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
. 2002 Dec 29;357(1428):1823–1834. doi: 10.1098/rstb.2002.1159

The influence of the corticothalamic projection on responses in thalamus and cortex.

Florentin Wörgötter 1, Dirk Eyding 1, Jeffrey D Macklis 1, Klaus Funke 1
PMCID: PMC1693092  PMID: 12626015

Abstract

We review results on the in vivo properties of neurons in the dorsal lateral geniculate nucleus (dLGN) that receives its afferent input from the retina and projects to the visual cortex. In addition, the dLGN receives input from the brain stem and from a rather strong corticothalamic back-projection, which originates in layer 6 of the visual cortex. We compare the behaviour of dLGN cells during spontaneous changes of the frequency contents of the electroencephalograph (EEG) (which are mainly related to a changing brain stem influence), with those that are obtained when experimentally silencing the corticothalamic feedback. The spatial and temporal response properties of dLGN cells are compared during these two conditions, and we report that the neurons behave similarly during a synchronized EEG state and during inactive corticothalamic feedback. In both situations, dLGN cells are rather phasic and their remaining tonic activity is temporally dispersed, indicating a hyperpolarizing effect. By means of a novel method, we were able to chronically eliminate a large proportion of the corticothalamic projection neurons from the otherwise intact cortex. In this condition, we found that cortical cells also lose their EEG specific response differences but, in this instance, probably due to a facilitatory (depolarizing) plasticity reaction of the remaining network.

Full Text

The Full Text of this article is available as a PDF (687.8 KB).

