Mechanisms underlying cross-orientation suppression in cat visual cortex

Nature Neuroscience

Volumn 9, Issue 4, 2006, Pages 552-561

  Priebe, Nicholas J ^a   Ferster, David ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CAT; CELL FUNCTION; CONTROLLED STUDY; FEEDBACK SYSTEM; GENICULATE BODY; LINEAR SYSTEM; MATHEMATICAL MODEL; MOLECULAR MECHANICS; NERVE EXCITABILITY; NEUROMODULATION; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RECORDING; SYNAPTIC INHIBITION; VISUAL CORTEX; VISUAL ORIENTATION; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; CATS; GENICULATE BODIES; MODELS, BIOLOGICAL; NEURONS; PATCH-CLAMP TECHNIQUES; SYNAPSES; SYNAPTIC TRANSMISSION; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 33645351673     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1660     Document Type: Article

References (50)

1. Hubel, D.H. & Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106-154 (1962).
2. Ferster, D. & Miller, K.D. Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23, 441-471 (2000).
3. Allison, J.D., Smith, K.R. & Bonds, A.B. Temporal-frequency tuning of cross-orientation suppression in the cat striate cortex. Vis. Neurosci. 18, 941-948 (2001).
4. Bishop, P.O., Coombs, J.S. & Henry, G.H. Receptive fields of simple cells in the cat striate cortex. J. Physiol. (Lond.) 231, 31-60 (1973).
5. 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, 144-163 (1992).
6. Geisler, W.S. & Albrecht, D.G. Cortical neurons: isolation of contrast gain control. Vision Res. 32, 1409-1410 (1992).
7. Morrone, M.C., Burr, D.C. & Maffei, L. Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc. R. Soc. Lond. B 216, 335-354 (1982).
8. Ben-Yishai, R., Bar-Or, R.L. & Sompolinsky, H. Theory of orientation tuning in visual cortex. Proc. Natl. Acad. Sci. USA 92, 3844-3848 (1995).
9. Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A. & Suarez, H.H. Recurrent excitation in neocortical circuits. Science 269, 981-985 (1995).
10. McLaughlin, D., Shapley, R. & Shelley, M. Large-scale modeling of the primary visual cortex: influence of cortical architecture upon neuronal response. J. Physiol. (Paris) 97, 237-252 (2003).
11. Somers, D.C., Nelson, S.B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448-5465 (1995).
12. Morrone, M.C., Burr, D.C. & Speed, H.D. Cross-orientation inhibition in cat is GABA mediated. Exp. Brain Res. 67, 635-644 (1987).
13. Sillito, A.M. 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 (1975).
14. Tsumoto, T., Eckart, W. & Creutzfeldt, O.D. Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp. Brain Res. 34, 351-363 (1979).
15. Anderson, J.S., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926 (2000).
16. Nelson, S., Toth, L., Sheth, B. & Sur, M. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 774-777 (1994).
17. Martinez, L.M., Alonso, J.M., Reid, R.C. & Hirsch, J.A. Laminar processing of stimulus orientation in cat visual cortex. J. Physiol. (Lond.) 540, 321-333 (2002).
18. Monier, C., Chavane, F., Baudot, P., Graham, L.J. & Fregnac, Y. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37, 663-680 (2003).
19. Freeman, T.C., Durand, S., Kiper, D.C. & Carandini, M. Suppression without inhibition in visual cortex. Neuron 35, 759-771 (2002).
20. Petrov, Y., Carandini, M. & McKee, S. Two distinct mechanisms of suppression in human vision. J. Neurosci. 25, 8704-8707 (2005).
21. Carandini, M., Heeger, D.J. & Senn, W. A synaptic explanation of suppression in visual cortex. J. Neurosci. 22, 10053-10065 (2002).
22. Boudreau, C.E. & Ferster, D. Short-term depression in thalamocortical synapses of cat primary visual cortex. J. Neurosci. 25, 7179-7190 (2005).
23. Reig, R., Gallego, R., Nowak, L.G. & Sanchez-Vives, M.V. Impact of cortical network activity on short-term synaptic depression. Cereb. Cortex published online August 17 2005 (doi: 10.1093/cercor/bhj014).
24. Chung, S. & Ferster, D. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177-1189 (1998).
25. Hansel, D. & van Vreeswijk, C. How noise contributes to contrast invariance of orientation tuning in cat visual cortex. J. Neurosci. 22, 5118-5128 (2002).
26. Miller, K.D. & Troyer, T.W. Neural noise can explain expansive, power-law nonlinearities in neural response functions. J. Neurophysiol. 87, 653-659 (2002).
27. Albrecht, D.G. & Geisler, W.S. Motion selectivity and the contrast-response function of simple cells in the visual cortex. Vis. Neurosci. 7, 531-546 (1991).
28. Heeger, D.J. Half-squaring in responses of cat striate cells. Vis. Neurosci. 9, 427-443 (1992).
29. DeAngelis, G.C., Ohzawa, I. & Freeman, R.D. Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. J. Neurophysiol. 69, 1118-1135 (1993).
30. Carandini, M. & Ferster, D. Atonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949-952 (1997).
31. Sanchez-Vives, M.V., Nowak, L.G. & McCormick, D.A. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J. Neurosci. 20, 4267-4285 (2000).
32. Hirsch, J.A., Alonso, J.M., Reid, R.C. & Martinez, L.M. Synaptic integration in striate cortical simple cells. J. Neurosci. 18, 9517-9528 (1998).
33. 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, 5908-5927 (1998).
34. Daugman, J.G. Uncertainty relation for resolution in space, spatial frequency, and orientation optimized by two-dimensional visual cortical filters. J. Opt. Soc. Am. A 2, 1160-1169 (1985).
35. Jones, J. & Palmer, L. The two-dimensional structure of simple receptive fields in cat striate cortex. J. Neurophysiol. 58, 1187-1211 (1987).
36. Bonds, A.B. Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis. Neurosci. 2, 41-55 (1989).
37. Carandini, M., Heeger, D.J. & Movshon, J.A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621-8644 (1997).
38. Tao, L., Shelley, M., McLaughlin, D. & Shapley, R. An egalitarian network model for the emergence of simple and complex cells in visual cortex. Proc. Natl. Acad. Sci. USA 101, 366-371 (2004).
39. Heeger, D.J., Simoncelli, E.P. & Movshon, J.A. Computational models of cortical visual processing. Proc. Natl. Acad. Sci. USA 93, 623-627 (1996).
40. Hirsch, J.A. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat. Neurosci. 6, 1300-1308 (2003).
41. Lauritzen, T.Z., Krukowski, A.E. & Miller, K.D. Local correlation-based circuitry can account for responses to multi-grating stimuli in a model of cat V1. J. Neurophysiol. 86, 1803-1815 (2001).
42. Smith, M.A., Bair, W. & Movshon, J.A. Dynamics of cross-orientation suppression in macaque V1. J. Neurosci. (in the press) (2006).
43. Carandini, M. & Ferster, D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470-484 (2000).
44. Priebe, N.J. & Ferster, D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45, 133-145 (2005).
45. Priebe, N.J., Mechler, F., Carandini, M. & Ferster, D. The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nat. Neurosci. 7, 1113-1122 (2004).
46. 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, 1968-1972 (2000).
47. Carandini, M. Amplification of trial-to-trial response variability by neurons in visual cortex. PLoS Biol. 2, E264 (2004).
48. Hochstein, S. & Shapley, R.M. Quantitative analysis of retinal ganglion cell classifications. J. Physiol. (Lond.) 262, 237-264 (1976).
49. Brainard, D.H. The psychophysics toolbox. Spat. Vis. 10, 433-436 (1997).
50. Sokal, R.R. & Rohlf, F.J. Biometry: the Principles and Practice of Statistics in Biological Research (W.H. Freeman, New York, 1995).