Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1

European Journal of Neuroscience

Volumn 28, Issue 3, 2008, Pages 447-459

  Gieselmann, M A ^a   Thiele, A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Contextual influences; Gamma oscillations; Primary visual cortex

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; MACACA; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; RECEPTIVE FIELD; SPATIAL FREQUENCY DISCRIMINATION; SPIKE WAVE; VISUAL CORTEX; VISUAL STIMULATION; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; ELECTROPHYSIOLOGY; HUMANS; MACACA; MALE; MODELS, NEUROLOGICAL; VISUAL CORTEX; VISUAL FIELDS; VISUAL PERCEPTION; WAKEFULNESS;

EID: 47849095933     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06358.x     Document Type: Article

References (93)

1. Allman, J., Miezin, F. McGuinness, E. (1985) Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu. Rev. Neurosci., 8, 407 430.
2. Amitai, Y., Gibson, J.R., Beierlein, M., Patrick, S.L., Ho, A.M., Connors, B.W. Golomb, D. (2002) The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J. Neurosci., 22, 4142 4152.
3. Angelucci, A., Levitt, J.B. Lund, J.S. (2002) Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. Prog. Brain Res., 136, 373 388.
4. Bair, W., Cavanaugh, J.R. Movshon, J.A. (2003) Time course and time-distance relationships for surround suppression in macaque V1 neurons. J. Neurosci., 23, 7690 7701.
5. Barlow, H.B., Blakemore, C. Pettigrew, J.D. (1967) The neural mechanism of binocular depth discrimination. J. Physiol., 193, 327 342.
6. Bauer, R., Brosch, M. Eckhorn, R. (1995) Different rules of spatial summation from beyond the receptive field for spike rates and oscillation amplitudes in cat visual cortex. Brain Res., 669, 291 297.
7. Boynton, G.M., Engel, S.A., Glover, G.H. Heeger, D.J. (1996) Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci., 16, 4207 4221.
8. Bringuier, V., Chavane, F., Glaeser, L. Fregnac, Y. (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science, 283, 695 699.
9. Brunel, N. Wang, X.J. (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance J. Neurophysiol., 90, 415 430.
10. Bush, P.C. Douglas, R.J. (1991) Synchronization of bursting action potential discharge in a model network of neocortical neurons. Neural Comput., 3, 19 30.
11. Buzsaki, G. (2004) Large-scale recording of neuronal ensembles. Nat. Neurosci., 7, 446 451.
12. Buzsaki, G. Draguhn, A. (2004) Neuronal oscillations in cortical networks. Science, 304, 1926 1929.
13. Carandini, M. Heeger, D.J. (1994) Summation and division by neurons in primate visual cortex. Science, 264, 1333 1336.
14. Cavanaugh, J.R., Bair, W. Movshon, J.A. (2002) Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol., 88, 2530 2546.
15. Daniel, P.M. Whitteridge, D. (1961) The representation of the visual field on the cerebral cortex in monkeys. J. Physiol., 159, 203 221.
16. Das, A. Gilbert, C.D. (1995) Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex. Nature, 375, 780 784.
17. DeAngelis, G.C., Ohzawa, I. Freeman, R.D. (1993) Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development. J. Neurophysiol., 69, 1091 1117.
18. DeAngelis, G.C., Freeman, R.D. Ohzawa, I. (1994) Length and width tuning of neurons in the cat's primary visual cortex. J. Neurophysiol., 71, 347 374.
19. Delicato, L.S., Hunter, D., Sun, L. Thiele, A. (2006). Contrast-dependent spatial integration in awake macaque V1 measured by fMRI. Soc. Neurosci. Abstr., 36, 436 438 (E446).
20. Dow, B.M., Snyder, A.Z., Vautin, R.G. Bauer, R. (1981) Magnification factor and receptive field size in foveal striate cortex of the monkey. Exp. Brain Res., 44, 213 228.
21. Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M. Reitboeck, H.J. (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat Biol. Cybern., 60, 121 130.
