Skip to main content

Physiological Evidence for Two Visual Subsystems

  • Chapter
Matters of Intelligence

Part of the book series: Synthese Library ((SYLI,volume 188))

Abstract

Many studies, including some in this volume, describe two distinct types of higher functions in the visual system. One visual function is concerned primarily with evaluation using information about shape, color and pattern to identify or categorize objects. The other function is more involved with spatial considerations, making use of visual information to determine the position movements and spatial relationships among objects. The notion that the visual system performs two distinguishable types of higher functions is well established, and many pairs of terms have been applied in describing this dichotomy: evaluating/orienting, what/where, focal/ambient, examining/noticing, figural/spatial, foveal/ambient, and object/spatial. 1 Although these terminologies may not all describe precisely the same visual functions, they draw very similar distinctions between two qualitatively different aspects of vision.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. D. Ingle, “Two visual mechanisms underlying the behavior of fish,” Psychol. Forsch., 31, 44-51, 1967

    Article  PubMed  Google Scholar 

  2. G. E. Schneider, “Contrasting visuomotor functions of tectum and cortex in the golden hamster,” Psychol. Forsch., 31, 52–62, 1967

    Article  PubMed  Google Scholar 

  3. C. B. Trevarthen, “Two mechanisms of vision in primates,”Psychol. Forsch., 31, 299–337, 1968

    Article  PubMed  Google Scholar 

  4. L. Weiskrantz, “Behavioral analysis of the monkey’s visual system,” Proc. R. Soc. Lond. B, 182, 427–455, 1972

    Article  PubMed  Google Scholar 

  5. B. G. Breitmeyer and L. Ganz, “Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression and information processing,” Psychol. Rev., 83, 1–36, 1976

    Article  PubMed  Google Scholar 

  6. J. Stone, B. Dreher and A. Leventhal, “Hierarchical and parallel mechanisms in the organization of visual cortex,” Brain Res. Rev., 1, 345–394, 1979

    Article  Google Scholar 

  7. M. Mishkin, L. G. Ungerleider and K. A. Macko, “Object vision and spatial vision: two cortical pathways,” Trends Neurosci., 6, 414–417, 1983.

    Article  Google Scholar 

  8. G. von Bonin and P. Bailey, The neocortex of macaca mulatta, U. Illinois Press, Urbana, 1947.

    Google Scholar 

  9. K. Brodmann, “Beitrage zur histologischen Localisation der Grosshirnrinde. Dritte Mitteilung. Die Rinderfelder der neideren Affen,” J. Psychol. Neurol., 4, 177–226, 1905.

    Google Scholar 

  10. D. J. Tolhurst, “Separate channels for the analysis of the shape and the movement of a moving visual stimulus,” J. Physiol. (Land), 231, 385–402, 1973

    Google Scholar 

  11. D. J. Tolhurst, “Sustained and transient channels in human vision,” Vision. Res., 15, 1151–1155, 1975

    Article  PubMed  Google Scholar 

  12. Breitmeyer and Ganz, 1976

    Google Scholar 

  13. Stone et al., 1979

    Google Scholar 

  14. J. Stone, Parallel processing in the visual system, Plenum Press, New York, 1983.

    Google Scholar 

  15. Schneider, 1967.

    Google Scholar 

  16. Trevarthen, 1968.

    Google Scholar 

  17. L. G. Ungerleider and M. Mishkin, “Two cortical visual systems,” in: Analysis of visual behavior, D. J. Ingle, M. A. Goodale and R. W. Mansfield, eds., MIT Press, Cambridge, Mass., 549–586, 1982;

    Google Scholar 

  18. Mishkin et al., 1983.

    Google Scholar 

  19. Reviewed by Ungerleider and Mishkin, 1982.

    Google Scholar 

  20. C. G. Gross, “Visual functions of inferotemporal cortex,” in: Handbook of sensory physiology, Vol. VII/3, R. Jung, ed., Springer, Berlin, 451–482, 1973

    Google Scholar 

  21. P. Dean, “Effects of inferotemporallesions on the behavior of monkeys,” Psychol. Bull., 83, 41–71, 1976

    Article  PubMed  Google Scholar 

  22. P. Dean, “Visual behavior in monkeys with inferotemporallesions,” in: Analysis of visual behavior, MIT Press, Cambridge, Mass. 587–628, 1982

