A model for the intracortical origin of orientation preference and tuning in macaque striate cortex

Visual Neuroscience

Volumn 16, Issue 2, 1999, Pages 303-318

  Adorjan P ^a   Levitt, J B ^b   Lund, J S ^b   Obermayer, K ^a  

^a TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Computational model; Macaque; Orientation selectivity; Receptive field; Spatial frequency

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENICULATE BODY; MACACA; NERVE CELL; NERVE CELL NETWORK; ORIENTATION; PHYSIOLOGY; THEORETICAL MODEL; VISUAL CORTEX;

ANIMALS; COMPUTER SIMULATION; GENICULATE BODIES; MACACA; MODELS, NEUROLOGICAL; MODELS, THEORETICAL; NERVE NET; NEURONS; ORIENTATION; VISUAL CORTEX;

EID: 0033103574     PISSN: 09525238     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0952523899162114     Document Type: Article

References (92)

1. ADORJÁN, P., BARNA, G., ÉRDI, P. & OBERMAYER, K. (1998). A statistical neural field approach to orientation selectivity. Neural Computing - Proceedings of the Computational Neuroscience Meeting CNS 98, (in press).
2. ALBRECHT, D.G. & HAMILTON, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217-237.
3. ANDERSON, J.C., DOUGLAS, R.J., MARTIN, K.A. & NELSON, J.C. (1994). Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 16-24.
4. ANDERSON, J.C., MARTIN, A.C. & WHITTERIDGE, D. (1993). Form, function, and intracortical projections of neurons in the striate cortex of monkey macacus nemestrinus. Cerebral Cortex 3, 412-420.
5. ANTONINI, A. & STRYKER, M.P. (1993). Rapid remodeling of axonal arbors in the visual cortex. Science 260, 1819-1821.
6. BARTSCH, H., STETTER, M. & OBERMAYER, K. (1997). A model for orientation tuning and contextual effects of orientation selective receptive fields. In Artificial Neural Networks-ICANN97, ed. GERSTNER, W., GERMOND, A., HASLER, M. & NICOUD, J., pp. 237-242. Springer.
7. BAUER, U., ADORJÁN, P., SCHOLZ, M., LEVITT, J., LUND, J. & OBERMAYER, K. (1997). On the anatomical basis of field size, contrast sensitivity, and orientation selectivity in macaque striate cortex: A model study. In Artificial Neural Networks-ICANN97, ed. GERSTNER, W., GERMOND, A., HASLER, M. & NICOUD, J. pp. 213-218. Springer.
8. BEAULIEU, C., KISVÁRDAY, Z., SOMOGYI, P., CYNADER, M. & COWEY, A. (1992). Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cerebral Cortex 2, 295-309.
9. BEN-YISHAI, R., BAR-OR, R.L. & SOMPOLINSKY, H. (1995). Theory of orientation tuning in visual cortex. Proceedings of the National Academy of Science of the U.S.A. 92, 3844-3848.
10. BERMAN, N.J., DOUGLAS, R.J. & MARTIN, K.A.C. (1992). GABA-mediated inhibition in the neural networks of visual cortex. In Progress in Brain Research, Vol. 90, ed. MIZE, R.R., MARC, R.E. & SILLITO, A.M., pp. 443-476. New York: Elsevier.
11. BLASDEL, G.G. & FITZPATRICK, D. (1984). Physiological organization of layer 4 in macaque striate cortex. Journal of Neuroscience 4, 880-895.
12. BLASDEL, G.G. & LUND, J.S. (1983). Termination of afferent axons in macaque striate cortex. Journal of Neuroscience 3, 1389-1413.
13. BLOOMFIELD, S.A. (1994). Orientation-sensitive amacrine and ganglion cells in the rabbit retina. Journal of Neurophysiology 71, 1672-1691.
14. BOLZ, J. & GILBERT, C.D. (1989). The role of horizontal connections in generating long receptive fields in cat visual cortex. European Journal of Neuroscience 1, 263-268.
15. BONDS, A.B. (1989). Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Visual Neuroscience 2, 41-55.
16. BONHOEFFER, T. & GOEDECKE, I. (1996). Development of identical orientation maps for two eyes without common visual experience. Nature 379, 251-254.
17. BOSKING, W.H., ZHANG, Y., SCHOFIELD, B. & FITZPATRICK, D. (1997). Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. Journal of Neuroscience 16, 2112-2127.
18. CARANDINI, M. & RINGACH, D.L. (1997). Predictions of a recurrent model of orientation selectivity. Vision Research 37, 3061-3071.
