Orientation and direction selectivity of synaptic inputs in visual cortical neurons: A diversity of combinations produces spike tuning

Neuron

Volumn 37, Issue 4, 2003, Pages 663-680

  Monier, Cyril ^a   Chavane, Frédéric ^a   Baudot, Pierre ^a   Graham, Lyle J ^a   Frégnac, Yves ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; DEPOLARIZATION; EVOKED VISUAL RESPONSE; HYPERPOLARIZATION; NERVE CELL MEMBRANE CONDUCTANCE; NERVE POTENTIAL; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; SYNAPSE; SYNAPTIC INHIBITION; VISUAL CORTEX;

EID: 0037456572     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(03)00064-3     Document Type: Article

References (69)

1. Adorjan P., Levitt J.B., Lund J.S., Obermayer K. A model for the intracortical origin of orientation preference and tuning in macaque striate cortex. Vis. Neurosci. 16:1999;303-318.
2. Ahmed B., Anderson J.C., Douglas R.J., Martin K.A.C., Nelson J.C. Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J. Comp. Neurol. 341:1994;39-49.
3. Anderson J., Lampl I., Reichova I., Carandini M., Ferster D. Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat. Neurosci. 3:2000;617-621. a.
4. Anderson J.S., Carandini M., Ferster D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84:2000;909-926. b.
5. Anderson J.S., Lampl I., Gillespie D.C., Ferster D. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science. 290:2000;1968-1972. c.
6. Ben-Yishai R., Bar-Or R.L., Sompolinsky H. Theory of orientation tuning in visual cortex. Proc. Natl. Acad. Sci. USA. 92:1995;3844-3848.
7. Benevento L.A., Creutzfeldt O.D., Kuhnt U. Significance of intracortical inhibition in the visual cortex. Nature. 238:1972;124-126.
8. Berman N.J., Douglas R.J., Martin K.A.C., Whitteridge D. Mechanisms of inhibition in cat visual cortex. J. Physiol. 440:1991;697-722.
9. Bishop P.O., Coombs J.S., Henry G.H. Receptive fields of simple cells in the cat striate cortex. J. Physiol. 231:1973;31-60.
10. Bonhoeffer T., Kim D.-S., Malonek D., Shoham D., Grinvald A. Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. Eur. J. Neurosci. 7:1995;1973-1988.
11. Borg-Graham L.J. The computation of directional selectivity in the retina occurs prior to the ganglion cell. Nat. Neurosci. 4:2001;176-182.
12. Borg-Graham L., Monier C., Frégnac Y. Voltage-clamp measurement of visually evoked conductances with whole-cell patch recordings in primary visual cortex. J. Physiol. (Paris). 90:1996;185-188.
13. Borg-Graham L.J., Monier C., Frégnac Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature. 393:1998;369-373.
14. Bringuier V., Frégnac Y., Baranyi A., Debanne D., Shulz D. Synaptic origin and stimulus dependency of neuronal oscillatory activity in the primary visual cortex of the cat. J. Physiol. 500:1997;751-774.
15. Bringuier V., Chavane F., Glaeser L., Frégnac Y. Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science. 283:1999;695-699.
16. Bush P.C., Sejnowski T.J. Effects of inhibition and dendritic saturation in simulated neocortical pyramidal cells. J. Neurophysiol. 71:1994;2183-2193.
17. Buzas P., Eysel U.T., Adorjan P., Kisvarday Z.F. Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps. J. Comp. Neurol. 437:2001;259-285.
18. Carandini M., Ferster D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20:2000;470-484.
19. Creutzfeldt O.D., Kuhnt V., Benevento L.A. An intracellular analysis of visual cortical neurons to moving stimuli. responses in a co-operative neuronal network Exp. Brain Res. 21:1974;251-274.
20. Crook J.M., Kisvarday Z.F., Eysel U.T. GABA-induced inactivation of functionally characterized sites in cat striate cortex. effects of orientation tuning and direction selectivity Vis. Neurosci. 14:1997;141-158.
