Neurophysiology of Perception: Non-Geniculostriate Pathways and the Neurones of Their Central Stations

  • Hugh Davson


The lateral geniculate body is the major processing nucleus for retinal information; however, in 1961 Altman and Carpenter drew attention to the thalamic projection from the superior colliculi; these bodies receive a powerful retinal projection, so that this collicular projection reveals an indirect access of visual information to the cerebral cortex. The target-areas of the ascending collicular projections are mainly within the pulvinar posterior system of the thalamus (PUL-PO), which, in turn, receives a strong projection from the visual cortex. Besides the colliculus, the adjacent pretectal region contains nuclei receiving retinal input; thus the circuitry for this subsidary processing system may be indicated crudely by Fig. 23.1. We shall see that the cortical influence on the colliculi is profound, so that their receptive-field characteristics become very similar to those of certain cortical cells.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Albus, K., Donate-Oliver, F., Sanides, D. & Fries, W. (1981) The distribution of pontine projection cells in visual and association cortex of the cat: an experimental study with horseradish peroxidase. J. Comp. Neurol. 201, 175–189.CrossRefGoogle Scholar
  2. Allman, J. M. & Kaas, J. H. (1974a) The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. Brain Res. 76, 247–265.CrossRefGoogle Scholar
  3. Allman, J. M. & Kaas, J. H. (1974b) A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus) Brain Res. 76, 247–265.CrossRefGoogle Scholar
  4. Allman, J. M., Kaas, J. H., Lane, R. H. & Miezin, F. M. (1972) A representation of the visual field in the inferior nucleus of the pulvinar in the owl monkey (Aotus trivirgatus). Brain Res. 40, 291–302.CrossRefGoogle Scholar
  5. Altman, J. & Carpenter, M. B. (1961) Fiber projections of the superior colliculus in the cat. J. Comp. Neurol. 116, 157–177.CrossRefGoogle Scholar
  6. Baker, J., Gibson, A., Glickstein, M. & Stein, J. (1976) Visual cells in the pontine nuclei of the cat. J. Physiol. 225, 415–433.CrossRefGoogle Scholar
  7. Baker, J., Gibson, A., Mower, G., Robinson, F. & Glickstein, M. (1983) Cat visual corticopontine cells project to the superior colliculus. Brain Res. 265, 227–232.CrossRefGoogle Scholar
  8. Bender, D. B. (1981) Retinotopic organization of macaque pulvinar. J. Neurophysiol. 46, 672–693.Google Scholar
  9. Bender, D. B. (1982) Receptive-field properties of neurons in the macaque inferior pulvinar. J. Neurophysiol. 48, 1–17.Google Scholar
  10. Bender, D. B. (1983) Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res. 279, 258–261.CrossRefGoogle Scholar
  11. Benevento, L. A. & Davis, B. (1977) Topographical projections of the prestriate cortex to the pulvinar nuclei in the macaque monkey: an autoradiographic study. Exp. Brain Res. 30, 405–424.Google Scholar
  12. Benevento, L. A. & Miller, J. (1981) Visual responses of single neurons in the caudal lateral pulvinar of the macaque monkey. J. Neorosci. 1, 1268–1278.Google Scholar
  13. Benevento, L. A. & Rezak, M. (1976) The cortical projections of the inferior pulvinar in the rhesus monkey (Macaca mulatta): an autoradiographic study. Brain Res. 108, 1–24.CrossRefGoogle Scholar
  14. Benevento, L. A. & Standage, G. P. (1983) The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral and medial pulvinar in the macaque monkey. J. Comp. Neurol. 217, 307–336.CrossRefGoogle Scholar