19. CELEBRINI, S., THORPE, S., TROTTER, Y. & IMBERT, M. (1993). Dynamics of orientation coding in area V1 of the awake monkey. Visual Neuroscience 10, 811-825.
20. CHAPMAN, B., ZAHS, K.R. & STRYKER, M.P. (1991). Relation of cortical cell orientation selectivity to augment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. Journal of Neuroscience 11, 1347-1358.
21. CRONER, L.J. & KAPLAN, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7-24.
22. CROOK, J.M., KISVÁRDAY, Z.F. & EYSEL, U.T. (1997). GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity. Visual Neuroscience 14, 141-158.
23. CROOK, J.M., KISVÁRDAY, Z.F. & EYSEL, U.T. (1998). Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: Reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques. European Journal of Neuroscience 10, 2056-2075.
24. DAS, A. (1996). Orientation in visual cortex: A simple mechanism emerges. Neuron 16, 447-480.
25. DAS, A. & GILBERT, C.D. (1997). Distorsions of visuotopic map match orientation singularities in primary visual cortex. Nature 387, 594-598.
26. DE VALOIS, R.L., ALBRECHI, D.G. & THORELL, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545-559.
27. DEANGELIS, G.C., ROBSON, J.G., OHZAWA, I. & FREEMAN, R.D. (1992). Organization of suppression in receptive fields of neurons in cat visual cortex. Journal of Neurophysiology 68, 144-163.
28. DINSE, H.R., KRUGER, K., MALLOT, H.A. & BEST, J. (1991). Temporal structure of cortical information processing: Cortical architecture, oscillations, and non-separability of spatio-temporal receptive field organization. In Neural Cooperativity, ed. KRUGER, J., pp. 68-104. Berlin: Springer.
29. DOUGLAS, R.J., KOCH, C., MAHOWALD, M., MARTIN, K.A.C. & SUAREZ, H.H. (1995). Recurrent excitation in neocortical circuits. Science 269, 981-985.
30. DOUGLAS, R.J., MARTIN, K.A.C. & WHITTERIDGE, D. (1988). Selective responses of visual cortical neurons do not depend on shunting inhibition. Nature 332, 642-644.
31. DOUGLAS, R.J., MARTIN, K.A.C. & WHITTERIDGE, D. (1991). An intracellular analysis of the visual responses of neurons in cat visual cortex. Journal of Physiology 440, 659-696.
32. DOUGLAS, R.J. & MARTIN, K.C. (1991). A functional microcircuit for cat visual cortex. Journal of Physiology 440, 735-769.
33. EYSEL, U.T., CROOK, J.M. & MACHEMER, H.F. (1990). GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Experimental Brain Research 80, 626-630.
34. FERSTER, D. (1986). Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. Journal of Neuroscience 6, 1284-1301.
35. FERSTER, D., CHUNG, S. & WHEAT, H. (1996). Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249-281.
36. FERSTER, D. & JAGADEESH, B. (1992). EPSP-IPSP interactions in cat visaual cortex studied in vivo whole-cell patch recording. Journal of Neuroscience 12, 1262-1274.
37. FITZPATRICK, D., LUND, J.S., SCHMECHEL, D.E. & TOWLES, A.C. (1987). Distribution of GABAergic neurons and axon terminals in the macaque striate cortex. Journal of Comparative Neurology 264, 73-91.
38. FREUND, T.F., MARTIN, K.A.C., SOLTESZ, I., SOMOGYI, P. & WHITTERIDGE, D. (1989). Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of macaque monkey. Journal of Comparative Neurology 289, 315-336.
39. HAMMOND, P. & POMFRETT, C.J.D. (1989). Influence of spatial frequency on tuning and bias for orientation and direction in the cat's striate cortex. Vision Research 30, 359-369.
40. HATA, Y., TSUMOTO, T., SATO, H., HAGIHARA, K. & TAMURA, H. (1988). Inhibition contributes to orientation selectivity in visual cortex of cat. Nature 335, 815-817.
41. HAWKEN, M.J. & PARKER, A.J. (1984). Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys. Experimental Brain Research 54, 367-372.
42. HAWKEN, M.J. & PARKER, A.J. (1987). Spatial properties in the monkey striate cortex. Proceedings of the Royal Society B (London) 231, 251-288.
43. HUBEL, D.H. & WIESEL, T.N. (1962). Receptive fields, binocular interaction and functional architecture in cat's visual cortex. Journal of Physiology 165, 559-568.