    Google Scholar 

  23. M. Wilson, “Visual systems: pulvinar-extrastriate cortex,” in: Handbook of behavioral neurobiology, Vol. 1: Sensory Integration, R. B. Masterton, ed., Plenum Press, New York, 209–247, 1978

    Google Scholar 

  24. C. G. Gross, C. J. Bruce, R. Desimone, J. Freming and R. Gattass, “Cortical visual areas of the temporal lobe,” in: Multiple cortical visual areas, C. N. Woolsey, ed., Humana Press, Clifton, N. J., 187–216, 1981

    Google Scholar 

  25. Ungerleider and Mishkin, 1982.

    Google Scholar 

  26. Dean, 1976.

    Google Scholar 

  27. Ungerleider and Mishkin, 1982.

    Google Scholar 

  28. W. Pohl, “Dissociation of spatial discrimination deficits following frontal and parietal lesions in monkeys,” J. Oomp. Physiol. Psychol., 82, 227–239, 1973.

    Article  Google Scholar 

  29. C. G. Gross, C. E. Rocha-Miranda and D. B. Bender, “Visual properties of neurons in inferotemporal cortex of the macaque,” J. Neurophysiol., 35, 96–111, 1972

    PubMed  Google Scholar 

  30. Gross, 1973

    Google Scholar 

  31. Gross et al., 1981

    Google Scholar 

  32. R. Desimone and C. G. Gross, “Visual areas in the temporal cortex of the macaque,” Brain Res., 178, 363–380, 1979.

    Article  PubMed  Google Scholar 

  33. Gross, 1973.

    Google Scholar 

  34. Gross et al., 1972

    Google Scholar 

  35. D. I. Perrett, E. T. Rolls and W. Caan, “Visual neurones responsive to faces in monkey temporal cortex,” Exp. Brain Res., 47, 329–342, 1982.

    Article  PubMed  Google Scholar 

  36. D. L. Robinson, M. E. Goldberg and G. B. Stanton, “Parietal association cortex in the primate: sensory mechanisms and behavioral modulations,” J. Neurophysiol., 41, 910–932, 1978

    PubMed  Google Scholar 

  37. B. C. Motter and Y. B. Mountcastle, “The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization,” J. Neurosci., 1, 3–26, 1981.

    PubMed  Google Scholar 

  38. Robinson et al., 1978.

    Google Scholar 

  39. Motter and Mountcastle, 1981.

    Google Scholar 

  40. R. H. Wurtz, M. E. Goldberg and D. L. Robinson, “Behavioral modulation of visual responses in the monkey: stimulus selection for attention and movement,” Prog. Psychobiol. Physiol., 9, 43–83, 1980.

    Google Scholar 

  41. V. N. Mountcastle, J. C. Lynch, A. Georgopoulos, H. Sakata and C. Acuna, “Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space,” J. Neurophysiol., 38, 871–908, 1975

    PubMed  Google Scholar 

  42. Robinson, et al., 1978

    Google Scholar 

  43. R. A. Anderson and Y. B. Mountcastle, “The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex,” J. Neurosci., 3, 432–548, 1983

    Google Scholar 

  44. H. Sakata, H. Shibutani and K. Kawano, “Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey,” J. Neurophysiol., 43, 1654–1672,1980

    PubMed  Google Scholar 

  45. H. Sakata, H. Shibutani and K. Kawano, “Functional properties of visual tracking neurons in posterior parietal association cortex of the monkey,” J. Neurophysiol., 49, 1364–1380, 1983.

    PubMed  Google Scholar 

  46. M. C. Bushnell, M. E. Goldberg and D. L. Robinson, “Enhancement of visual responses in monkey cerebral cortex. 1. Modulation in posterior parietal cortex related to selective attention,” J. Neurophysiol., 46, 755–772, 1981.

    PubMed  Google Scholar 

  47. B. J. Richmond and T. Sato, “Visual responses of inferior temporal neurons are modified by attention to different stimulus dimensions,” Soc. Nwrosci. Abstr., 8, 812, 1982.

    Google Scholar 

  48. D. C. Van Essen, “Visual areas of the mammalian cerebral cortex,” Ann. Rev. Neurosci., 2, 227–263, 1979.

    Article  PubMed  Google Scholar 

  49. D. C. Van Essen, W. T. Newsome and J. L. Bixby, “The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey,” J. Neurosci., 2, 265–283, 1982.

