An emergent model of orientation selectivity in cat visual cortical simple cells

Journal of Neuroscience

Volumn 15, Issue 8, 1995, Pages 5448-5465

  Somers, David C ^a   Nelson, Sacha B ^b   Sur, Mriganka ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

computational neuroscience; cortical circuits; intracortical inhibition; orientation selectivity; recurrent excitation; visual cortex

Indexed keywords

ANIMAL CELL; ARTICLE; CAT; FEEDBACK SYSTEM; LATERAL GENICULATE BODY; MATHEMATICAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; VISUAL CORTEX; VISUAL ORIENTATION;

EID: 0029160319     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-08-05448.1995     Document Type: Article

References (128)

1. Ahmed BA, Andersen JC, Douglas RJ, Martin KAC, Nelson JC (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol 341:39-49.
2. Albrecht DG, Geisler W (1991) Motion selectivity and the contrastresponse function of simple cells in the striate cortex. Vis Neurosci 7:531-546.
3. Anderson JC, Douglas RJ, Martin KAC, Nelson JC (1994a) Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex. J Comp Neurol 341:16-24.
4. Anderson JC, Douglas RJ, Martin KAC, Nelson JC (1994b) Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex. J Comp Neurol 341:25-38.
5. Beaulieu C, Colonnier M (1983) The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat. J Comp Neurol 217 :337-344.
6. Beaulieu C, Colonnier M (1985) A laminar analysis of the number of round asymmetrical and flat symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. J Comp Neurol 231:180-189.
7. Beaulieu C, Somogyi P (1990) Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. Eur J Neurosci 2:296-303.
8. Bell AJ, Mainen ZF, Tsodyks M, Sejnowski TJ (1995) "Balancing" of conductances may explain irregular cortical spiking. Technical report INC-9502. San Diego: Institute for Neural Computation, UCSD.
9. Berman NJ, Douglas RJ, Martin KAC, Whitteridge D (1991) Mechanisms of inhibition in cat visual cortex. J Physiol (Lond) 440:697-722.
10. Bishop PO, Coombs JS, Henry GH (1973) Receptive fields of simple cells in the cat striate cortex. J Physiol (Lond) 231:31-60.
11. Bonds AB (1989) Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis Neurosci 2:41-55.
12. Bonds AB (1993) The encoding of cortical contrast gain control. In: Contrast sensitivity (Shapley RM, Lam D-K, eds), pp 215-230. Cambridge, MA: MIT Press.
13. Bush PC, Sejnowski TC (1994) Effects of inhibition and dendritic saturation in simulated neocortical pyramidal cells. J Neurophysiol 74: 2183-2193.
14. Carandini M, Heeger DJ (1994) Summation and division by neurons in primate visual cortex. Science 264:1333-1336.
15. Chapman B, Zahs KR, Stryker MP (1991) Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J Neurosci 11:1347-1358.
16. Chino YM, Kaplan E (1988) Abnormal orientation bias of LGN neurons in strabismic cats. Invest Ophthalmol Vis Sci 29:644-648.
17. Connors BW, Gutnick MJ, Prince DA (1982) Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302-1320.
18. Creutzfeldt OD, Kuhnt U, Benevento LA (1974a) An intracellular analysis of visual cortical neurons to moving stimuli: responses in a cooperative neuronal network. Exp Brain Res 21:251-274.
19. Creutzfeldt OD, Innocenti G, Brooks D (1974b) Vertical organization in the visual cortex (area 17). Exp Brain Res 21:315-336.
20. Crook JM, Eysel UT (1992) GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on orientation tuning. J Neurosci 12:1816-1825.
21. Dean AF, Tolhurst DJ (1986) Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex. Exp Brain Res 62:143-151.
22. DeAngelis GC, Robson JG, Ohzawa I, Freeman RD (1992) Organization of suppression in receptive fields of neurons in cat visual cortex. J Neurophysiol 68:144-163.
23. Dehay C, Douglas RJ, Martin KAC, Nelson C (1991) Excitation by geniculocortical synapses is not "vetoed" at the level of dendritic spines in cat visual cortex. J Physiol (Lond) 440:723-734.
24. Douglas RJ, Martin KAC (1991) A functional microcircuit for cat visual cortex. J Physiol (Lond) 440:735-769.
25. Douglas RJ, Martin KAC, Whitteridge D (1988) Selective responses of visual cortical neurones do not depend on shunting inhibition. Nature 332:642-644.
26. Douglas RJ, Martin KAC, Whitteridge D (1991a) An intracellular analysis of the visual responses of neurones in cat visual cortex. J Physiol (Lond) 44:659-696.
27. Douglas RJ, Martin KAC, Whitteridge D (1991b) A canonical microcircuit for neocortex. Neural Comput 1:480-488.
28. Einstein G, Davis TL, Sterling P (1987) Pattern of lateral geniculate synapses on neuron somata in layer IV of the cat striate cortex. J Comp Neurol 260:76-86.