44. HUBEL, D.H. & WIESEL, T.N. (1974). Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor. Journal of Comparative Neurology 158, 295-306.
45. JAGADEESH, B. & FERSTER, D. (1990). Receptive field lengths in cat striate cortex can increase with decreasing stimulus contrast. Society of Neuroscience Abstracts 16, 293.
46. JONES, J.P. & PALMER, L.A. (1987a). An evaluation of the two-dimensional Gabor filter model of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1233-1258.
47. JONES, J.P. & PALMER, L.A. (1987b). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1187-1211.
48. JONES, J.P., STEPNOSKI, A. & PALMER, L.A. (1987). The two-dimensional spectral structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1212-1232.
49. KIM, D.S. & BONHOEFFER, T. (1994). Reverse occlusion leads to a precise restoration of orientation preference maps in visual cortex. Nature 370, 370-372.
50. LIVINGSTONE, M.S. (1998). Mechanisms of direction selectivity in macaque v1. Neuron 20, 509-526.
51. LUND, J.S. (1980). Intrinsic organization of the primate visual cortex, area 17, as seen in Golgi preparations. In The Organization of Cerebral Cortex: Proceedings of Neuroscience Research Program Colloquium, ed. ADELMAN, E., SCHMIDT, F.I., WORDEN, F.G. & DENNIS, S.G., pp. 105-124. Cambridge, Massachusetts: MIT Press.
52. LUND, J.S. (1987). Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4C and 5A. Journal of Comparative Neurology 257, 60-92.
53. MUNDEL, T., DIMITROV, A. & COWAN, J.D. (1997). Visual cortex circuitry and orientation tuning. In Advances in Neural Information Processing Systems, Vol. 9, ed. MOZER, M., JORDAN, M. & PETSCHE, T., pp. 887-893. Cambridge, Massachusetts: MIT Press.
54. NELSON, S., TOTH, L., SHETH, B. & SUR, M. (1994). Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 774-777.
55. OHZAWA, I., SCLAR, G. & FREEMAN, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651-667.
56. PEL X., VIDYASAGAR, T.R., VOLGUSHEV, M. & CREUTZFELD, O.D. (1994). Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. Journal of Neuroscience 14, 7130-7140.
57. PETERS, A., PAYNE, B.R. & BUDD, J. (1994). A numerical analysis of the geniculocortical input to striate cortex in the monkey. Cerebral Cortex 4, 215-29.
58. PRESS, W.H., TEUKOLSKY, S.A., VETTERLING, W.T. & FLANNERY, B.P. (1994). Numerical Recipies in C. Cambridge, Massachusetts: Cambridge University Press.
59. REID, R.C. & ALONSO, J.M. (1995). Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281-284.
60. REID, R.C., SOODAK, R.E. & SHAPLEY, R.M. (1991). Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505-529.
61. RINGACH, D.L., HAWKEN, M.J. & SHAPLEY, R. (1997a). Dynamics of excitatory and inhibitory mechanisms shaping the orientation tuning of neurons in V1. Society of Neuroscience Abstracts 23, 1544.
62. RINGACH, D.L., HAWKEN, M.J. & SHAPLEY, R. (1997b). Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281-284.
63. RODIECK, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583-601.
64. SABATINI, S.P. (1996). Recurrent inhibition and clustered connectivity as a basis for Gabor-like receptive fields in the visual cortex. Biological Cybernetics 74, 189-202.
65. SATO, H., KATSUYAMA, N., TAMURA, H., HATA, Y. & TSUMOTO, T. (1996). Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of macaque. Journal of Physiology 494, 757-771.
66. SCHILLER, P. (1982). Central connections of the retinal ON and OFF pathways. Nature 297, 580-583.
67. SCHUMER, R.A. & MOVSHON, J.A. (1984). Length summation in simple cells of cat striate cortex. Vision Research 24, 565-571.
68. SCHWARTZ, C. & BOLZ, J. (1991). Functional specificity of a long-range horizontal connection in cat visual cortex: A cross-correlation study. Journal of Neuroscience 11, 2995-3007.
69. SCLAR, G. & FREEMAN, R.D. (1982). Invariance of orientation tuning with stimulus contrast. Experimental Brain Research 46, 457-461.
70. SHERK, H. & HORTON, J.C. (1984). Receptive field properties in cat's area 17 in absence of ON-center geniculate input. Journal of Neuroscience 4, 381-393.