    PubMed  Google Scholar 

  50. D. C. Van Essen and J. H. R. Maunsell, “Hierarchical organization and functional streams in the visual cortex,”Trends Neurosci., 6, 370–375, 1983(a)

    Article  Google Scholar 

  51. Mishkin et al., 1983

    Google Scholar 

  52. K. S. Rockland and D. N. Pandya, “Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey,” Brain Res., 179, 3–20, 1979

    Article  PubMed  Google Scholar 

  53. R. Desimone, J. Fleming and C. G. Gross, “Prestriate afferents to inferotemporal cortex: an HRP study,” Brain Res., 184, 41–55, 1980.

    Article  PubMed  Google Scholar 

  54. S. M. Zeki, “Cortical projections from two prestriate areas in the monkey,” Brain Res., 34, 19–35, 1971.

    Article  PubMed  Google Scholar 

  55. J. H. R. Maunsell and D. C. Van Essen, “The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey,”J. Neurosci., 3, 2563–2586, 1983(c).

    PubMed  Google Scholar 

  56. Zeki, 1971

    Google Scholar 

  57. B. G. Cragg, “The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method,” Vision Res., 9, 733–747, 1969

    Article  PubMed  Google Scholar 

  58. S. M. Zeki, “Representation of central fields in prestriate cortex of monkey,” Brain Res., 14, 271–291, 1969.

    Article  PubMed  Google Scholar 

  59. R. Dubner and S. M. Zeki, “Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus,” Brain Res., 35, 528–532, 1971.

    Article  PubMed  Google Scholar 

  60. S. M. Zeki, “Functional organization of a visual area in the posterior bank of the superior temporal sulcus,” J. Physiol. (Lond), 236, 549–573, 1974

    Google Scholar 

  61. D. C. Van Essen, J. H. R. Maunsell and J. L. Bixby, “The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties and topographic organization,” J. Compo Neurol., 199, 293–326, 1981

    Article  Google Scholar 

  62. T. D. Albright, R. Desimone and C. G. Gross, “Columnar organization of directionally selective cells in visual area MT of the macaque,” J. Neurophysiol., 51, 16–31, 1984.

    PubMed  Google Scholar 

  63. Maunsell and Van Essen, 1983(a)

    Google Scholar 

  64. J. H. R. Maunsell and D. C. Van Essen “Functional properties of neurons in the middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity,” J. Neu;ophysiol., 49, 1148–1167, 1983(b).

    Google Scholar 

  65. S. M. Zeki, “Color coding in the rhesus monkey prestriate cortex,” Brain Res., 53, 422–427, 1973

    Article  PubMed  Google Scholar 

  66. S. M. Zeki, “Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex,” J. Physiol. (Lond), 277, 273–290, 1978.

    Google Scholar 

  67. S. J. Schein, R. T. Marrocco and F. M. deMonasterio, “Is there a high concentration of color-selective cells in area V4 of monkey visual cortex?” J. Neurophysiol., 47, 193–213, 1982.

    PubMed  Google Scholar 

  68. C. Enroth-Cugell and J. G. Robson, “The contrast sensitivity of retinal ganglion cells of the cat,” J. Physiol. (Lond), 187,517–552, 1966.

    Google Scholar 

  69. R. W. Rodieck, “Visual pathways,” Ann. Rev. Neurosci., 2, 193–226, 1979

    Article  PubMed  Google Scholar 

  70. P. Lennie, “Parallel visual pathways: a review,” Vision Res., 20, 561–591, 1980(a)

    Article  PubMed  Google Scholar 

  71. Stone, 1983

    Google Scholar 

  72. Stone, 1983

    Google Scholar 

  73. S. M. Sherman, J. R. Wilson, J. H. Kaas and S. V. Webb, “X- and V-like cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus),” Science, 192, 475–477,1976

    PubMed  Google Scholar 

  74. B. Dreher, Y. Fukada and R. W. Rodieck, “Identification, classification and anatomical segregation of cells with X-like and Y -like properties in the lateral geniculate of old world primates,” J. Physiol. (Lond), 258, 433–452, 1976.