22. Freiwald, W.A., Kreiter, A.K. Singer, W. (1995) Stimulus dependent intercolumnar synchronization of single unit responses in cat area 17. Neuroreport, 6, 2348 2352.
23. Friedman-Hill, S., Maldonado, P.E. Gray, C.M. (2000) Dynamics of striate cortical activity in the alert macaque: I. incidence and stimulus-dependence of gamma-band neuronal oscillations. Cereb. Cortex, 10, 1105 1116.
24. Frien, A., Eckhorn, R., Bauer, R., Woelbern, T. Gabriel, A. (2000) Fast oscillations display sharper orientation tuning than slower components of the same recordings in striate cortex of the awake monkey. Eur. J. Neurosci., 12, 1453 1465.
25. Fries, P., Reynolds, J.H., Rorie, A.E. Desimone, R. (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science, 291, 1560 1563.
26. Gail, A., Brinksmeyer, H.J. Eckhorn, R. (2004) Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. Cereb. Cortex, 14, 300 313.
27. Galarreta, M. Hestrin, S. (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature, 402, 72 75.
28. Gray, C.M. McCormick, D.A. (1996) Chattering cells: superficial pyramidal neurons contributing to the generation of synchronous oscialltions in the visual cortex. Science, 274, 109 113.
29. Gray, C.M., König, P., Engel, A.K. Singer, W. (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature, 338, 334 337.
30. Grinvald, A., Lieke, E.E., Frostig, R.D. Hildesheim, R. (1994) Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci., 14, 2545 2568.
31. Hammond, P. MacKay, D.M. (1981) Modulatory influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex. J. Physiol., 319, 431 442.
32. Hasenstaub, A., Shu, Y., Haider, B., Kraushaar, U., Duque, A. McCormick, D.A. (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron, 47, 423 435.
33. Henrie, J.A. Shapley, R. (2005) LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol., 94, 479 490.
34. Herculano-Houzel, S., Munk, M.H., Neuenschwander, S. Singer, W. (1999) Precisely synchronized oscillatory firing patterns require electroencephalographic activation. J. Neurosci., 19, 3992 4010.
35. Hestrin, S. Galarreta, M. (2005) Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci., 28, 304 309.
36. Hubel, D.H. Wiesel, T.N. (1968) Receptive fields and functional architecture of monkey striate cortex. J. Physiol., 195, 215 243.
37. Hubel, D.H. Wiesel, T.N. (1974) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol., 158, 267 293.
38. Ichida, J.M., Schwabe, L., Bressloff, P.C. Angelucci, A. (2007) Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. J. Neurophysiol., 98, 2168 2181.
39. Johnson, R.R. Burkhalter, A. (1994) Evidence for excitatory amino acid neurotransmitters in forward and feedback corticocortical pathways within rat visual cortex. Eur. J. Neurosci., 6, 272 286.
40. Jones, M.V. Harrison, N.L. (1993) Effects of volatile anesthetics on the kinetics of inhibitory postsynaptic currents in cultured rat hippocampal neurons. J. Neurophysiol., 70, 1339 1349.
41. Jones, H.E., Grieve, K.L., Wang, W. Sillito, A.M. (2001) Surround suppression in primate V1. J. Neurophysiol., 86, 2011 2028.
42. Kapadia, M.K., Westheimer, G. Gilbert, C.D. (2000) Spatial distribution of contextual interactions in primary visual cortex and in visual perception. J. Neurophysiol., 84, 2048 2062.
43. Kayser, C. Konig, P. (2004) Stimulus locking and feature selectivity prevail in complementary frequency ranges of V1 local field potentials. Eur. J. Neurosci., 19, 485 489.
44. Kayser, C., Kim, M., Ugurbil, K., Kim, D.S. Konig, P. (2004) A comparison of hemodynamic and neural responses in cat visual cortex using complex stimuli. Cereb. Cortex, 14, 881 891.
45. Kreiman, G., Hung, C.P., Kraskov, A., Quiroga, R.Q., Poggio, T. DiCarlo, J.J. (2006) Object selectivity of local field potentials and spikes in the macaque inferior temporal cortex. Neuron, 49, 433 445.
