Synaptic physiology of the flow of information in the cat's visual cortex in vivo

Journal of Physiology

Volumn 540, Issue 1, 2002, Pages 335-350

  Hirsch, Judith A ^a,d   Martinez, Luis M ^b   Alonso, José Manuel ^c   Desai, Komal ^a   Pillai, Cinthi ^a   Pierre, Carhine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF A CORUÑA   (Spain)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL TYPE; CONTROLLED STUDY; ELECTRODE; EVOKED VISUAL RESPONSE; LATENT PERIOD; MOTION; NERVE CELL NETWORK; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RECEPTIVE FIELD; RESPONSE TIME; SENSORY NERVE; SPIKE; STAGING; STRIATE CORTEX; SYNAPSE; THALAMUS; VISION; VISUAL CORTEX; VISUAL STIMULATION; ADULT; ANIMAL CELL; BRAIN CELL; CAT; CONNECTOME; CORTEX LAYER IV; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; IN VIVO STUDY; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; VISUAL INFORMATION;

ACTION POTENTIALS; ANIMALS; CATS; CELL SIZE; DENDRITES; NEURONS; PHOTIC STIMULATION; SYNAPSES; THALAMUS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 0036554721     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2001.012777     Document Type: Article

References (109)

1. AHMED, B., ANDERSON, J. C., DOUGLAS, R. J., MARTIN, K. A. & NELSON, J. C. (1994). Polyneuronal innervation of spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 39-49.
2. ALLEN, C. & STEVENS, C. F. (1994). An evaluation of causes of unreliability of synaptic transmission. Proceedings of the National Academy of Sciences of the USA 9, 10380-10383.
3. ALONSO, J. M. & MARTINEZ, L. M. (1998). Functional connectivity between simple cells and complex cells in cat striate cortex. Nature Neuroscience 5, 395-403.
4. BERNANDER, O., DOUGLAS, R. J., MARTIN, K. A. & KOCH, C. (1991). Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proceedings of the National Academy of Sciences of the USA 88, 11569-11573.
5. BLANTON, M., LO TURCO, J. J. & KRIEGSTEIN, A. R. (1989). Wholecell recording from neurons in slices of reptilian and mammalian cerebral cortex. Journal of Neuroscience Methods 30, 203-210.
6. BORG-GRAHAM, L. J., MONIER, C. & FREGNAC, Y. (1998). Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393, 369-373.
7. BRUMBERG, J. C., PINTO, D. J. & SIMONS, D. J. (1999). Cortical columnar processing in the rat whisker-to-barrel system. Journal of Neurophysiology 82,1808-1817.
8. BULLIER, J. & HENRY, G. H. (1979a). Ordinal position of neurons in cat striate cortex. Journal of Neurophysiology 42, 1251-1263.
9. BULLIER, J. & HENRY, G. H. (1979b). Laminar distribution of first-order neurons and afferent terminals in cat striate cortex. Journal of Neurophysiology 42, 1271-1281.
10. CALLAWAY, E. M. (1998). Local circuits in primary visual cortex of the macaque monkey. Annual Review of Neuroscience 21, 47-74.
11. CHUNG, S. & FERSTER, D. (1998). Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177-1189.
12. DAVIS, T. L. & STERLING, P. (1979). Microcircuitry of cat visual cortex: Classification of neurons in layer iv of area 17, and identification of the patterns of lateral geniculate input. Journal of Comparative Neurology 188, 599-627.
13. DE ANGELIS, G. C., OHZAWA, I. & FREEMAN, R. D. (1995). Receptive field dynamics in central visual pathways. Trends in Neurosciences 18, 451-458.
14. DESTEXHE, A. & PARE, D. (1999). Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. Journal of Neurophysiology 81, 1531-1547.
15. DOBRUNZ, L. E. & STEVENS, C. F. (1997). Heterogeneity of release probability, facillitation, and depletion at central synapses. Neuron 18, 995-1008.
16. DOUGLAS, R. J., MARTIN, K. A. & WHITTERIDGE, D. (1991). An intracellular analysis of the visual responses of neurones in cat visual cortex. Journal of Physiology 440, 659-696.