    Google Scholar 

  75. Dreher et al., 1976.

    Google Scholar 

  76. P. Gouras, “Antidromic responses of orthodromically identified ganglion cells in monkey retina,” J. Physiol. (Lond), 204, 407–419, 1969

    Google Scholar 

  77. F. M. deMonasterio and P. Gouras, “Functional properties of ganglion cells of the rhesus monkey retina,” J. Physiol. (Lond), 251, 167–195, 1975

    Google Scholar 

  78. P. H. Schiller and J. G. Malpeli, “Properties and tectal projections of monkey retinal ganglion cells,” J. Neurophysiol., 40, 428–445, 1977(a)

    PubMed  Google Scholar 

  79. A. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. (Lond), in press.

    Google Scholar 

  80. E. Kaplan and R. M. Shapley, “X- and Y- cells in the lateral geniculate nucleus of macaque monkeys,” J. Physiol. (Lond), 330, 125–143, 1982

    Google Scholar 

  81. C. Blakemore and F. Vital-Durance, “Distribution of X- and V-cells in the monkey’s lateral geniculate nucleus,” J. Physiol. (Long), 320, 17P-18P, 1981

    Google Scholar 

  82. A. M. Derrington and P. Lennie, “Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque,” J. Physiol. (Lond), in press.

    Google Scholar 

  83. J. P. Kelly and C. D. Gilbert, “The projections of different morphological types of ganglion cells in the cat retina,” J. Compo Neurol., 163,65–80, 1975

    Article  Google Scholar 

  84. D. B. Bowling and C. M. Michael, “Projection patterns of single physiologically identified optic tract fibres in the cat,” Nature (Lond), 286, 899–902, 1980.

    Article  Google Scholar 

  85. J. Stone and K. P. Hoffman, “Very slow conducting ganglion cells in the eat’s retina: a major new functional type?” Brain Res., 43, 610–616, 1972.

    Article  PubMed  Google Scholar 

  86. R. W. Rodieck, The Vertebrate Retina, Freeman, San Francisco, 1973.

    Google Scholar 

  87. Schiller and Malpeli, 1977(a)

    Google Scholar 

  88. Stone, 1983.

    Google Scholar 

  89. M. Yukie and E. Iwai, “Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys,” J. Compo Neurol., 201, 81–97, 1981

    Article  Google Scholar 

  90. K. Yoshida and L. A. Beneveneto, “The projection from the dorsal lateral geniculate nucleus of the thalamus to extrastriate visual cortex association cortex in the macaque monkey,” Neurosci. Lett., 22, 103–108, 1981.

    Article  PubMed  Google Scholar 

  91. D. H. Hubel and T. N. Wiesel, “Laminar and columnar distribution of geniculocortical fibers in macaque monkey,” J. Compo Neurol., 146,421–450, 1972.

    Article  Google Scholar 

  92. P. H. Schiller, J. G. Malpeli and S. J. Schein, “Composition of geniculostriate input to superior colliculus of the rhesus monkey,” J. Neurophysiol., 42, 1124–1133, 1979.

    PubMed  Google Scholar 

  93. J. S. Lund and R. G. Boothe, “Introlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey,” J. Compo Neurol., 159, 305–334,1975

    Article  Google Scholar 

  94. J. S. Lund, G. H. Henry, C. L. MacQueen and A. R. Harvey, “Anatomical organization of the primary visual cortex (area 17) of the cat: a comparison with area 17 of the macaque monkey,” J. Compo Neurol., 184, 599–618, 1979.

    Article  Google Scholar 

  95. Lund, et al., 1979.

    Google Scholar 

  96. Ibid.

    Google Scholar 

  97. J. S. Lund, R. D. Lund, A. E. Hendrickson, A. H. Brunt and A. F. Fuchs, “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. Compo Neurol., 164, 287–304, 1976.

    Article  Google Scholar 

  98. J. G. Malpeli, P. H. Schiller and C. L. Colby, “Response properties of single cells in monkey striate cortex during reversible inactivation of individual lateral geniculate laminae,” J. Neurophysiol., 46, 1102–1119, 1981.

    PubMed  Google Scholar 

  99. D. A. Robinson, “A method of measuring eye movements using a scleral search coil in a magnetic field,” IEEE Trans. Biomed.. Eng., 10, 137–145,1963.

    PubMed  Google Scholar 

  100. Cragg, 1969

    Google Scholar 

  101. Zeki, 1969, 1971.

    Google Scholar 

  102. U. Mitzdord and W. Singer, “Excitatory synaptic ensemble properties in the visual cortex of the macaque monkey: a current source density analysis of electrically evoked potentials,” J. Compo Neural., 187,71–84, 1979.