Selected References

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

  1. Allison J. D., Casagrande V. A., Bonds A. B. The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate. Vis Neurosci. 1995 Mar-Apr;12(2):309–320. doi: 10.1017/s0952523800007999. [DOI] [PubMed] [Google Scholar]
  2. Baker F. H., Malpeli J. G. Effects of cryogenic blockade of visual cortex on the responses of lateral geniculate neurons in the monkey. Exp Brain Res. 1977 Sep 28;29(3-4):433–444. doi: 10.1007/BF00236182. [DOI] [PubMed] [Google Scholar]
  3. Balz G. W., Hock H. S. The effect of attentional spread on spatial resolution. Vision Res. 1997 Jun;37(11):1499–1510. doi: 10.1016/s0042-6989(96)00296-9. [DOI] [PubMed] [Google Scholar]
  4. Bender D. B., Youakim M. Effect of attentive fixation in macaque thalamus and cortex. J Neurophysiol. 2001 Jan;85(1):219–234. doi: 10.1152/jn.2001.85.1.219. [DOI] [PubMed] [Google Scholar]
  5. Bolz J., Gilbert C. D. Generation of end-inhibition in the visual cortex via interlaminar connections. 1986 Mar 27-Apr 2Nature. 320(6060):362–365. doi: 10.1038/320362a0. [DOI] [PubMed] [Google Scholar]
  6. Brefczynski J. A., DeYoe E. A. A physiological correlate of the 'spotlight' of visual attention. Nat Neurosci. 1999 Apr;2(4):370–374. doi: 10.1038/7280. [DOI] [PubMed] [Google Scholar]
  7. Contreras D., Destexhe A., Sejnowski T. J., Steriade M. Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci. 1997 Feb 1;17(3):1179–1196. doi: 10.1523/JNEUROSCI.17-03-01179.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Contreras D., Steriade M. Spindle oscillation in cats: the role of corticothalamic feedback in a thalamically generated rhythm. J Physiol. 1996 Jan 1;490(Pt 1):159–179. doi: 10.1113/jphysiol.1996.sp021133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Crick F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4586–4590. doi: 10.1073/pnas.81.14.4586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cudeiro J., Rivadulla C., Grieve K. L. Visual response augmentation in cat (and macaque) LGN: potentiation by corticofugally mediated gain control in the temporal domain. Eur J Neurosci. 2000 Apr;12(4):1135–1144. doi: 10.1046/j.1460-9568.2000.00000.x. [DOI] [PubMed] [Google Scholar]
  11. Cudeiro J., Sillito A. M. Spatial frequency tuning of orientation-discontinuity-sensitive corticofugal feedback to the cat lateral geniculate nucleus. J Physiol. 1996 Jan 15;490(Pt 2):481–492. doi: 10.1113/jphysiol.1996.sp021159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deco G., Zihl J. A neurodynamical model of visual attention: feedback enhancement of spatial resolution in a hierarchical system. J Comput Neurosci. 2001 May-Jun;10(3):231–253. doi: 10.1023/a:1011233530729. [DOI] [PubMed] [Google Scholar]
  13. Desimone R., Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci. 1995;18:193–222. doi: 10.1146/annurev.ne.18.030195.001205. [DOI] [PubMed] [Google Scholar]
  14. Dossi R. C., Nuñez A., Steriade M. Electrophysiology of a slow (0.5-4 Hz) intrinsic oscillation of cat thalamocortical neurones in vivo. J Physiol. 1992 Feb;447:215–234. doi: 10.1113/jphysiol.1992.sp018999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Einevoll G. T., Heggelund P. Mathematical models for the spatial receptive-field organization of nonlagged X-cells in dorsal lateral geniculate nucleus of cat. Vis Neurosci. 2000 Nov-Dec;17(6):871–885. doi: 10.1017/s0952523800176060. [DOI] [PubMed] [Google Scholar]
  16. Eysel U. T. Maintained activity, excitation and inhibition of lateral geniculate neurons after monocular deafferentation in the adult cat. Brain Res. 1979 Apr 27;166(2):259–271. doi: 10.1016/0006-8993(79)90212-9. [DOI] [PubMed] [Google Scholar]
  17. Funke K., Eysel U. T. EEG-dependent modulation of response dynamics of cat dLGN relay cells and the contribution of corticogeniculate feedback. Brain Res. 1992 Feb 28;573(2):217–227. doi: 10.1016/0006-8993(92)90766-3. [DOI] [PubMed] [Google Scholar]
  18. Funke K., Kerscher N. High-frequency (300-800 Hz) components in cat geniculate (dLGN) early visual responses. J Physiol Paris. 2000 Sep-Dec;94(5-6):411–425. doi: 10.1016/s0928-4257(00)01099-8. [DOI] [PubMed] [Google Scholar]
  19. Funke K., Wörgötter F. On the significance of temporally structured activity in the dorsal lateral geniculate nucleus (LGN). Prog Neurobiol. 1997 Sep;53(1):67–119. doi: 10.1016/s0301-0082(97)00032-4. [DOI] [PubMed] [Google Scholar]
  20. Funke K., Wörgötter F. Temporal structure in the light response of relay cells in the dorsal lateral geniculate nucleus of the cat. J Physiol. 1995 Jun 15;485(Pt 3):715–737. doi: 10.1113/jphysiol.1995.sp020764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Guillery R. W., Herrup K. Quantification without pontification: choosing a method for counting objects in sectioned tissues. J Comp Neurol. 1997 Sep 15;386(1):2–7. doi: 10.1002/(sici)1096-9861(19970915)386:1<2::aid-cne2>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