17. EDWARDS, F. A. & KONNERTH, A. R. (1992). Patch-clamping cells in sliced-tissue preparations. Methods in Enzymology 207, 208-222.
18. EGGER, V., FELDMEYER, D. & SAKMANN, B. (1999). Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nature Neuroscience 2, 1098-1105.
19. EMERSON, R. C., CITRON, M. C., VAUGHN, W. J. & KLEIN, S. A. (1987). Nonlinear directionally selective subunits in complex cells of cat striate cortex. Journal of Neurophysiology 58, 33-65.
20. FAIRÉN, A., DEFELIPE, J. & REGIDOR, J. (1983). Nonpyramidal neurons: General account. In Cerebral Cortex: Cellular Components of the Cerebral Cortex, ed. PETERS, A. & JONES, E. G., pp. 201-253. Plenum Press, New York.
21. FARIÑAS, I. & DEFELIPE, J. (1991a). Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The cell body. Journal of Comparative Neurology 304, 53-69.
22. FARIÑAS, I. & DEFELIPE, J. (1991b). Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The axon initial segment. Journal of Comparative Neurology 304, 70-77.
23. FATT A. & KATZ, B. (1951). An analysis of the endplate potential recorded with an intracellular electrode. Journal of Physiology 115, 320-370.
24. FELDMEYER, D., EGGER, V., LUBKE, J. & SAKMANN, B. (1999). Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. Journal of Physiology 521, 169-190.
25. FERSTER, D. (1988). Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. Journal of Neuroscience 8, 1172-1180.
26. FERSTER, D. & JAGADEESH, B. (1992). EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. Journal of Neuroscience 12, 1262-1274.
27. FERSTER, D. & LINDSTRÖM, S. (1983). An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. Journal of Physiology 342, 181-215.
28. FERSTER, D. & LINDSTRÖM, S. (1985). Synaptic excitation of neurones in area 17 of the cat by intracortical axon collaterals of cortico-geniculate cells. Journal of Physiology 367, 233-252.
29. FITZPATRICK, D. (1996). The functional organization of local circuits in visual cortex: Insights from the study of tree shrew striate cortex. Cerebral Cortex 6, 329-341.
30. GHOSE, G. M., FREEMAN, R. D. & OHZAWA, I. (1994). Local intracortical connections in the cat's visual cortex: Postnatal development and plasticity. Journal of Neurophysiology 72, 1290-1303.
31. GIL, Z., CONNORS, B. W. & AMITAI, Y. (1999). Efficacy of thalamocortical and intracortical synaptic connections: Quanta, innervation, and reliability. Neuron 23, 385-397.
32. GILBERT, C. D. (1977). Laminar differences in receptive field properties of cells in cat primary visual cortex. Journal of Physiology 268, 391-421.
33. GILBERT, C. D. & KELLY, J. P. (1975). The projections of cells in different layers of the cat's visual cortex. Journal of Comparative Neurology 163, 81-105.
34. GILBERT, C. D. & WIESEL, T. N. (1979). Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120-125.
35. GILBERT, C. D. & WIFSEL, T. N. (1981). Laminar specialization and intracortical connections in cat primary visual cortex. In The Organization of the Cerebral Cortex, ed. SCHMITT, F. O., WORDEN, F. G., ADELMAN, G. & DENNIS, S. G., pp. 164-190. MIT Press, Cambridge, MA, USA.
36. GOLDING, N. L. & SPRUSTON, N. (1998). Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal ca1 pyramidal neurons. Neuron 21, 1189-1200.
37. GRIEVE, K. L. & SILLITO, A. M. (1995). Non-length-tuned cells in layers II/III and IV of the visual cortex: The effect of blockade of layer VI on responses to stimuli of different lengths. Experimental Brain Research 104, 12-20.
38. HEGGELUND, P. (1986). Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. Journal of Physiology 373, 293-310.
39. HENRY, G. H. (1977). Receptive field classes of cells in the striate cortex of the cat. Brain Research 133, 1-28.
40. HIRSCH, J. A. (1995). Synaptic integration in layer IV of the ferret striate cortex. Journal of Physiology 483, 183-199.