46. Kreiter, A.K. Singer, W. (1996) Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci., 16, 2381 2396.
47. Kruse, W. Eckhorn, R. (1996) Inhibition of sustained gamma oscillations (35-80 Hz) by fast transient responses in cat visual cortex. Proc. Natl Acad. Sci. USA, 93, 6112 6117.
48. Levitt, J.B. Lund, J.S. (2002) The spatial extent over which neurons in macaque striate cortex pool visual signals. Vis. Neurosci., 19, 439 452.
49. Li, C.Y. Li, W. (1994) Extensive integration field beyond the classical receptive field of cat's striate cortical neurons-classification and tuning properties. Vision Res., 34, 2337 2355.
50. Liu, J. Newsome, W.T. (2006) Local field potential in cortical area, MT: stimulus tuning and behavioral correlations. J. Neurosci., 26, 7779 7790.
51. Logothetis, N.K. (2002) The neural basis of the blood-oxygen-level- dependent functional magnetic resonance imaging signal. Philos. Trans. R Soc. Lond. B Biol. Sci., 357, 1003 1037.
52. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. Oeltermann, A. (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150 157.
53. Maffei, L. Fiorentini, A. (1976) The unresponsive regions of visual cortical receptive fields. Vision Res., 16, 1131 1139.
54. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G. Wu, C. (2004) Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci., 5, 793 807.
55. McGurie, B.A., Gilbert, C.D., Rivlin, P.K. Wiesel, T.N. (1991) Targets of horizontal connections in Macaque primary visual cortex. J. Comp. Neurol., 305, 370 392.
56. Miller, R. (2007) Theory of the normal waking EEG: from single neurones to waveforms in the alpha, beta and gamma frequency ranges. Int. J. Psychophysiol., 64, 18 23.
57. Mitzdorf, U. (1987) Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. Int. J. Neurosci., 33, 33 59.
58. Mody, I., Tanelian, D.L. MacIver, M.B. (1991) Halothane enhances tonic neuronal inhibition by elevating intracellular calcium. Brain Res., 538, 319 323.
59. Mukamel, R., Gelbard, H., Arieli, A., Hasson, U., Fried, I. Malach, R. (2005) Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science, 309, 951 954.
60. Nelson, J.I. Frost, B.J. (1978) Orientation selective inhibition from beyond the classic visual receptive field. Brain Res., 139, 359 365.
61. Niessing, J., Ebisch, B., Schmidt, K.E., Niessing, M., Singer, W. Galuske, R.A. (2005) Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science, 309, 948 951.
62. Nir, Y., Fisch, L., Mukamel, R., Gelbard-Sagiv, H., Arieli, A., Fried, I. Malach, R. (2007) Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol., 17, 1275 1285.
63. de Oliveira, S.C., Thiele, A. Hoffmann, K.P. (1997) Synchronization of neuronal activity during stimulus expectation in a direction discrimination task. J. Neurosci., 17, 9248 9260.
64. Palanca, B.J. DeAngelis, G.C. (2005) Does neuronal synchrony underlie visual feature grouping? Neuron, 46, 333 346.
65. Pesaran, B., Pezaris, J.S., Sahani, M., Mitra, P.P. Andersen, R.A. (2002) Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat. Neurosci., 5, 805 811.
66. Raiguel, S., Van Hulle, M.M., Xiao, D.K., Marcar, V.L. Orban, G.A. (1995) Shape and spatial distribution of receptive fields and antagonistic motion surrounds in the middle temporal area (V5) of the macaque. Eur. J. Neurosci., 7, 2064 2082.
67. Rees, G., Friston, K. Koch, C. (2000) A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci., 3, 716 723.
68. Ringach, D. Shapley, R. (2004) Reverse correlation in neurophysiology. Cogn. Sci., 28, 147 166.
69. Roberts, M.J., Zinke, W., Guo, K., Robertson, R., McDonald, J.S. Thiele, A. (2005) Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol., 93, 2062 2072.