  22. Hennig Matthias H., Funke Klaus, Wörgötter Florentin. The influence of different retinal subcircuits on the nonlinearity of ganglion cell behavior. J Neurosci. 2002 Oct 1;22(19):8726–8738. doi: 10.1523/JNEUROSCI.22-19-08726.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hillenbrand U., van Hemmen J. L. Spatiotemporal adaptation through corticothalamic loops: a hypothesis. Vis Neurosci. 2000 Jan-Feb;17(1):107–118. doi: 10.1017/s0952523800171111. [DOI] [PubMed] [Google Scholar]
  24. Hock H. S., Balz G. W., Smollon W. Attentional control of spatial scale: effects on self-organized motion patterns. Vision Res. 1998 Dec;38(23):3743–3758. doi: 10.1016/s0042-6989(98)00023-6. [DOI] [PubMed] [Google Scholar]
  25. Ikeda H., Wright M. J. Sensitivity of neurones in visual cortex (area 17) under different levels of anaesthesia. Exp Brain Res. 1974;20(5):471–484. doi: 10.1007/BF00238014. [DOI] [PubMed] [Google Scholar]
  26. Kalil R. E., Chase R. Corticofugal influence on activity of lateral geniculate neurons in the cat. J Neurophysiol. 1970 May;33(3):459–474. doi: 10.1152/jn.1970.33.3.459. [DOI] [PubMed] [Google Scholar]
  27. Kirkland K. L., Sillito A. M., Jones H. E., West D. C., Gerstein G. L. Oscillations and long-lasting correlations in a model of the lateral geniculate nucleus and visual cortex. J Neurophysiol. 2000 Oct;84(4):1863–1868. doi: 10.1152/jn.2000.84.4.1863. [DOI] [PubMed] [Google Scholar]
  28. Li B., Funke K., Wörgötter F., Eysel U. T. Correlated variations in EEG pattern and visual responsiveness of cat lateral geniculate relay cells. J Physiol. 1999 Feb 1;514(Pt 3):857–874. doi: 10.1111/j.1469-7793.1999.857ad.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Livingstone M. S., Hubel D. H. Effects of sleep and arousal on the processing of visual information in the cat. Nature. 1981 Jun 18;291(5816):554–561. doi: 10.1038/291554a0. [DOI] [PubMed] [Google Scholar]
  30. Llinás R., Jahnsen H. Electrophysiology of mammalian thalamic neurones in vitro. Nature. 1982 Jun 3;297(5865):406–408. doi: 10.1038/297406a0. [DOI] [PubMed] [Google Scholar]
  31. Macklis J. D. Transplanted neocortical neurons migrate selectively into regions of neuronal degeneration produced by chromophore-targeted laser photolysis. J Neurosci. 1993 Sep;13(9):3848–3863. doi: 10.1523/JNEUROSCI.13-09-03848.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Magavi S. S., Leavitt B. R., Macklis J. D. Induction of neurogenesis in the neocortex of adult mice. Nature. 2000 Jun 22;405(6789):951–955. doi: 10.1038/35016083. [DOI] [PubMed] [Google Scholar]
  33. Marrocco R. T., McClurkin J. W., Alkire M. T. The influence of the visual cortex on the spatiotemporal response properties of lateral geniculate nucleus cells. Brain Res. 1996 Oct 21;737(1-2):110–118. doi: 10.1016/0006-8993(96)00660-9. [DOI] [PubMed] [Google Scholar]
  34. McClurkin J. W., Marrocco R. T. Visual cortical input alters spatial tuning in monkey lateral geniculate nucleus cells. J Physiol. 1984 Mar;348:135–152. doi: 10.1113/jphysiol.1984.sp015103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McClurkin J. W., Optican L. M., Richmond B. J. Cortical feedback increases visual information transmitted by monkey parvocellular lateral geniculate nucleus neurons. Vis Neurosci. 1994 May-Jun;11(3):601–617. doi: 10.1017/s0952523800002492. [DOI] [PubMed] [Google Scholar]
  36. McCormick D. A., von Krosigk M. Corticothalamic activation modulates thalamic firing through glutamate "metabotropic" receptors. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2774–2778. doi: 10.1073/pnas.89.7.2774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Murphy P. C., Duckett S. G., Sillito A. M. Comparison of the laminar distribution of input from areas 17 and 18 of the visual cortex to the lateral geniculate nucleus of the cat. J Neurosci. 2000 Jan 15;20(2):845–853. doi: 10.1523/JNEUROSCI.20-02-00845.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Murphy P. C., Sillito A. M. Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature. 1987 Oct 22;329(6141):727–729. doi: 10.1038/329727a0. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Posner M. I., Gilbert C. D. Attention and primary visual cortex. Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2585–2587. doi: 10.1073/pnas.96.6.2585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Rivadulla Casto, Martínez Luis M., Varela Carmen, Cudeiro Javier. Completing the corticofugal loop: a visual role for the corticogeniculate type 1 metabotropic glutamate receptor. J Neurosci. 2002 Apr 1;22(7):2956–2962. doi: 10.1523/JNEUROSCI.22-07-02956.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ruksenas O., Fjeld I. T., Heggelund P. Spatial summation and center-surround antagonism in the receptive field of single units in the dorsal lateral geniculate nucleus of cat: comparison with retinal input. Vis Neurosci. 2000 Nov-Dec;17(6):855–870. doi: 10.1017/s0952523800176059. [DOI] [PubMed] [Google Scholar]