29. Enroth-Cugell C, Robson JG, Schweizer-Tong DE, Watson AB (1983) Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. J Physiol (Lond) 341:279-307.
30. Eysel UT, Crook JM, Machemer HF (1990) GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Exp Brain Res 80:626-630.
31. Ferster D (1986) Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci 6:1284-1301.
32. Ferster D (1987) Origin of orientation-selective EPSPs in simple cells of the cat visual cortex. J Neurosci 7:1780-1791.
33. Ferster D (1994) Linearity of synaptic interactions in the assembly of receptive fields in cat visual cortex. Curr Opin Neurobiol 4:563-568.
34. Ferster D, Jagadeesh B (1992) EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J Neurosci 12:1262-1274.
35. Ferster D, Koch C (1987) Neuronal connections underlying orientation selectivity in cat visual cortex. Trends Neurosci 10:487-492.
36. Freund TF, Martin KAC, Somogyi P, Whitteridge D (1985) Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y-type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and golgi impregnation. J Comp Neurol 242:275-291.
37. Gabbott PLA, Somogyi P (1986) Quantitative distribution of GABA-immunoreceptive neurons in the visual cortex (area 17) of the cat. Exp Brain Res 61:323-331.
38. Garey LJ, Powell TPS (1971) An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc R Soc Lond [Biol] 179:41-63.
39. Ghose GM, Freeman RD, Ohzawa I (1994) Local intracortical connections in the cat's visual cortex: postnatal development and plasticity. J Neurophysiol 72:1290-1303.
40. Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116-1133.
41. Grossberg S (1973) Contour enhancement, short-term memory, and constancies in reverberating neural networks. Stud Appl Math 52: 217-257.
42. Grossberg S (1983) The quantized geometry of visual space: the coherent computation of depth, form, and lightness. Behav Brain Sci 6:625-692.
43. Grossberg S, Mingolla E (1987) Neural dynamics of surface perception: boundary webs, illuminants, and shape-from-shading. Comput Vis Graph Image Process 37:116-165.
44. Grossberg S, Olson SJ (1994) Rules for the cortical map of ocular dominance and orientation columns. Neural Networks 7:883-894.
45. 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.
46. Heeger DJ (1992) Normalization of cell responses in cat striate cortex. Vis Neurosci 9:181-197.
47. Heggelund P (1981) Receptive field organization of simple cells in cat striate cortex. Exp Brain Res 42:89-98.
48. Heggelund P (1986) Quantitative studies of the discharge fields of single cells in cat striate cortex. J Physiol (Lond) 373:277-292.
49. Hess R, Murata K (1974) Effects of glutamate and GABA on specific response properties of neurons in the visual cortex. Exp Brain Res 21:285-297.
50. Hestrin S (1992) Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex. Neuron 9:991-999.
51. Hornung JP, Garey LJ (1981) The thalamic projection to the cat visual cortex: ultrastructure of neurons identified by Golgi impregnation or retrograde horseradish peroxidase transport. Neuroscience 6:1053-1068.
52. Horton JC, Sherk H (1984) Receptive field properties in the cat's lateral geniculate nucleus in the absence of on-center retinal input. J Neurosci 4:374-380.
53. Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol (Lond) 165:559-568.
54. Jagadeesh B, Wheat HS, Ferster D (1993) Linearity of summation of synaptic potentials underlying direction selectivity of simple cells of the cat visual cortex. Science 262:1901-1904.
55. Jones JP, Palmer LA (1987) The two-dimensional spatial structure of simple receptive fields in cat striate cortex. J Neurophysiol 58:1187-1211.
56. Kaplan E, Purpura K, Shapley RM (1987) Contrast affects the transmission of visual information through the mammalian lateral geniculate nucleus. J Physiol (Lond) 391:267-288.
57. Kisvàrday ZF, Martin KAC, Whitteridge D, Somogyi P (1985) Synaptic connections of intracellularly filled clutch neurons, a type of small basket neuron in the visual cortex of the cat. J Comp Neurol 241:111-137.
58. Kisvàrday ZF, Beaulieu C, Eysel UT (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327:398-415.
59. Koch C, Poggio T (1985) The synaptic veto mechanism: does it underlie direction and orientation selectivity in the visual cortex? In: Models of the visual cortex (Rose DR, Dobson VG, eds), pp 408-419. New York: Wiley.
60. Koch C, Douglas RJ, Wehmeier U (1990) Visibility of synaptically induced conductance changes: theory and simulations of anatomically characterized cortical pyramidal cells. J Neurosci 10:1728-1744.
