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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

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  • 136 Citations

Summary

  1. 1.

    In the cat visual cortex (VC), electrophoretic glutamate application at a depth corresponding to layer VI may have excitatory or inhibitory effects on relay cells of the lateral geniculate nucleus (LGN). Corticofugal excitation was seen, if the receptive field centers (RFCs) of the VC neurons recorded at the application site were within 2.3 ° of the RFCs of the LGN neurons under test. Inhibitory effects were seen if the RFCs of both cells were further apart up to 3.1 °. Glutamate application at more superficial cortical sites had no effect on LGN-neuron activity.

  2. 2.

    Cross-correlation analysis between spontaneous activities of simultaneously recorded VC and LGN neurons revealed excitatory cortico-geniculate connections in 18 pairs with RFCs separated by less than 1.7 °. In 15 pairs the peak latency of the excitation was 2–5 msec (3.4 msec in the average), 3 pairs showed long cortico-geniculate latencies (13–18 msec). The existence of a fast and slow cortico-geniculate system is suggested.

  3. 3.

    Inhibitory cortico-geniculate interaction was demonstrated with cross-correlation analysis in 8 pairs of which 4 had RFCs separated by more than 1.7 °. The onset latency of the inhibition was 2–7 msec except for 2 pairs with about 20 msec latency.

  4. 4.

    Most of the LGN neurons which were affected by cortical glutamate application or which showed an excitatory or inhibitory connection with a VC neuron were sustained cells, while the majority of VC neurons which were recorded in the effective glutamate application sites or which showed a significant interaction with LGN neurons in the cross-correlogram were binocularly driven and complex, with mostly large RFCs (mean diameter 3.5 °). They responded briskly to moving small spots as well as to moving slits.

  5. 5.

    It is concluded that the corticofugal excitatory effect is transmitted through monosynaptic links from VC neurons located in layer VI (complex cell) to LGN relay neurons (mostly sustained-cell) and this system is organized in a precise topographical manner.

  6. 6.

    In an Appendix neuron pairs which showed a positive correlation in the geniculo-cortical direction were described. The findings may support the view that complex as well as simple cells are driven monosynaptically from geniculo-cortical afferents of the sustained or transient type.

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References

  1. Ajmone-Marsan, C., Morillo, A.: Cortical control and callosal mechanisms in the visual system of cat. Electroenceph. clin. Neurophysiol. 13, 553–562 (1961)

  2. Albus, K.: A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. Exp. Brain Res. 24, 159–179 (1975)

  3. Cajal, S. Ramón y: Histologie du systéme nerveux de l'homme et des vertébrés, Vol. IIA. Paris: Maloine 1911

  4. Burke, W., Sefton, A.J.: Discharge patterns of principal cells and interneurons in lateral geniculate nucleus of rat. J. Physiol. (Lond.) 187, 201–212 (1966)

  5. Cleland, B.G., Dubin, M.W., Levick, W.R.: Sustained and transient neurons in the cat's retina and lateral geniculate nucleus. J. Physiol. (Lond.) 217, 473–496 (1971)

  6. Creutzfeldt, O.D., Innocenti, G.M., Brooks, D.: Vertical organisation in the visual cortex (area 17) in the cat. Exp. Brain Res. 21, 315–336 (1974)

  7. Curtis, D.R., Crawford, J.M.: Central synaptic transmission-microelectrophoretic studies. Pharmacol. Rev. 9, 209–240 (1969)

  8. Dubin, M.W., Cleland, B.G.: Organization of visual inputs to interneurons of the lateral geniculate nucleus of the cat. J. Neurophysiol. 40, 410–427 (1976)

  9. Fernald, R., Chase, R.: An improved method for plotting retinal landmarks and focusing the eyes. Vision Res. 11, 95–96 (1971)

  10. Fukuda, Y., Stone, J.: Evidence of differential inhibitory influences on X- and Y-type relay cells in the cat's lateral geniculate nucleus. Brain Res. 113, 188–196 (1976)

  11. Gilbert, C.D., Kelly, J.P.: The projections of cells in different layers of the cat's visual cortex. J. comp. Neurol. 163, 81–106 (1975)

  12. Guillery, R.W.: Patterns of fiber degeneration in the dorsal lateral geniculate nucleus of the cat following lesions in the visual cortex. J. comp. Neurol. 130, 197–222 (1967)

  13. Guillery, R.W.: The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z. Zellforsch. 96, 1–38 (1969)

  14. Hess, R., Murata, K.: Effects of glutamate and GABA on specific response properties of neurons in the visual cortex. Exp. Brain Res. 21, 285–297 (1974)

  15. Hess, R., Negishi, K., Creutzfeldt, O.: The horizontal spread of intracortical inhibition in the visual cortex. Exp. Brain Res. 22, 415–419 (1975)

  16. Holländer, H.: The projection from the visual cortex to the lateral geniculate body (LGB). An experimental study with silver impregnation methods in the cat. Exp. Brain Res. 10, 219–235 (1970)

  17. Hubel, D.H., Wiesel, T.N.: Receptive fields, binocular interactions and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962)

  18. Hull, E.: Corticofugal influence in the macaque lateral geniculate nucleus. Vision Res. 8, 1285–1298 (1968)

  19. Ito, M., Sanides, D., Creutzfeldt, O.D.: A study of binocular convergence in cat visual cortex neurons. Exp. Brain Res. 28, 21–36 (1977)

  20. Iwama, K., Sakajura, H., Kasamatsu, T.: Presynaptic inhibition in the lateral geniculate body induced by stimulation of the cerebral cortex. Japan. J. Physiol. 15, 310–322 (1965)

  21. Jones, E.G., Powell, T.P.S.: An electron microscopic study of the mode of termination of cortico-thalamic fibers within the sensory relay nuclei of the thalamus. Proc. Roy. Soc. (Lond.) Ser. B 172, 173–185 (1969)

  22. Kalil, R.E., Chase, R.: Corticofugal influence on activity of lateral geniculate neurons in the cat. J. Neurophysiol. 33, 459–474 (1970)

  23. Kato, H., Yamamoto, M., Nakahama, H.: Intracellular recordings from lateral geniculate neurons of cat. Japan J. Physiol. 21, 307–323 (1971)

  24. Kawamura, S., Sprague, J.M., Niimi, K.: Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat. J. comp. Neurol. 159, 339–362 (1974)

  25. Kelly, J.P., van Essen, D.C.: Cell structure and function in the visual cortex of the cat. J. Physiol. (Lond.) 238, 515–547 (1974)

  26. Lee, B., Cleland, B., Creutzfeldt, O.D.: The retinal input to cells in area 17 of the cat's cortex. Exp. Brain Res. 30, 527–538 (1977)

  27. 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. 164, 287–304 (1975)

  28. Macchi, G., Rinvik, E.: Thalamo-telencephalic circuits: a neuroanatomical survey. In: Handbook of Electroencephalography and Clinical Neurophysiology (ed. A. Rémond), Vol. 2, Part A, pp. 86–133. Amsterdam: Elesevier 1976

  29. McIlwain, J.T., Creutzfeldt, O.D.: Microelectrode study of synaptic excitation and inhibition in the lateral geniculate nucleus of the cat. J. Neurophysiol. 30, 1–21 (1967)

  30. Moore, G.P., Segundo, J.P., Perkel, D.H., Levitan, H.: Statistical signs of synaptic interaction in neurons. Biophys. J. 10, 876–900 (1970)

  31. Niimi, K., Kawamura, S., Ishimaru, S.: Projections of the visual cortex to the lateral geniculate and posterior thalamic nuclei in the cat. J. comp. Neurol. 143, 279–312 (1971)

  32. Orem, J., Schlag, J.: Direct projections from cat frontal eye field to internal medullary lamina of the thalamus. Exp. Neurol. 33, 509–517 (1971)

  33. Palmer, L.A., Rosenquist, A.C.: Visual receptive field of single striate cortical units projecting to the superior colliculus in the cat. Brain Res. 67, 27–42 (1974)

  34. Pettigrew, J.D., Nikara, T., Bishop, P.O.: Responses to moving slits by single units in cat striate cortex. Exp. Brain Res. 6, 373–390 (1968)

  35. Richard, D., Gioanni, Y., Kitsikis, A., Buser, P.: A study of geniculate unit activity during cryogenic blockage of the primary cortex in the cat. Exp. Brain Res. 22, 235–242 (1975)

  36. Robson, J.A., Hall, W.C.: Connections of Layer VI in the striate cortex of the grey squirrel. Brain Res. 90, 133–139 (1975)

  37. Sanderson, K.J.: The projection of the visual field to lateral geniculate and medial interlaminar nuclei in the cat. J. comp. Neurol. 143, 101–118 (1971)

  38. Sanides, D., Donate-Oliver, F.: Identification and localization of some relay cells in cat visual cortex. In: Architectonics of the Cerebral Cortex, M.A.B. Brazier and H. Petsche (Edit.). IBRO Monograph Series, pp. 227–234. New York: Raven Press 1978

  39. Schmielau, F., Singer, W.: The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res. 120, 354–361 (1977)

  40. Singer, W., Creutzfeldt, O.: Reciprocal lateral inhibition of on- and off-center neurons in the lateral geniculate nucleus in the cat. Exp. Brain Res. 10, 311–330 (1970)

  41. Singer, W., Tretter, F., Cynader, M.: Organization of cat striate cortex: A correlation of receptive-field properties with afferent and efferent connections. J. Neurophysiol. 38, 1080–1098 (1975)

  42. Stone, J., Dreher, B.: Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex. J. Neurophysiol. 36, 551–567 (1973)

  43. Sumitomo, I., Nakamura, M., Iwama, K.: Location and function of the so-called interneurons of rat lateral geniculate body. Exp. Neurol. 51, 110–123 (1976)

  44. Suzuki, H., Kato, E.: Cortically induced presynaptic inhibition in cat's lateral geniculate body. Tohoku J. exp. Med. 86, 277–289 (1965)

  45. Thomas, R.C., Wilson, V.J.: Precise localization of Renshaw cells with a new marking technique. Nature (Lond.) 206, 211–213 (1965)

  46. Toyama, K., Matsunami, T., Ohno, T., Tokashiki, S.: An intracellular study of neuronal organization in the visual cortex. Exp. Brain Res. 21, 45–66 (1974)

  47. Tsumoto, T., Nakamura, S.: Inhibitory organization of the thalamic ventrobasal neurons with different peripheral representations. Exp. Brain Res. 21, 195–210 (1974)

  48. Tsumoto, T., Suzuki, D.A.: Effects of frontal eye field stimulation upon activities of the lateral geniculate body of the cat. Exp. Brain Res. 25, 291–306 (1976)

  49. Updyke, B.V.: The patterns of projections of cortical areas 17, 18 and 19 onto the laminae of the dorsal lateral geniculate nucleus in the cat. J. comp. Neurol. 163, 377–396 (1975)

  50. Vastola, E.F.: Steady-state effects of visual cortex on geniculate cells. Vision Res. 7, 599–609 (1967)

  51. Walker, A.E.: The primate thalamus. Chicago, London: University of Chicago Press, 1938 (reprint 1966)

  52. Widén, L., Ajmone-Marson, C.: Effects of corticopetal and corticofugal impulses upon single elements of the dorsolateral geniculate nucleus. Exp. Neurol. 2, 468–502 (1960)

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Present address: Dept. of Physiology, Kanazawa University Medical School, Kanazawa, 920 Japan

Present address: Albert Einstein College, Kennedy Center, Room 322, 1410 Pelham Parkway South, Bronx, N.Y. 10461, USA

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Tsumoto, T., Creutzfeldt, O.D. & Legéndy, C.R. Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat. Exp Brain Res 32, 345–364 (1978). https://doi.org/10.1007/BF00238707

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Key words

  • Visual system
  • Cortico-thalamic connections
  • Thalamocortical input
  • Functional organization
  • Cat