  44. Sawai H., Morigiwa K., Fukuda Y. Effects of EEG synchronization on visual responses of the cat's geniculate relay cells: a comparison among Y, X and W cells. Brain Res. 1988 Jul 12;455(2):394–400. doi: 10.1016/0006-8993(88)90102-3. [DOI] [PubMed] [Google Scholar]
  45. Scharff C., Kirn J. R., Grossman M., Macklis J. D., Nottebohm F. Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron. 2000 Feb;25(2):481–492. doi: 10.1016/s0896-6273(00)80910-1. [DOI] [PubMed] [Google Scholar]
  46. Scharfman H. E., Lu S. M., Guido W., Adams P. R., Sherman S. M. N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4548–4552. doi: 10.1073/pnas.87.12.4548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sheen V. L., Macklis J. D. Targeted neocortical cell death in adult mice guides migration and differentiation of transplanted embryonic neurons. J Neurosci. 1995 Dec;15(12):8378–8392. doi: 10.1523/JNEUROSCI.15-12-08378.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sherman S. M., Koch C. The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res. 1986;63(1):1–20. doi: 10.1007/BF00235642. [DOI] [PubMed] [Google Scholar]
  49. Shin J. J., Fricker-Gates R. A., Perez F. A., Leavitt B. R., Zurakowski D., Macklis J. D. Transplanted neuroblasts differentiate appropriately into projection neurons with correct neurotransmitter and receptor phenotype in neocortex undergoing targeted projection neuron degeneration. J Neurosci. 2000 Oct 1;20(19):7404–7416. doi: 10.1523/JNEUROSCI.20-19-07404.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sillito A. M., Cudeiro J., Murphy P. C. Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus. Exp Brain Res. 1993;93(1):6–16. doi: 10.1007/BF00227775. [DOI] [PubMed] [Google Scholar]
  51. Sillito A. M., Grieve K. L., Jones H. E., Cudeiro J., Davis J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature. 1995 Nov 30;378(6556):492–496. doi: 10.1038/378492a0. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Singer W. Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiol Rev. 1977 Jul;57(3):386–420. doi: 10.1152/physrev.1977.57.3.386. [DOI] [PubMed] [Google Scholar]
  54. Singer W., Tretter F., Cynader M. The effect of reticular stimulation on spontaneous and evoked activity in the cat visual cortex. Brain Res. 1976 Jan 30;102(1):71–90. doi: 10.1016/0006-8993(76)90576-x. [DOI] [PubMed] [Google Scholar]
  55. Somers D. C., Dale A. M., Seiffert A. E., Tootell R. B. Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1663–1668. doi: 10.1073/pnas.96.4.1663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Steriade M. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb Cortex. 1997 Sep;7(6):583–604. doi: 10.1093/cercor/7.6.583. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. Suder K., Wörgötter F. The control of low-level information flow in the visual system. Rev Neurosci. 2000;11(2-3):127–146. doi: 10.1515/revneuro.2000.11.2-3.127. [DOI] [PubMed] [Google Scholar]
  59. Tsal Y., Shalev L. Inattention magnifies perceived length: the attentional receptive field hypothesis. J Exp Psychol Hum Percept Perform. 1996 Feb;22(1):233–243. doi: 10.1037//0096-1523.22.1.233. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Vidyasagar T. R., Urbas J. V. Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Exp Brain Res. 1982;46(2):157–169. doi: 10.1007/BF00237172. [DOI] [PubMed] [Google Scholar]
  62. Weber A. J., Kalil R. E., Behan M. Synaptic connections between corticogeniculate axons and interneurons in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol. 1989 Nov 1;289(1):156–164. doi: 10.1002/cne.902890113. [DOI] [PubMed] [Google Scholar]
  63. 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]
  64. Wörgötter F., Nelle E., Li B., Funke K. The influence of corticofugal feedback on the temporal structure of visual responses of cat thalamic relay cells. J Physiol. 1998 Jun 15;509(Pt 3):797–815. doi: 10.1111/j.1469-7793.1998.797bm.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Wörgötter F., Suder K., Funke K. The dynamic spatio-temporal behavior of visual responses in thalamus and cortex. Restor Neurol Neurosci. 1999;15(2-3):137–152. [PubMed] [Google Scholar]
  66. Wörgötter F., Suder K., Zhao Y., Kerscher N., Eysel U. T., Funke K. State-dependent receptive-field restructuring in the visual cortex. Nature. 1998 Nov 12;396(6707):165–168. doi: 10.1038/24157. [DOI] [PubMed] [Google Scholar]
  67. Yeshurun Y., Carrasco M. Attention improves or impairs visual performance by enhancing spatial resolution. Nature. 1998 Nov 5;396(6706):72–75. doi: 10.1038/23936. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES