatosensory cortex are doing. J Neurosci. 2001 Apr 1;21(7):2462–2473. doi: 10.1523/JNEUROSCI.21-07-02462.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Salinas E., Sejnowski T. J. Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci. 2001 Aug;2(8):539–550. doi: 10.1038/35086012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schmielau F., Singer W. The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res. 1977 Jan 21;120(2):354–361. doi: 10.1016/0006-8993(77)90914-3. [DOI] [PubMed] [Google Scholar]
  55. 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]
  56. 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]
  57. Shadlen M. N., Newsome W. T. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J Neurosci. 1998 May 15;18(10):3870–3896. doi: 10.1523/JNEUROSCI.18-10-03870.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sherman S. M. Dual response modes in lateral geniculate neurons: mechanisms and functions. Vis Neurosci. 1996 Mar-Apr;13(2):205–213. doi: 10.1017/s0952523800007446. [DOI] [PubMed] [Google Scholar]
  59. Sherman S. M. Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci. 2001 Feb;24(2):122–126. doi: 10.1016/s0166-2236(00)01714-8. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Softky W. R., Koch C. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci. 1993 Jan;13(1):334–350. doi: 10.1523/JNEUROSCI.13-01-00334.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Stevens C. F., Zador A. M. Input synchrony and the irregular firing of cortical neurons. Nat Neurosci. 1998 Jul;1(3):210–217. doi: 10.1038/659. [DOI] [PubMed] [Google Scholar]
  63. Stratford K. J., Tarczy-Hornoch K., Martin K. A., Bannister N. J., Jack J. J. Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature. 1996 Jul 18;382(6588):258–261. doi: 10.1038/382258a0. [DOI] [PubMed] [Google Scholar]
  64. Swadlow H. A., Gusev A. G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat Neurosci. 2001 Apr;4(4):402–408. doi: 10.1038/86054. [DOI] [PubMed] [Google Scholar]
  65. Tanaka K. Organization of geniculate inputs to visual cortical cells in the cat. Vision Res. 1985;25(3):357–364. doi: 10.1016/0042-6989(85)90060-4. [DOI] [PubMed] [Google Scholar]
  66. Tsumoto T., Creutzfeldt O. D., Legéndy C. R. Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat (with an appendix on geniculo-cortical mono-synaptic connections). Exp Brain Res. 1978 Jul 14;32(3):345–364. doi: 10.1007/BF00238707. [DOI] [PubMed] [Google Scholar]
  67. Usrey W. M., Alonso J. M., Reid R. C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex. J Neurosci. 2000 Jul 15;20(14):5461–5467. doi: 10.1523/JNEUROSCI.20-14-05461.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Usrey W. M., Fitzpatrick D. Specificity in the axonal connections of layer VI neurons in tree shrew striate cortex: evidence for distinct granular and supragranular systems. J Neurosci. 1996 Feb 1;16(3):1203–1218. doi: 10.1523/JNEUROSCI.16-03-01203.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. 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]
  70. Usrey W. M., Reppas J. B., Reid R. C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature. 1998 Sep 24;395(6700):384–387. doi: 10.1038/26487. [DOI] [PubMed] [Google Scholar]
  71. Usrey W. M., Reppas J. B., Reid R. C. Specificity and strength of retinogeniculate connections. J Neurophysiol. 1999 Dec;82(6):3527–3540. doi: 10.1152/jn.1999.82.6.3527. [DOI] [PubMed] [Google Scholar]
  72. Weliky M. Recording and manipulating the in vivo correlational structure of neuronal activity during visual cortical development. J Neurobiol. 1999 Oct;41(1):25–32. doi: 10.1002/(sici)1097-4695(199910)41:1<25::aid-neu5>3.0.co;2-#. [DOI] [PubMed] [Google Scholar]
  73. Weyand T. G., Boudreaux M., Guido W. Burst and tonic response modes in thalamic neurons during sleep and wakefulness. J Neurophysiol. 2001 Mar;85(3):1107–1118. doi: 10.1152/jn.2001.85.3.1107. [DOI] [PubMed] [Google Scholar]

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

RESOURCES