41. HIRSCH, J. A., ALONSO, J. M. & REID, R. C. (1995). Visually evoked calcium action potentials in cat striate cortex. Nature 378, 612-616.
42. HIRSCH, J. A., ALONSO, J. M., REID, C. R. & MARTINEZ, L. M. (1997). Different synaptic responses of first and second order complex cells in cat striate cortex. Society for Neuroscience Abstracts 23, 1668.
43. HIRSCH, J. A., ALONSO, J. M. & MARTINEZ, L. M. (1998a). The receptive field structure of inhibitory complex cells mirrors that of excitatory complex cells. Society for Neuroscience Abstracts, 24, 766.
44. HIRSCH, J. A., ALONSO, J. M., REID, R. C. & MARTINEZ, L. M. (1998b). Synaptic integration in striate cortical simple cells. Journal of Neuroscience 18, 9517-9528.
45. HIRSCH, J. A., GALLAGHER, C. A., ALONSO, J. M. & MARTINEZ, L. M. (1998c). Ascending projections of simple and complex cells in layer 6 of the cat striate cortex. Journal of Neuroscience 18, 8086-8094.
46. HIRSCH, J. A. & GILBERT, C. D. (1991). Synaptic physiology of horizontal connections in the cat's visual cortex. Journal of Neuroscience 11, 1800-1809.
47. HIRSCH, J. A. & GILBERT, C. D. (1993). Long-term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. Journal of Physiology 461, 247-262.
48. HIRSCH, J. A., MARTINEZ, L. M., ALONSO, J. M., PILLAI, C. & PIERRE, C. (2000). Simple and complex inhibitory cells in layer 4 of the cat visual cortex. Society for Neuroscience Abstracts 26, 1083.
49. HOFFMAN, K. P. & STONE, J. (1971). Conduction velocity of afferents to cat visual cortex., A correlation with cortical receptive field properties. Brain Research 32, 460-466.
50. HORIKAWA, K. & ARMSTRONG, W. E. (1988). A versatile means of labeling: Injection of biocytin and its detection with avidin conjugates. Journal of Neuroscience Methods 25, 1-11.
51. HUBEL, D. H. & WIESEL, T. N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106-154.
52. HUMPHREY, A. L., SUR, M., UHLRICH, D. J. & SHERMAN, S. M. (1985). Projection patterns of individual x-and y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat. Journal of Comparative Neurology 233, 159-189.
53. JOHNSON, R. R. & BURKHALTER, A. (1996). Microcircuitry of forward and feedback connections within rat visual cortex. Journal of Comparative Anatomy 368, 383-398.
54. JONES, J. P. & PALMER, L. A. (1987). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1187-1211.
55. JORIS, P. X., SMITH, P. H. & YIN, T. C. (1998). Coincidence detection in the auditory system: 50 years after Jeffress. Neuron 21, 1235-1238.
56. KIM, H. G. & CONNORS, B. W. (1993). Apical dendrites of the neocortex: Correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. Journal of Neuroscience 13, 5301-5311.
57. LAUGHLIN, S. B., DE RUYTER VAN STEVENINCK, R. R. & ANDERSON, J. C. (1998). The metabolic cost of neural information. Nature Neuroscience 1, 36-41.
58. LEVAY, S. (1973). Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of golgi preparations. Journal of Comparative Neurology 150, 53-85.
59. LEVAY, S. & GILBERT, C. D. (1976). Laminar patterns of geniculocortical projection in the cat. Brain Research 113, 1-19.
60. LORENTE DE NÒ, R. (1944). Architecture, intracortical connections, motor projections. In Physiology of the Nervous System, ed. FULTON, J. F., pp. 291-325. Oxford University Press, London.
61. LUND, J. S., HENRY, G. H., MACQUEEN, C. L. & HARVEY, A. R. (1979). Anatomical organization of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the macaque monkey. Journal of Comparative Neurology 184, 599-618.
62. MCGUIRE, B. A., GILBERT, C. D., RIVLIN, P. K. & WIESEL, T. N. (1991). Targets of horizontal connections in macaque primary visual cortex. Journal of Comparative Neurology 305, 370-392.