61. Kohonen T (1984) Self-organization and associative memory. New York: Springer.
62. Komatsu Y, Nakajima S, Toyama K, Fetz E (1988) Intracortical connectivity revealed by spike-triggered averaging in slice preparations of cat visual cortex. Brain Res 442:359-362.
63. LeVay S (1986) Synaptic organization of claustral and geniculate afferents to the visual cortex of the cat. J Neurosci 6:3564-3575.
64. LeVay S, Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res 113:1-19.
65. Linsenmeier RA, Frishman LJ, Jakiela HG, Enroth-Cugell C (1982) Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Res 22:1173-1183.
66. Malpeli JG (1983) Activity of cells in area 17 of the cat in absence of input from layer A of lateral geniculate nucleus. J Neurophysiol 49: 595-610.
67. Malpeli JG, Lee C, Schwark HD, Weyand TG (1986) Cat area 17. I. Pattern of thalamic control of cortical layers. J Neurophysiol 56: 1062-1073.
68. Marr D, Hildreth E (1980) Theory of edge detection. Proc R Soc Lond [Biol] 207:187-217.
69. Martin KAC (1988) From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol 73:637-702.
70. Mason A, Nicoll A, Stratford K (1991) Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J Neurosci 11:72-84.
71. Matsubara JA, Cynader MS, Swindale NV (1987) Anatomical projections and physiological correlates of the intrinsic connections in cat area 18. J Neurosci 7:1428-1446.
72. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of physiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
73. Michalski A, Gerstein GI, Czarkowska J, Tarnecki R (1983) Interactions between cat striate cortex neurons. Exp Brain Res 51:97-107
74. Miller KD (1992) Development of orientation columns via competition between on- and off-center inputs. Neuroreport 3:73-76.
75. Miller KD (1994) A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between on- and off-center inputs. J Neurosci 14:409-441.
76. Morrone MC, Burr DC, Maffei L (1982) Functional implications of cross-orientation inhibition of visual cortical cells. I. Neurophysiological evidence. Proc R Soc Lond [Biol] 216:335-354.
77. Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol (Lond) 283:53-77.
78. Nelson SB (1991) Temporal interactions in the cat visual system. III. Pharmacological studies of cortical suppression suggest a presynaptic mechanism. J Neurosci 11:369-380.
79. Nelson SB, Smetters DK (1993) Short-term plasticity of minimal synaptic currents in visual cortical neurons. Soc Neurosci Abstr 19:263.7.
80. Nelson SB, Toth LJ, Sheth B, Sur M (1994) Orientation selectivity of cortical neurons persists during intracellular blockade of inhibition. Science 265:774-777.
81. Orban GA (1984) Neuronal operations in the visual cortex. Berlin: Springer.
82. Palmer LA, Davis TL (1981) Receptive-field structure in cat striate cortex. J Neurophysiol 46:260-276.
83. Pei X, Vidyasagar TR, Volgushev M, Creutzfeldt OD (1994) Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. J Neurosci 14:7130-7140.
84. Peichl L, Wässle H (1979) Size, scatter and coverage of ganglion cell receptive field centers in the cat retina. J Physiol (Lond) 291:117-141.
85. Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3:69-78.
86. Peters A, Yilmaz E (1993) Neuronal organization in area 17 of cat visual cortex. Cereb Cortex 3:49-68.
87. Poggio T, Reichardt WE (1976) Visual control of orienting behavior in the fly. II. Towards the underlying neural interactions. Q Rev Biophys 9:377-438.
88. Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1992) Numerical recipes in C: the art of scientific computing, 2d ed, pp 566-597. Cambridge: Cambridge UP.
89. Ramoa AS, Shadlen M, Skottun BC, Freeman RD (1986) A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex. Nature 321:237-239.
90. Reid, RC, Soodak RE, Shapley RM (1987) Linear mechanisms of direction selectivity in simple cells of cat striate cortex. Proc Natl Acad Sci USA 84:8740-8744.
91. Richter J, Ullman S (1982) A model for the temporal organization of X- and Y- type receptive fields in the primate retina. Biol Cybern 43:127-145.
92. Rodieck RW, Stone J (1965) Analysis of receptive fields of cat retinal ganglion cells. J Neurophysiol 28:833-849.
93. Rojer A, Schwartz EL (1990) Cat and monkey cortical columnar patterns modeled by band-pass-filtered 2d white noise. Biol Cybern 62: 381-391.
94. Schiller P (1982) Central connections of the retinal ON and OFF pathways. Nature 297:580-583.
95. Sclar G, Freeman RD (1982) Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast. Exp Brain Res 46:457-461.