  15. Berman, N. & Jones, E. G. (1977) A retino-pulvinar projection in the cat. Brain Res. 134, 237–248.CrossRefGoogle Scholar
  16. Berman, N. & Sterling, P. (1976) Cortical suppression of the retinocollicular pathway in the monocularly deprived cat. J. Physiol. 255, 263–273.CrossRefGoogle Scholar
  17. Berson, D. M. & Graybiel, A. M. (1978) Parallel thalamic zones in the LP-pulvinar complex of the cat identified by their afferent and efferent connections. Brain Res. 147, 139–148.CrossRefGoogle Scholar
  18. Berson, D. M. & Graybiel, A. M. (1983) Organization of the striate-recipient zone of the cat’s lateralis posterior-pulvinar complex and its relations with the geniculostriate system. Neuroscience 9, 337–372.CrossRefGoogle Scholar
  19. Bunt, A. H., Hendrickson, A. E., Lund, J. S., Lund, R. D. & Fuchs, A. J. (1975) Monkey retinal ganglion cells: morphometric analysis and tracing of axonal projections, with a consideration of the peroxidase technique. J. Comp. Neurol. 164, 265–286.CrossRefGoogle Scholar
  20. Campos-Ortega, J. A. & Hayhow, W. R. (1972) On the organization of the visual cortical projections to the pulvinar in Macaca mulatta. Brain Behav. Evol. 6, 394–423.CrossRefGoogle Scholar
  21. Campos-Ortega, J. A., Hayhow, W. R. & Cluver, P. F. deV. (1970) A note on the problem of the retinal projections to the inferior pulvinar nucleus of primates. Brain Res. 22, 126–130.CrossRefGoogle Scholar
  22. Casagrande, V. A. & Diamond, I. T. (1974) Ablation study of the superior colliculus in the tree shrew (Tupaia glis). J. Comp. Neurol. 156, 207–238.CrossRefGoogle Scholar
  23. Chalupa, L. M., Coyle, R. S. & Lindsley, D. B. (1976) Effect of pulvinar lesions on pattern discrimination in monkeys. J. Neurophysiol. 39, 354–369.Google Scholar
  24. Chalupa, L. M. & Fish, S. E. (1978) Response characteristics of visual and extravisual neurones in the pulvinar and lateral posterior nuclei of the cat. Exp. Neurol. 61, 96–120.CrossRefGoogle Scholar
  25. Cowey, A. & Perry, V. H. (1980) The projection of the fovea to the superior colliculus in rhesus monkeys. Neuroscience 5, 53–61.CrossRefGoogle Scholar
  26. Cynader, M. & Berman, N. (1972) Receptive field organization of monkey superior colliculus. J. Neurophysiol. 35, 187–201.Google Scholar
  27. Distel, H. & Fries, W. (1982) Contralateral cortical projections to the superior colliculus in the macaque monkey. Exp. Brain Res. 48, 157–162.CrossRefGoogle Scholar
  28. Dreher, B. & Hoffmann, K.-P. (1973) Properties of excitatory and inhibitory regions in the receptive fields of single units in the cat’s superior colliculus. Exp. Brain Res. 16, 333–353.CrossRefGoogle Scholar
  29. Fukuda, Y. & Stone, J. (1974) Retinal distribution and central projections of Y-, X- and W-cells of the cat’s retina. J. Neurophysiol. 37, 749–772.Google Scholar
  30. Gattass, R., Oswaldo-Cruz, E. & Sousa, A. P. B. (1978) Visuotopic organization of the Cebus pulvinar: a double representation of the contralateral hemifield. Brain Res. 152, 1–16.CrossRefGoogle Scholar
  31. Glendenning, K. K., Hall, J. A. & Diamond, I. T. (1975) The pulvinar nucleus of Galago senegalensis. J. Comp. Neurol. 161, 419–457.CrossRefGoogle Scholar
  32. Goldberg, M. E. & Wurtz, R. H. (1972) Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. J. Neurophysiol. 35, 542–559.Google Scholar
  33. Graybiel, A. M. (1972) Some extrageniculate visual pathways in the cat. Invest. Ophthal. 11, 322–332.Google Scholar
  34. Graybiel, A. M. (1975) Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Res. 96, 1–23.CrossRefGoogle Scholar
  35. Harting, J. K. & Guillery, R. W. (1976) Organization of retinocollicular pathways in the cat. J. Comp. Neurol. 166, 133–144.CrossRefGoogle Scholar
  36. Harting, J. K., Hall, W. C. & Diamond, I. T. (1972) Evolution of the pulvinar. Brain Behav. Evol. 6, 425–452.Google Scholar
  37. Harting, J. K., Huerta, M. F., Frankfurter, A. J., Strominger, N. L. & Royce, G. J. (1980) Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J. Comp. Neurol. 192, 853–882.CrossRefGoogle Scholar
  38. Hayashi, Y., Sumitomo, I. & Iwama, K. (1967) Activation of lateral geniculate neurons by electrical stimulation of superior colliculus in cats. Jap. J. Physiol. 17, 638–651.CrossRefGoogle Scholar
  39. Hoffmann, K.-P. (1973) Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties. J. Neurophysiol. 36, 409–425.Google Scholar
  40. Hoffmann, K.-P. & Dreher, B. (1973) The spatial organisation of the excitatory region of receptive fields in the cat’s superior colliculus. Exp. Brain Res. 16, 354–370.CrossRefGoogle Scholar
  41. Hoffmann, K. P. & Sherman, S. M. (1974) Effects of early monocular deprivation on visual input to cat superior colliculus. J. Neurophysiol. 37, 1276–1286.Google Scholar
  42. Hoffmann, K.-P. & Stone, J. (1973) Central termination of W-, X- and Y-type ganglion cell axons from cat retina. Brain Res. 49, 500–501.CrossRefGoogle Scholar
  43. Hoffmann, K.-P. & Straschill, M. (1971) Influences of corticotectal and intertectal connections on visual responses in the cat’s superior colliculus. Exp. Brain Res. 12, 120–131.CrossRefGoogle Scholar
  44. Hubel, D. H., LeVay, S. & Wiesel, T. N. (1975) Mode of termination of retinotectal fibers in macaque monkey: an autoradiographic study. Brain Res. 96, 25–40.CrossRefGoogle Scholar
  45. Hubel, D. H. & Wiesel, T. N. (1972) Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. J. Comp. Neurol. 146, 421–450.CrossRefGoogle Scholar
  46. Itaya, S. K. & Van Hoesen, G. W. (1983) Retinal axons to the medial terminal nucleus of the accessory optic system in old world monkeys. Brain Res. 269, 361–369.CrossRefGoogle Scholar
  47. Itoh, K. et al. (1979) Cerebello-pulvino-cortical and retinopulvino-cortical pathway in the cat as revealed by the use of anterograde and retrograde transport of horseradish peroxidase. J. Comp. Neurol. 187, 349–357.CrossRefGoogle Scholar
  48. Kanaseki, T. & Sprague, J. M. (1974) Anatomical organization of pretectal nuclei and tectal laminae in the cat. J. Comp. Neurol. 158, 319–337.CrossRefGoogle Scholar
  49. Kawamura, K. & Chiba, M. (1979) Cortical neurons projecting to the pontine nuclei in the cat. An experimental study with the horseradish peroxidase technique. Exp. Brain Res. 35, 269–285.Google Scholar
  50. Kawamura, S., Sprague, J. M. & Niimi, K. (1974) Corticofugal projections from the visual cortex to the thalamus, pretectum and superior colliculus in the cat. J. Comp. Neurol. 158, 339–362.CrossRefGoogle Scholar
  51. Leichnetz, G. R., Spencer, R. F., Hardy, S. G. P. & Astruc, J. (1981) The prefrontal corticotectal projection in the monkey; an anterograde and retrograde study. Neuroscience 6, 1023–1041.CrossRefGoogle Scholar
  52. LeVay, S. & Gilbert, C. D. (1976) Laminar patterns of geniculo-cortical projection in the cat. Brain Res. 113, 1–19.CrossRefGoogle Scholar
  53. Lin, C. S. & Kaas, J. H. (1979) The inferior pulvinar complex in owl monkeys: architectonic subdivisions and patterns of input from superior colliculus and subdivisions of the visual cortex. J. Comp. Neurol. 187, 655–678.CrossRefGoogle Scholar
  54. Livingstone, M. S. & Hubel, D. H. (1982) Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc. Nat. Acad. Sci. 79, 6098–6101.CrossRefGoogle Scholar
  55. Lund, J. S., Lund, R. D., Hendrickson, A. E., Bunt, A. W. & Fuchs, A. F. (1975) 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, 287–303.CrossRefGoogle Scholar
  56. Marrocco, R. T. & Li, R. H. (1977) Monkey superior colliculus: properties of single cell’s and their afferent inputs. J. Neurophysiol. 40, 844–860.Google Scholar
  57. Mason, R. (1978) Functional organization in the cat’s pulvinar complex. Exp. Brain Res. 31, 51–66.CrossRefGoogle Scholar
  58. Mathers, L. H. & Rapisardi, S. C. (1973) Visual and somatosensory receptive fields of neurons in the squirrel monkey pulvinar. Brain Res. 64, 65–83.CrossRefGoogle Scholar
  59. Moors, J. & Vendrik, A. J. H. (1979) Responses of single units in the monkey superior colliculus to stationary flashing stimuli. Exp. Brain Res. 35, 333–347.Google Scholar
  60. Mower, G., Gibson, A. & Glickstein, M. (1979) Tectopontine pathways in the cat: laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus. J. Neurophysiol. 42, 1–15.Google Scholar
  61. Mower, G., Gibson, A., Robinson, F., Stein, J. & Glickstein, M. (1980) Visual pontocerebellar projections in the cat. J. Neurophysiol. 43, 355–366.Google Scholar
  62. Nakagawa, S. & Tanaka, S. (1984) Retinal projections to the pulvinar nucleus of the macaque monkey: a re-investigation using autoradiography. Exp. Brain Res. 57, 151–157.CrossRefGoogle Scholar
  63. Ogasawa, K., McHaffie, J. G. & Stein, B. E. (1984) Two visuocortical systems in cat. J. Neurophysiol. 52, 1126–1245.Google Scholar
  64. Ogren, M. & Hendrickson, A. (1976). Pathways between striate cortex and subcortical regions in Macaca mulatta and Saimiri sciureus: evidence for a reciprocal pulvinar connection. Exp. Neurol. 53, 780–800.CrossRefGoogle Scholar
  65. Palmer, L. A. & Rosenquist, A. C. (1974) Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat. Brain Res. 67, 27–42.CrossRefGoogle Scholar
  66. Partlow, G. D., Colonnier, M. & Szabo, J. (1977) Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscope study. J. Comp. Neurol. 171, 285–318.CrossRefGoogle Scholar
  67. Petersen, S. E., Robinson, D. L. & Keys, W. (1985) Pulvinar nucleis of the behaving rhesus monkey: visual responses and their modulation. J. Neurophysiol. 54, 867–886.Google Scholar
  68. Powell, T. P. S. (1976) Bilateral cortico-tectal projection from the visual cortex in the cat. Nature 260, 526–527.CrossRefGoogle Scholar
  69. Raczkowski, D. & Rosenquist, A. C. (1983) Connections of multiple visual cortical areas with the lateral posterior-pulvinar complex and adjacent thalamic nuclei in the cat. J. Neurosci. 3, 1912–1942.Google Scholar
  70. Rezak, M. & Benevento, L. A. (1979) A comparison of the organization of the dorsal lateral geniculate nucleus, the inferior pulvinar and adjacent lateral pulvinar to primary visual cortex (area 17) in the macaque monkey. Brain Res. 167, 19–40.CrossRefGoogle Scholar
  71. Rizzolatti, G., Buchtel, H. A., Camarda, R. & Scandolara, C. (1980) Neurons with complex visual properties in the superior colliculus of the macaque monkey Exp. Brain Res. 38, 37–42.CrossRefGoogle Scholar
  72. Robinson, D. A. (1972) Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 12, 1795–1808.CrossRefGoogle Scholar
  73. Robinson, D. A. & Wurtz, R. H. (1975) Superior colliculus neurons distinguish between stimulus movement and self-induced stimulus movement. ARVO Suppl.Google Scholar
  74. Schiller, P. H. & Koerner, F. (1971) Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35, 920–936.Google Scholar
  75. Schiller, P. H., Malpeli, J. G. & Schein, S. J. (1979) Composition of geniculostriate input to superior colliculus of the rhesus monkey. J. Neurophysiol. 42, 1124–1133.Google Scholar
  76. Schiller, P. H., Stryker, M. Cynader, M. & Berman, N. (1974) Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. J. Neurophysiol. 37, 181–194.Google Scholar
  77. Spatz, W. B. & Erdmann, G. (1974) Striate cortical projections to the lateral geniculate and other thalamic nuclei: a study using degeneration and autoradiographic tracing methods in the marmoset Callithrix. Brain Res. 82, 91–108.CrossRefGoogle Scholar
  78. Sprague, J. M. (1972) The superior colliculus and pretectum in visual behavior. Invest. Ophthal. 11, 473–482.Google Scholar
  79. Stein, B. E., Magalhaes-Castro, B. & Kruger, L. (1976) Relationship between visual and tactile representation in cat superior colliculus. J. Neurophysiol. 39, 401–419.Google Scholar
  80. Sterling, P. & Wickelgren, B. G. (1969) Visual receptive fields in the superior colliculus of the cat. J. Neurophysiol. 32, 1–15.Google Scholar
  81. Trojanowski, J. Q. & Jacobson, S. (1976) Areal and laminar distribution of some pulvinar cortical efferents in rhesus monkey. J. Comp. Neurol. 169, 371–392.CrossRefGoogle Scholar
  82. Ungergleider, L. G. & Christensen, C. A. (1977) Pulvinar lesions in monkeys produce abnormal eye movements during visual discrimination training. Brain Res. 136, 189–196.CrossRefGoogle Scholar
  83. Updyke, B. V. (1974) Characteristics of unit responses in superior colliculus of the Cebus monkey. J. Neurophysiol. 37, 296–309.Google Scholar
  84. Weyand, T. G., Malpeli, J. G., Lee, C. & Schwark, H. D. (1986a) Cat area 17. III. Response properties and orientation anisotropies of corticotectal cells. J. Neurophysiol. 56, 1088–1101.Google Scholar
  85. Weyand, T. G., Malpeli, J. G., Lee, C. & Schwark, H. D. (1986b) Cat area 17. IV. Two types of corticotectal cells defined by controlling geniculate inputs. J. Neurophysiol. 56, 1102–1108.Google Scholar
  86. Wilson, M. E. & Toyne, M. J. (1970) Retino-tectal and corticotectal projections in Macaca mulatta. Brain Res. 24, 395–406.Google Scholar
  87. Wurtz, R. H. (1969) Comparison of effects of eye movements and stimulus movements on striate cortical neurons of the monkey. J. Neurophysiol. 32, 987–994.Google Scholar
  88. Wurtz, R. H. & Albano, J. E. (1980) Visual motor function of the primate superior colliculus. Ann. Rev. Neurosci. 3, 189–226.CrossRefGoogle Scholar
  89. Wurtz, R. W. & Goldberg, M. E. (1972) Activity of superior colliculus in behaving monkey. III and IV. J. Neurophysiol. 35, 575–586, 587–596.Google Scholar
  90. Wurtz, R. W. & Goldberg, M. E. (1972) The primate superior colliculus and the shift of visual attention. Invest Ophthal. 11, 441–450.Google Scholar
  91. Wurtz, R. W. & Mohler, C. W. (1976a) Organization of monkey superior colliculus: enhanced visual response of superificial layer cells. J. Neurophysiol., 39, 745–765.Google Scholar
  92. Wurtz, R. W. & Mohler, C. W. (1976b) Enhancement of visual response in monkey striate cortex and frontal eye fields. J. Neurophysiol. 39, 766–772.Google Scholar

Copyright information

© Hugh Davson 1990

Authors and Affiliations

  • Hugh Davson
    • 1
    • 2
    • 3
  1. 1.St. Thomas’s HospitalSouthampton University Medical SchoolsLondonUK
  2. 2.King’s CollegeLondonUK
  3. 3.University CollegeLondonUK

Personalised recommendations