63. MCGUIRE, B. A., HORNUNG, J. P., GILBERT, C. D. & WIESEL, T. N. (1984). Patterns of synaptic input to layer 4 of cat striate cortex. Journal of Neuroscience 4, 3021-3033.
64. MAGEE, J. C. (1999). Dendritic Ih normalizes temporal summation in hippocampal cal neurons. Nature Neuroscience, 2, 508-514.
65. MALINOW, R. & TSIEN, R. W. (1990). Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180.
66. MARTIN, K. A. & WHITTERIDGE, D. (1984). Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. Journal of Physiology 353, 463-504.
67. MARTINEZ, L. M., REID, R. C., ALONSO, J. M. & HIRSCH, J. A. (1999). The synaptic structure of the simple receptive field. Society for Neuroscience Abstracts 25, 1048.
68. MARTINEZ, L. M., ALONSO, J. M., REID, R. C. & HIRSCH, J. A. (2002). Laminar processing of stimulus orientation in cat visual cortex. Journal of Physiology 340, 321-333.
69. MOORE, C. I. & NELSON, S. B. (1998). Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. Journal of Neurophysiology 80, 2882-2892.
70. MOVSHON, J. A., THOMPSON, I. D. & TOLHURST, D. J. (1978a). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 53-77.
71. MOVSHON, J. A., THOMPSON, I. D. & TOLHURST, D. J. (1978b). Receptive field organization of complex cells in the cat's striate cortex. Journal of Physiology 283, 79-99.
72. MULLIKIN, W. H., JONES, J. P. & PALMER, L. A. (1984). Receptive-field properties and laminar distribution of x-like and y-like simple cells in cat area 17. Journal of Neurophysiology 52, 350-371.
73. OHZAWA, I. & FREEMAN, R. D. (1997). Spatial pooling of subunits in complex cell receptive fields. Society for Neuroscience Abstracts 23, 1669.
74. PALMER, L. A. & DAVIS, T. L. (1981a). Receptive-field structure in cat striate cortex. Journal of Neurophysiology 46, 260-276.
75. PALMER, L. A. & DAVIS, T. L. (1981b). Comparison of responses to moving and stationary stimuli in cat striate cortex. Journal of Neurophysiology 46, 277-295.
76. PARE, D., LANG, E. J. & DESTEXHE, A. (1998a). Inhibitory control if somatic and dendritic sodium spikes in neocortical pyramidal neurons in vivo:An intracellular study. Neuroscience 84, 377-402.
77. PARE, D., SHINK, E., GAUDREAU, H., DESTEXHE, A. & LANG, E. J. (1998b). Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. Journal of Neurophysiology 79, 1450-1460.
78. PEI, X., VOLGUSHEV, M., VIDYASAGAR, T. R. & CREUTZFELDT, O. D. (1991). Whole cell recording and conductance measurements in cat visual cortex in-vivo. NeuroReport 2,485-488.
79. PETERS, A. & PAYNE, B. R. (1993). Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cerebral Cortex 3, 69-78.
80. RALL, W. (1977). Core conductor theory and cable properties of neurons., in Handbook of Physiology, The Nervous System: Cellular Biology of Neurons, pp. 39-97. American Physiological Society, Bethesda.
81. REGEHR, W., KEHOE, J., ASCHER, P. & ARMSTRONG, C. (1993). Synaptically triggered action potentials in dendrites. Neuron, 11, 145-151.
82. REID, R. C. & ALONSO, J. M. (1996). The processing and encoding of information in the visual cortex. Current Opinion in Neurobiology 6, 475-480.
83. REYES, A., LUJAN, R., ROZOV, A., BURNASHEV, N., SOMOGYI, P. & SAKMANN, B. (1998). Target-cell-specific facilitation and depression in neocortical circuits. Nature Neuroscience 1, 279-285.
84. RINGACH, D. L., HAWKEN, M. J. & SHAPLEY, R. (1997). Dynamics of orientation tuning in macaque primary visual cortex. Nature 387, 281-284.