70. Roberts, M., Delicato, L.S., Herrero, J., Gieselmann, M.A. Thiele, A. (2007) Attention alters spatial integration in macaque V1 in an eccentricity-dependent manner. Nat. Neurosci., 10, 1483 1491.
71. Roelfsema, P.R., Lamme, V.A. Spekreijse, H. (2004) Synchrony and covariation of firing rates in the primary visual cortex during contour grouping. Nat. Neurosci., 7, 982 991.
72. Sceniak, M.P., Ringach, D.L., Hawken, M.J. Shapley, R. (1999) Contrast's effect on spatial summation by macaque V1 neurons. Nat. Neurosci., 2, 733 739.
73. Sceniak, M.P., Hawken, M.J. Shapley, R. (2001) Visual spatial characterization of macaque V1 neurons. J. Neurophysiol., 85, 1873 1887.
74. Scherberger, H., Jarvis, M.R. Andersen, R.A. (2005) Cortical local field potential encodes movement intentions in the posterior parietal cortex. Neuron, 46, 347 354.
75. Shao, Z. Burkhalter, A. (1996) Different balance of excitation and inhibition in forward and feedback circuits of rat visual cortex. J. Neurosci., 16, 7353 7365.
76. Shao, Z. Burkhalter, A. (1999) Role of GABAB receptor-mediated inhibition in reciprocal interareal pathways of rat visual cortex. J. Neurophysiol., 81, 1014 1024.
77. Singer, W. (1999) Neuronal synchrony: a versatile code for the definition of relations. Neuron, 24, 49 65.
78. Swindale, N.V. (1991) Coverage and the design of striate cortex. Biol. Cybern., 65, 415 424.
79. Tamas, G., Buhl, E.H., Lorincz, A. Somogyi, P. (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci., 3, 366 371.
80. Thiele, A. Stoner, G. (2003) Neuronal synchrony does not correlate with motion coherence in cortical area MT. Nature, 421, 366 370.
81. Thiele, A., Delicato, L.S., Roberts, M.J. Gieselmann, M.A. (2006) A novel electrode-pipette design for simultaneous recording of extracellular spikes and iontophoretic drug application in awake behaving monkeys. J. Neurosci. Methods, 158, 207 211.
82. Tiesinga, P.H. Sejnowski, T.J. (2004) Rapid temporal modulation of synchrony by competition in cortical interneuron networks. Neural Comput., 16, 251 275.
83. Tootell, R.B., Switkes, E., Silverman, M.S. Hamilton, S.L. (1988) Functional anatomy of macaque striate cortex. II. Retinotopic organization. J. Neurosci., 8, 1531 1568.
84. Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G. Jefferys, J.G. (1996a). Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493 (Pt. 2 471 484.
85. Traub, R.D., Whittington, M.A., Stanford, I.M. Jefferys, J.G.R. (1996b) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature, 383, 621 624.
86. Wang, X.J. Buzsaki, G. (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci., 16, 6402 6413.
87. Whittington, M.A. Traub, R.D. (2003) Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci., 26, 676 682.
88. Wilke, M., Logothetis, N.K. Leopold, D.A. (2006) Local field potential reflects perceptual suppression in monkey visual cortex. Proc. Natl Acad. Sci. USA, 103, 17507 17512.
89. Williams, A.L., Singh, K.D. Smith, A.T. (2003) Surround modulation measured with functional MRI in the human visual cortex. J. Neurophysiol., 89, 525 533.
90. Wilson, J.R. Sherman, S.M. (1976) Receptive-field characteristics of neurons in cat striate cortex: changes with visual field eccentricity. J. Neurophysiol., 39, 512 533.
91. Woelbern, T., Frien, A., Eckhorn, R., Bauer, R. Kehr, H. (1994) Distribution of oscillation frequencies depend on stimulus size and velocity in monkey visual cortex. In Elsner, N. Breer, H. (Eds Sensory Transduction. Thieme, New York, p. 337.
92. Womelsdorf, T., Fries, P., Mitra, P.P. Desimone, R. (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature, 439, 733 736.
93. Zenger-Landolt, B. Heeger, D.J. (2003) Response suppression in V1 agrees with psychophysics of surround masking. J. Neurosci., 23, 6884 6893.