96. Shadlen M, Newsome W (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4:569-579.
97. Sherk H, Horton JC (1984) Receptive field properties in the cat's area 17 in the absence of on-center geniculate input. J Neurosci 4:381-393.
98. Shou T, Leventhal AG (1989) Organized arrangement of orientation-selective relay cells in the cat's dorsal lateral geniculate nucleus. J Neurosci 9:4287-4302.
99. Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol (Lond) 250:305-329.
100. Sillito AM (1979) Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J Physiol (Lond) 289:33-53.
101. Sillito AM, Kemp JA, Milson JA, Berardi N (1980) A re-evaluation of the mechanisms underlying simple cell orientation selectivity. Brain Res 194:517-520.
102. Smetters DK, Nelson SB (1993) Estimates of functional synaptic convergence in rat and cat visual cortical neurons. Soc Neurosci Abstr 19:263.6.
103. Softky WR, Koch C (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13:334-450.
104. Somers DC, Nelson SB, Sur M (1993) Computational model of the effects of short-range excitation and inhibition on orientation selectivity in visual cortex. Soc Neurosci Abstr 19:263.5.
105. Somers DC, Nelson SB, Sur M (1994) Effects of long-range connections on gain control in an emergent model of visual cortical orientation selectivity. Soc Neurosci Abstr 20:646.7.
106. Somers DC, Nelson SB, Sur M (1995) An emergent model of visual cortical orientation selectivity. In: Computation and neural systems: 1994 proceedings (Bower JM, ed), in press. Norwell, MA: Kluwer.
107. Soodak RE, Shapley RM, Kaplan E (1987) Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. J Neurophysiol 58:267-275.
108. Suarez H, Koch C, Douglas R (1995) Direction selectivity in primary visual cortex using massive intracortical connections. In: Advances in neural information processing systems, Vol 6, in press. Kauffman.
109. Swindale NV (1992) A model for the coordinated development of columnar systems in primate striate cortex. Biol Cybern 66:217-230.
110. Swindale NV (1993) Contrast integration along the length axis of area 17 neurons: linear or non-linear? Soc Neurosci Abstr 19:263.1.
111. Szentàgothai J (1965) The use of degeneration in the investigation of short neuronal connections. In: Progress in brain research (Singer M, Shade JR, eds), pp 1-32. Amsterdam: Elsevier.
112. Thomson AM, Deuchars J (1994) Temporal and spatial properties of local circuits in neocortex. Trends Neurosci 17:119-126.
113. Tolhurst DJ, Dean AF (1987) Spatial summation by simple cells in the striate cortex of the cat. Exp Brain Res 66:607-620.
114. Tolhurst DJ, Dean AF (1990) The effects of contrast on the linearity of spatial summation of simple cells in the cat's striate cortex. Exp Brain Res 79:582-588.
115. Toyama K, Kimura M, Tanaka K (1981) Organization of cat visual cortex as investigated by cross-correlation technique. J Neurophysiol 46:202-214.
116. Traub RD, Miles R (1991) Neuronal networks of the hippocampus. Cambridge: Cambridge UP.
117. Tsodyks M, Bell A, Mainen ZF, Sejnowski TJ (1994) Why do cortical neurons fire irregularly? Soc Neurosci Abstr 20:627.8.
118. Tsumoto T, Eckart W, Creutzfeldt OD (1979) Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res 34:351-363.
119. Usher M, Stemmler M, Koch C, Olami Z (1994) Network amplification of local fluctuations causes high spike variability, fractal firing patterns, and oscillatory field potentials. Neural Comput 6:795-836.
120. Vidyasagar TR, Urbas JV (1982) Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17, 18. Exp Brain Res 46:157-169.
121. Vogels R, Orban GA (1991) Quantitative study of striate single unit responses in monkeys performing an orientation discrimination task. Exp Brain Res 84:1-11.
122. Volgushev M, Vidyasagar TR, Pei X (1995) Dynamics of the orientation tuning of post-synaptic potentials in the cat visual cortex. Vis Neurosci. in press.
123. Watkins DW, Berkley MA (1974) The orientation selectivity of single neurons in cat striate cortex. Exp Brain Res 19:433-446.
124. Wehmeier U, Dong D, Koch C, Van Essen D (1989) Modeling the visual system. In: Methods in neuronal modeling (Koch C, Segev I, eds), pp 335-359. Cambridge, MA: MIT Press.
125. White EL (1989) Cortical circuits. Boston: Birkhauser.
126. Wilson HR, Cowan JD (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12:1-24.
127. Winfield DA, Powell TPS (1983) Laminar cell counts and geniculocortical boutons in area 17 of cat and monkey. Brain Res 227:223-229.
128. Wörgotter F, Koch C (1991) A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. J Neurosci 11:1959-1979.