85. SAKITT, B. & BARLOW, H. B. (1982). A model for the economical encoding of the visual image in cerebral cortex. Biological Cybernetics 43, 97-108.
86. SCHILLER, J., SCHILLER, Y., STUART, G. & SAKMANN, B. (1997). Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. Journal of Physiology, 505 605-616.
87. SHAO, Z. & BURKHALTER, A. (1996). Different balance of excitation and inhibition in forward and feedback circuits of rat visual cortex. Journal of Neuroscience 16, 3009-3018.
88. SKOTTUN, B. C., DE VALOIS, R. L., GROSOF, D. H., MOVSHON, J. A., ALBRECHT, D. G. & BONDS, A. B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 1079-1086.
89. SPENCER, W. A. & KANDEL, E. R. (1961). Electrophysiology of hippocampal neurons. IV. Fast prepotentials. Journal of Neurophysiology 24, 272-285.
90. STAFSTROM, C. E., SCHWINDT, P. C., CHUBB, M. C. & CRILL, W. E. (1985). Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. Journal of Neurophysiology 53, 153-170.
91. STERN, P., EDWARDS, F. A. & SAKMANN, B. (1992). Fast and slow components of unitary epscs on stellate cells elicited by focal stimulation in slice of the rat visual cortex. Journal of Physiology 449, 247-278.
92. STRATFORD, K. J., TARCZY-HORNOCH, K., MARTIN, K. A., BANNISTER, N. J. & JACK, J. J. (1996). Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature, 382, 258-261.
93. STÜHMER, A., ROBERTS, M. & ALMERS, W. (1983). The loose patch clamp. In Single Channel Recording, ed. SAKMANN, B. & NEHER, E., pp. 123-132. Plenum, New York.
94. SVOBODA, K., HELMCHEN, F., DENK, W. & TANK, D. W. (1999). Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nature Neuroscience 2, 65-73.
95. SZULBORSKI, R. G. & PALMER, L. A. (1990). The two-dimensional spatial structure of nonlinear subunits in the receptive fields of complex cells. Vision Research 30, 249-254.
96. TANAKA, K. (1983). Cross-correlation analysis of geniculostriate neuronal relationships in cats. Journal of Neurophysiology 49, 1303-1318.
97. TANAKA, K. (1985). Organization of geniculate inputs to visual cortical cells in the cat. Vision Research 25, 357-364.
98. TANK, D. W., REGEHR, W. G. & DELANEY, K. R. (1995). A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. Journal of Neuroscience 15, 7940-7952.
99. THOMSON, A. M. & WEST, D. C. (1993). Fluctuation in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex. Neuroscience 54, 329-346.
100. THOMSON, A. M. (1997). Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. Journal of Physiology 502, 131-147.
101. THOMSON, A. M. & DEUCHARS, J. (1997). Synaptic interactions in neocortical local circuits: Dual intracellular recordings in vitro. Cerebral Cortex 7, 510-522.
102. TOLHURST, D. J. & DEAN, A. F. (1987). Spatial summation by simple cells in the striate cortex of the cat. Experimental Brain Research 66, 607-620.
103. TOYAMA, K. (1988). Functional connection of the visual cortex studied by cross-correlation techniques. In Neurobiology of Neocortex, ed. RAKIC, P. & SINGER, W., pp. 203-217. John Wiley & Sons, New York.
104. TSODYKS, M. V. & MARKRAM, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proceedings of the National Academy of Sciences of the USA 94, 719-723.
105. VARELA, J. A., SEN, K., GIBSON, J., FOST, J., ABBOTT, L. F. & NELSON, S. B. (1997). A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. Journal of Neuroscience 17, 7926-7940.
106. VINJE, W. E. & GALLANT, J. L. (2000). Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287, 1273-1276.
107. WOLFE, J. & PALMER, L. A. (1998). Temporal diversity in the lateral geniculate nucleus of cat. Visual Neuroscience 15, 653-675.
108. YUSTE, R. & TANK, D. W. (1996). Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16, 701-716.
109. ZHU, J. J. & CONNORS, B. W. (1999). Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. Journal of Neurophysiology 81, 1171-1183.