21. Crook J.M., Kisvarday Z.F., Eysel U.T. 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 Eur. J. Neurosci. 10:1998;2056-2075.
22. Das A., Gilbert C.D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature. 399:1999;655-661.
23. Dean A.F. The variability of discharge of simple cells in the cat striate cortex. Exp. Brain Res. 44:1981;437-440.
24. DeAngelis G.C., Robson J.G., Ohzawa I., Freeman R.D. Organization of suppression in receptive fields of neurons in cat visual cortex. J. Neurophysiol. 68:1992;144-163.
25. Douglas R.J., Martin K.A.C., Whitteridge D. Selective responses of visual cortical cells do not depend on shunting inhibition. Nature. 332:1988;642-644.
26. Douglas R.J., Martin K.A.C., Whitteridge D. An intracellular analysis of the visual responses of neurones in cat visual cortex. J. Physiol. 440:1991;659-696.
27. Douglas R.J., Koch C., Mahowald M.A., Martin K.A.C., Suarez H.H. Recurrent excitation in neocortical circuits. Science. 269:1995;981-985.
28. Douglas R., Koch C., Mahowald M., Martin K. The role of recurrent excitation in neocortical circuits. Ulinsky P.S., Jones E.G., Peters A. Cerebral Cortex. Models of Cortical Circuits:1999;Kluwer Academic: Plenum Publishers, New York. 251-282.pp.
29. Dragoi V., Rivadulla C., Sur M. Foci of orientation plasticity in visual cortex. Nature. 411:2001;80-86.
30. Eysel U.T., Shevelev I.A. Time-slice analysis of inhibition in cat striate cortical neurones. Neuroreport. 5:1994;2033-2036.
31. Eysel U.T., Crook J.M., Machemer H.F. GABA-induced remote activation reveals cross-orientation inhibition in the cat striate cortex. Exp. Brain Res. 80:1990;626-630.
32. Ferster D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J. Neurosci. 6:1986;1284-1301.
33. Ferster D., Jagadeesh B. EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J. Neurosci. 12:1992;1262-1274.
34. Ferster D., Koch C. Neuronal connections underlying orientation selectivity in cat visual cortex. Trends Neurosci. 10:1987;487-492.
35. Ferster D., Miller K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23:2000;441-472.
36. nd edition:2002;MIT Press, Boston, MA. 512-522.pp.
37. Heggelund P., Albus K. Response variability and orientation descrimination of single cells in striate cortex of cat. Expl. Brain Res. 32:1978;197-211.
38. Hirsch J.A., Alonso J.M., Reid R.C., Martinez L.M. Synaptic integration in striate cortical simple cells. J. Neurosci. 18:1998;9517-9528.
39. Hubel D.H., Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160:1962;106-154.
40. Innocenti G.M., Fiore L. Post-synaptic inhibitory components of the responses to moving stimuli in area 17. Brain Res. 80:1974;122-126.
41. Kisvarday Z.F., Kim D.S., Eysel U.T., Bonhoeffer T. Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex. Eur. J. Neurosci. 6:1994;1619-1632.
42. Kisvarday Z.F., Buzas P., Eysel U.T. Calculating direction maps from intrinsic signals revealed by optical imaging. Cereb. Cortex. 11:2001;636-647.
43. Maldonado P.E., Godecke I., Gray C.M., Bonhoeffer T. Orientation selectivity in pinwheel centers in cat striate cortex. Science. 276:1997;1551-1555.
44. Martinez L.M., Alonso J.M., Reid R.C., Hirsch J.A. Laminar processing of stimulus orientation in cat visual cortex. J. Physiol. 540:2002;321-333.
45. McLaughlin D., Shapley R., Shelley M., Wielaard D.J. A neuronal network model of macaque primary visual cortex (V1). orientation selectivity and dynamics in the input layer 4Calpha Proc. Natl. Acad. Sci. USA. 97:2000;8087-8092.
46. Mechler F., Victor J.D., Purpura K.P., Shapley R. Robust temporal coding of contrast by V1 neurons for transient but not for steady-state stimuli. J. Neurosci. 18:1998;6583-6598.
47. Nelson S., Toth L., Sheth B., Sur M. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science. 265:1994;774-777.
48. Paré D., Shink E., Gaudreau H., Destexhe A., Lang E. Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J. Neurophysiol. 79:1998;1450-1460.
49. Ringach D.L., Bredfeldt C.E., Shapley R.M., Hawken M.J. Suppression of neural responses to non-optimal stimuli correlates with tuning selectivity in macaque V1. J. Neurophysiol. 87:2002;1018-1027.
50. Roerig B., Kao J.P. Organization of intracortical circuits in relation to direction preference maps in ferret visual cortex. J. Neurosci. 19:1999;RC44.
51. Ruff P.I., Rauschecker J.P., Palm G.A. Model of direction-selective "simple" cells in the visual cortex based inhibition asymmetry. Biol. Cybern. 57:1987;147-157.
52. Sabatini S.P., Solari F. An architectural hypothesis for direction selectivity in the visual cortex. the role of spatially asymmetric intracortical inhibition Biol. Cybern. 80:1999;171-183.
53. Sato H., Daw N.W., Fox K. An intracellular recording study of stimulus-specific response properties in cat area 17. Brain Res. 544:1991;156-161.
54. Schuett S., Bonhoeffer T., Hubener M. Pairing-induced changes of orientation maps in cat visual cortex. Neuron. 32:2001;325-337.
55. Schummers J., Marino J., Sur M. Synaptic integration by V1 neurons depends on location within the orientation map. Neuron. 36:2002;969-978.
56. Sclar G., Freeman R.D. Orientation selectivity in the cat's striate cortex is invariant with stimulus contrast. Exp. Brain Res. 46:1982;457-461.
57. Shmuel A., Grinvald A. Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J. Neurosci. 16:1996;6945-6964.
58. Sillito A.M. Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. J. Physiol. 289:1979;33-53.
59. Sillito A.M., Kemp J.A., Milson J.A., Berardi N. A re-evaluation of the mechanism underlying simple cell orientation selectivity. Brain Res. 194:1980;517-520.
60. Sillito A.M., Grieve K.L., Jones H.E., Cudeiro J., Davis J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature. 378:1995;492-496.
61. Somers D.C., Nelson S.B., Sur M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15:1995;5448-5465.
62. Thompson K.G., Leventhal A.G., Zhou Y.F., Liu D. Stimulus dependence of orientation and direction sensitivity of cat LGNd relay cells without cortical inputs. a comparison with area 17 cells Vis. Neurosci. 11:1994;939-951.
63. Troyer T.W., Krukowski A.E., Priebe N.J., Miller K.D. Contrast-invariant orientation tuning in cat visual cortex. thalamocortical input tuning and correlation-based intracortical connectivity J. Neurosci. 18:1998;5908-5927.
64. Volgushev M., Pei X., Vidyasagar T.R., Creutzfeldt O.D. Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Vis. Neurosci. 10:1993;1151-1155.
65. Volgushev M., Pernberg J., Eysel U.T. Comparison of the selectivity of postsynaptic potentials and spike responses in cat visual cortex. Eur. J. Neurosci. 12:2000;257-263.
66. Wörgötter F., Eysel U.T. Quantitative determination of orientational and directional components in the response of visual cortical cells to moving stimuli. Biol. Cybern. 57:1987;349-355.
67. Wörgötter F., Koch C. 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. 11:1991;1959-1979.
68. Yousef T., Bonhoeffer T., Kim D.S., Eysel U.T., Toth E., Kisvarday Z.F. Orientation topography of layer 4 lateral networks revealed by optical imaging in cat visual cortex (area 18). Eur. J. Neurosci. 11:1999;4291-4308.
69. Zar J.H. Biostatistical Analysis, fourth edition. 1974;Prentice-Hall Inc, New Jersey.