71. SILLITO, A.M. (1975). The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. Journal of Physiology 250, 305-329.
72. SILLITO, A.M., KEMP. J.A., MILSON, J.A. & BERARDI, N. (1980). A reevaluation of the mechanisms underlying simple cell orientation selectivity. Brain Research 194, 517-520.
73. SMITH, E.L., CHINO, Y.M., RIDDER, W.H., KITAGAWA, K. & LANGSTON, A. (1990). Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Visual Neuroscience 5, 525-545.
74. SOMERS, D.C., NELSON, S.B. & SUR, M. (1995). An emergent model of orientation selectivity in cat visual cortical simple cells. Journal of Neuroscience 15, 5448-5465.
75. SOMPOLINSKY, H. & SHAPLEY, R. (1997). New perspectives on the mechanisms for orientation selectivity. Current Opinion in Neurobiology 7, 514-522.
76. SPEAR, P.D., MOORE, R.J., KIM, C.B.Y., XUE, J. & TUMOSA, N. (1994). Effects on aging on primate visual system: Spatial and temporal processing by lateral geniculate neurons in young adult and old rhesus monkeys. Journal of Neurophysiology 72, 402-420.
77. STETTER, M., ADORJÁN, P., BARTSCH, H. & OBERMAYER, K. (1998). Modelling contrast adaptation and contextual effects in primary visual cortex. In Proceedings of the International Conference on Neural Information Processing ICONIP 98 2, 669-672.
78. TANAKA, K. (1983). Cross-correlation analysis of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 1303-1318.
79. TODOROV, E., SIAPAS, A. & SOMERS, D. (1997). A model of recurrent interactions in primary visual cortex. In Advances in Neural Information Processing Systems, Vol. 9, ed. MOZER, M.C., JORDAN, M.I. & PETSCHE, T., pp. 1118-124. Cambridge, Massachusetts: MIT Press.
80. TROYER, T.W., KRUKOWSKI, A.E., PRIEBE, N.J. & MILLER, K.D. (1998). Contrast-invariant orientation tuning in visual cortex: Feedforward tuning and correlation-based intracortical connectivity. Journal of Neuroscience 18, 5908-5927.
81. TSODYKS, M.V. & SEJNOWSKI, T. (1995). Rapid state switching in balanced cortical network models. Network: Computation in Neural Systems 6, 111-124.
82. TSUMOTO, T., ECKART, W. & CREUTZFELD, O.D. (1979). Modifications of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Experimental Brain Research 34, 351-363.
83. VIDYASAGAR, T.R., PEI, X. & VOLGUSHEV, M. (1996). Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends in Neuroscience 19, 272-277.
84. VIDYASAGAR, T.R. & SIGUENZA, J.A. (1985). Relationship between orientation tuning and spatial frequency in neurones of cat area 17. Experimental Brain Research 57, 628-631.
85. VOLGUSHEV, M., VIDYASAGAR, T.R. & PEI, X. (1995). Dynamics of the orientation tuning of postsynaptic potentials in the cat visual cortex. Visual Neuroscience 12, 621-628.
86. VOLGUSHEV, M., VIDYASAGAR, T.R. & PEI, X. (1996). A linear model fails to predict orientation selectivity of cells in the cat visual cortex. Journal of Physiology 496, 597-606.
87. WEBSTER, M.A. & DE VALOIS, R.L. (1985). Relationship between spatial-frequency and orientation tuning of striate cells. Journal of Optical Society America A 2, 1124-1132.
88. WEHMEIER, U., DONG, D., KOCH, C. & VAN ESSEN, D. (1989). Modeling the visual system. In Methods in Neuronal Modeling, ed. KOCH, C. & SEGEV, I., pp. 335-359. Cambridge, Massachusetts: MIT Press.
89. WOLF, F., BAUER, H.U., PAWELZIK, K. & GEISEL, T. (1996). Organization of the visual cortex. Nature 382, 306-307.
90. WÖRGÖTTER, F. & EYSEL, U.T. (1991). Topographical aspects of intracortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual-cortex. European Journal of Neuroscience 3, 1232-1244.
91. WÖRGÖTTER, F. & KOCH, C. (1991). A detailed model of the primary visual pathway in the cat: Comparison of afferent excitatory and intracortical inhibitory schemes for orientation selectivity. Journal of Neuroscience 11, 1959-1979.
92. YOSHIOKA, T., LEVITT, J.B. & LUND, J.S. (1994). Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections. Visual Neuroscience 11, 467-489.