    Article  Google Scholar 

  103. P. Lennie, “Perceptual signs of parallel pathways,” Phil. Trans. R. Soc. Lond. B, 290, 23–37, 1980(b).

    Article  Google Scholar 

  104. Kaplan and Shapley, 1982.

    Google Scholar 

  105. R. M. Shapley and J. D. Victor, “The effect of contrast on the transfer properties of cat retinal ganglion cells,” J. Physiol. (Lond), 285, 275–298, 1978.

    Google Scholar 

  106. S. Hochstein and R. M. Shapley, “Quantitative analysis of retinal ganglion cell classifications,” J. Physiol. (Lond), 262, 237–264, 1976

    Google Scholar 

  107. H. G. Jakiela, C. Enroth-Cugell and R. M. Shapley, “Adaptation and dynamics in X-cells and Y -cells of cat retina,” Exp. Brain Res., 24, 335–342, 1976

    Article  PubMed  Google Scholar 

  108. Lennie, 1980(b)

    Google Scholar 

  109. Maunsell and Van Essen, 1983(c).

    Google Scholar 

  110. J. Tigges, M. Tigges, N. A. Cross, R. L. McBride, W. D. Letbetter and S. Anschel, “Subcortical structure projecting to visual cortical areas in squirrel monkey,” J. Camp. Neural., 209, 29–40, 1982.

    Article  Google Scholar 

  111. Motter and Mountcastle, 1981.

    Google Scholar 

  112. For example, Desimone and Gross, 1979.

    Google Scholar 

  113. Schiller and Malpeli, 1977(b).

    Google Scholar 

  114. C. E. Rocha-Miranda, D. B. Bender, C. G. Gross and M. Mishkin, “Visual activation of neurons in inferotemporal cortex depends upon striate cortex and forebrain commissures,” J. Neurophysiol., 38, 475–491, 1975.

    PubMed  Google Scholar 

  115. Stone, 1983.

    Google Scholar 

  116. M. Carlson, “Characteristics of sensory deficits following lesions of Brodmann’s areas 1 and 2 in the front central gyrus of Macaca mulatta,” Brain Res., 204, 424–430, 1981.

    Article  PubMed  Google Scholar 

  117. R. W. Dykes, “Parallel processing of somatosensory information: a theory,” Brain Res. Rev., 6, 47–115, 1983.

    Article  Google Scholar 

  118. M. M. Merzenich and J. H. Kaas, “Principles of organization of sensory-perceptual systems in mammals,” Prog. Psychobiol. Psychol., 9, 2–42, 1980.

    Google Scholar 

  119. E. B. Kevern, “Olfaction and taste: dual systems for sensory processing,” it Trends Neurosci., 1, 32–34, 1978

    Article  Google Scholar 

  120. S. F. Takagi, “Dual systems for sensory olfactory processing the higher primates,” Trends. Neurosci., 2, 313–315, 1979.

    Article  Google Scholar 

  121. J. Atema, “Structures and functions of the sense oftaste in the catfish,” Brain Behav. Evol., 4, 273–294, 1971

    Article  PubMed  Google Scholar 

  122. T. E. Finger and Y. Morita, “Two gustatory systems: facial and gagal gustatory nuclei have different brainstem connections,” Science, 227, 776–778, 1985.

    Article  PubMed  Google Scholar 

  123. H. B. Barlow and W. R. Levick, “The mechanism of directionally selective units in rabbit’s retina,” J. Physiol. (Lond), 178,477–504, 1965.

    Google Scholar 

  124. Stone, 1983.

    Google Scholar 

  125. Breitmeyer and Ganz, 1976.

    Google Scholar 

  126. Tolhurst, 1973, 1975

    Google Scholar 

  127. Stone, et al., 1979, 1983.

    Google Scholar 

  128. D. H. Hubel and T. N. Wiesel, “Receptive fields and functional architecture of monkey striate cortex,” J. Physiol. (Lond), 195, 215–243, 1968.

    Google Scholar 

  129. G. F. Poggio and B. Fischer, “Binocular interactions and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey,” J. Neurophysiol., 40, 1392–1405, 1977.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1987 D. Reidel Publishing Company, Dordrecht, Holland

About this chapter

Cite this chapter

Maunsell, J.H.R. (1987). Physiological Evidence for Two Visual Subsystems. In: Vaina, L.M. (eds) Matters of Intelligence. Synthese Library, vol 188. Springer, Dordrecht. https://doi.org/10.1007/978-94-009-3833-5_3

Download citation

  • DOI: https://doi.org/10.1007/978-94-009-3833-5_3

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-8206-8

  • Online ISBN: 978-94-009-3833-5

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics