Rapid adaptation in visual cortex to the structure of images

Science

Volumn 285, Issue 5432, 1999, Pages 1405-1408

  Müller, James R ^a,c   Metha, Andrew B ^a,d   Krauskopf, John ^b   Lennie, Peter ^a,b  

^a UNIVERSITY OF ROCHESTER   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ARTICLE; BRAIN CORTEX; HUMAN; IMAGING; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; VISUAL ADAPTATION; VISUAL ORIENTATION;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; EVOKED POTENTIALS, VISUAL; FIXATION, OCULAR; MACACA FASCICULARIS; NEURONS; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; TIME FACTORS; VISUAL CORTEX;

EID: 0344172831     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.285.5432.1405     Document Type: Article

References (61)

1. 2, and the display was refreshed at 75 Hz. Action potentials from isolated single units were recorded with 0.1-ms accuracy. All receptive fields lay within 3° of the center of the fovea. Simple and complex cells were distinguished by their responses to moving gratings.
2. 2, and the display was refreshed at 75 Hz. Action potentials from isolated single units were recorded with 0.1-ms accuracy. All receptive fields lay within 3° of the center of the fovea. Simple and complex cells were distinguished by their responses to moving gratings.
3. A rapidly decaying response to a step stimulus implies low sensitivity to low temporal frequencies of stimulation, and this is found [M. J. Hawken, R. M. Shapley, D. H. Grosof, Vis. Neurosci. 13, 477 (1996)]. Nonlinearities in the behavior of cortical neurons make the decay of responses to steps even more rapid than would be expected from the temporal modulation transfer function [D. J. Tothurst, N. S. Walker, I. D. Thompson, A. F. Dean, Exp. Brain Res. 38, 431 (1980); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998)].
4. A rapidly decaying response to a step stimulus implies low sensitivity to low temporal frequencies of stimulation, and this is found [M. J. Hawken, R. M. Shapley, D. H. Grosof, Vis. Neurosci. 13, 477 (1996)]. Nonlinearities in the behavior of cortical neurons make the decay of responses to steps even more rapid than would be expected from the temporal modulation transfer function [D. J. Tothurst, N. S. Walker, I. D. Thompson, A. F. Dean, Exp. Brain Res. 38, 431 (1980); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998)].
5. A rapidly decaying response to a step stimulus implies low sensitivity to low temporal frequencies of stimulation, and this is found [M. J. Hawken, R. M. Shapley, D. H. Grosof, Vis. Neurosci. 13, 477 (1996)]. Nonlinearities in the behavior of cortical neurons make the decay of responses to steps even more rapid than would be expected from the temporal modulation transfer function [D. J. Tothurst, N. S. Walker, I. D. Thompson, A. F. Dean, Exp. Brain Res. 38, 431 (1980); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998)].
6. M. J. Hawken, R. M. Shapley, D. H. Grosof, Vis. Neurosci. 13, 477 (1996);
7. P. Lennie and J. Krauskopf, unpublished observations.
8. The median time-constant of recovery of sensitivity in our sample of cells was 6 s. The median time-constant of desensitization was less than 100 ms.
9. In six of eight neurons in which we compared the desensitization brought about by stationary and counterphase flickering gratings, the counterphase adapter was at least as effective as the stationary one.
10. R. G. Vautin and M. A. Berkley, J. Neurophysiol. 40, 1051 (1978); J. A. Movshon and P. Lennie, Nature 278, 850 (1979); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984); G. Sclar, P. Lennie, D. D. DePriest, Vision Res. 29, 747 (1989).
11. R. G. Vautin and M. A. Berkley, J. Neurophysiol. 40, 1051 (1978); J. A. Movshon and P. Lennie, Nature 278, 850 (1979); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984); G. Sclar, P. Lennie, D. D. DePriest, Vision Res. 29, 747 (1989).
12. R. G. Vautin and M. A. Berkley, J. Neurophysiol. 40, 1051 (1978); J. A. Movshon and P. Lennie, Nature 278, 850 (1979); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984); G. Sclar, P. Lennie, D. D. DePriest, Vision Res. 29, 747 (1989).
13. R. G. Vautin and M. A. Berkley, J. Neurophysiol. 40, 1051 (1978); J. A. Movshon and P. Lennie, Nature 278, 850 (1979); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984); G. Sclar, P. Lennie, D. D. DePriest, Vision Res. 29, 747 (1989).
14. A. B. Bonds, Vis. Neurosci. 6, 239 (1991); S. B. Nelson, J. Neurosci. 11, 344 (1991).
15. A. B. Bonds, Vis. Neurosci. 6, 239 (1991); S. B. Nelson, J. Neurosci. 11, 344 (1991).
16. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Bonds, Vis. Neurosci. 6, 239 (1991); I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; P. Lennie, M. J. M. Lankheet, J. Krauskopf, Invest. Ophthalmol. Vis. Sci. (suppl.) 35, 1662 (1994).
17. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Bonds, Vis. Neurosci. 6, 239 (1991); I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; P. Lennie, M. J. M. Lankheet, J. Krauskopf, Invest. Ophthalmol. Vis. Sci. (suppl.) 35, 1662 (1994).
18. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Bonds, Vis. Neurosci. 6, 239 (1991); I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; P. Lennie, M. J. M. Lankheet, J. Krauskopf, Invest. Ophthalmol. Vis. Sci. (suppl.) 35, 1662 (1994).
19. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Bonds, Vis. Neurosci. 6, 239 (1991); I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; P. Lennie, M. J. M. Lankheet, J. Krauskopf, Invest. Ophthalmol. Vis. Sci. (suppl.) 35, 1662 (1994).
20. I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; W. S. Geisler and D. G. Albrecht, Vision Res. 32, 1409 (1992); D. J. Heeger, Vis. Neurosci. 9, 181 (1992)]; M. Carandini, D. J. Heeger, J. A. Movshon, J. Neurosci. 17, 8621 (1997).
21. I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; W. S. Geisler and D. G. Albrecht, Vision Res. 32, 1409 (1992); D. J. Heeger, Vis. Neurosci. 9, 181 (1992)]; M. Carandini, D. J. Heeger, J. A. Movshon, J. Neurosci. 17, 8621 (1997).
22. I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; W. S. Geisler and D. G. Albrecht, Vision Res. 32, 1409 (1992); D. J. Heeger, Vis. Neurosci. 9, 181 (1992)]; M. Carandini, D. J. Heeger, J. A. Movshon, J. Neurosci. 17, 8621 (1997).
23. I. Ohzawa, G. Sclar, R. D. Freeman, J. Neurophysiol. 54, 651 (1985)]; W. S. Geisler and D. G. Albrecht, Vision Res. 32, 1409 (1992); D. J. Heeger, Vis. Neurosci. 9, 181 (1992)]; M. Carandini, D. J. Heeger, J. A. Movshon, J. Neurosci. 17, 8621 (1997).
24. W. S. Geisler and D. G. Albrecht, Vision Res. 32, 1409 (1992).
25. A. B. Bonds, Vis. Neurosci. 6, 239 (1991); D. J. Heeger, Ibid 9, 181 (1992); G. C. DeAngelis, J. G. Robson, I. Ohzawa, R. D. Freeman, J. Neurophysiol. 68, 144 (1992).
26. A. B. Bonds, Vis. Neurosci. 6, 239 (1991); D. J. Heeger, Ibid 9, 181 (1992); G. C. DeAngelis, J. G. Robson, I. Ohzawa, R. D. Freeman, J. Neurophysiol. 68, 144 (1992).
27. A. B. Bonds, Vis. Neurosci. 6, 239 (1991); D. J. Heeger, Ibid 9, 181 (1992); G. C. DeAngelis, J. G. Robson, I. Ohzawa, R. D. Freeman, J. Neurophysiol. 68, 144 (1992).
28. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Saul and M. S. Cynader, Vis. Neurosci. 2, 593 (1989); ibid., p. 609; M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B 352, 1149 (1997).
29. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Saul and M. S. Cynader, Vis. Neurosci. 2, 593 (1989); ibid., p. 609; M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B 352, 1149 (1997).
30. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Saul and M. S. Cynader, Vis. Neurosci. 2, 593 (1989); ibid., p. 609; M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B 352, 1149 (1997).
31. J. A. Movshon and P. Lennie, Nature 278, 850 (1979); A. B. Saul and M. S. Cynader, Vis. Neurosci. 2, 593 (1989); ibid., p. 609; M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B 352, 1149 (1997).
32. H. B. Barlow, D. I. A. MacLeod, A. van Meeteren, Vision Res. 16, 1043 (1976)]; D. Regan and K. I. Beverley, J. Opt. Soc. Am. 2, 147 (1985)]; M. W. Greenlee and F. Heitger, Vision Res. 28, 791 (1988).
33. H. B. Barlow, D. I. A. MacLeod, A. van Meeteren, Vision Res. 16, 1043 (1976)]; D. Regan and K. I. Beverley, J. Opt. Soc. Am. 2, 147 (1985)]; M. W. Greenlee and F. Heitger, Vision Res. 28, 791 (1988).
34. H. B. Barlow, D. I. A. MacLeod, A. van Meeteren, Vision Res. 16, 1043 (1976)]; D. Regan and K. I. Beverley, J. Opt. Soc. Am. 2, 147 (1985)]; M. W. Greenlee and F. Heitger, Vision Res. 28, 791 (1988).
35. At the beginning of each trial lasting 1.75 s, an adapting grating (or a blank field) was presented for 0.5 s. This was followed after 215 ms (Fig. 2A) or 27 ms (Fig. 2B) by a 94-ms presentation of a test grating at one of 10 orientations (0°, ±7°, ±14°, ±21°, ±28°, or +90°), or by nothing. Discharge rate was calculated from the whole response to the test grating. Gratings had optimal spatial frequency, size, and position, and 100% contrast In successive trials the different adapting and test grating pairs were randomly interleaved, and each such trial was repeated 40 times. When no grating was visible, the screen displayed a spatially uniform field of the average luminance.
36. i of the responses to stimuli with orientations i ∈ [0°, ±7°, ±14°, ±21°, ±28°]. For sharply (and symmetrically) tuned neurons with half-width <28° this is exactly the preferred orientation. For all neurons it increases monotonically with preferred orientation. The average neuron's center-of-mass changed by 1.5°.
37. 2 dx. This measure characterizes the performance of an ideal observer.
38. Not much is known about this, but successive fixations are often close together [A. L. Yarbus, Eye Movements and Vision (Plenum, New York, 1967); A. T. Bahill, D. Adler, L. Stark, Invest. Ophthalmol. 14, 468 (1975)], and nearby image patches have correlated orientation and spatial frequency [E. P. Simoncelli and O. Schwartz, in Advances in Neural Information Processing Systems 11, M. S. Kearns, S. A. Solla, D. A. Cohn, Eds. (MIT Press, Cambridge, MA, 1999)].
39. Not much is known about this, but successive fixations are often close together [A. L. Yarbus, Eye Movements and Vision (Plenum, New York, 1967); A. T. Bahill, D. Adler, L. Stark, Invest. Ophthalmol. 14, 468 (1975)], and nearby image patches have correlated orientation and spatial frequency [E. P. Simoncelli and O. Schwartz, in Advances in Neural Information Processing Systems 11, M. S. Kearns, S. A. Solla, D. A. Cohn, Eds. (MIT Press, Cambridge, MA, 1999)].
40. Not much is known about this, but successive fixations are often close together [A. L. Yarbus, Eye Movements and Vision (Plenum, New York, 1967); A. T. Bahill, D. Adler, L. Stark, Invest. Ophthalmol. 14, 468 (1975)], and nearby image patches have correlated orientation and spatial frequency [E. P. Simoncelli and O. Schwartz, in Advances in Neural Information Processing Systems 11, M. S. Kearns, S. A. Solla, D. A. Cohn, Eds. (MIT Press, Cambridge, MA, 1999)].
41. Barlow [H. B. Barlow, in Vision: Coding and Efficiency, C. Blakemore, Ed. (Cambridge Univ. Press, Cambridge, 1990), p. 363.] first drew attention to this consequence of adaptation.
42. We define redundancy in the population's response (ψ) due to each probe orientation (θ) relative to the adapting orientation by ψ(θ) = ∑ All cells Resp(cell A,θ)·Resp(cell B,θ)/Number of cell pairs the average, unnormalized, point-by-point product of the responses of all pairs of neurons. This is an intermediate stage in the calculation of the cross-correlation. To establish how adaptation reduces the redundancy among responses, we calculate ψ before and after adaptation, for probes at a range of orientations. We treat every neuron as if it had been adapted to the pattern at orientation 0°.
43. E. P. Simoncelli and O. Schwartz, in Advances in Neural Information Processing Systems 11, M. S. Kearns, S. A. Solla, D. A. Cohn, Eds. (MIT Press, Cambridge, MA, 1999).
44. L. Maffei and A. Fiorentini, Vision Res. 16, 1131 (1976); J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); G. C. DeAngelis, R. D. Freeman, I. Ohzawa, J. Neurophysiol. 71, 347 (1994); A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, J. Davis, Nature 378, 492 (1995); J. B. Levitt and J. S. Lund, ibid. 387, 73 (1997).
45. L. Maffei and A. Fiorentini, Vision Res. 16, 1131 (1976); J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); G. C. DeAngelis, R. D. Freeman, I. Ohzawa, J. Neurophysiol. 71, 347 (1994); A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, J. Davis, Nature 378, 492 (1995); J. B. Levitt and J. S. Lund, ibid. 387, 73 (1997).
46. L. Maffei and A. Fiorentini, Vision Res. 16, 1131 (1976); J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); G. C. DeAngelis, R. D. Freeman, I. Ohzawa, J. Neurophysiol. 71, 347 (1994); A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, J. Davis, Nature 378, 492 (1995); J. B. Levitt and J. S. Lund, ibid. 387, 73 (1997).
47. L. Maffei and A. Fiorentini, Vision Res. 16, 1131 (1976); J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); G. C. DeAngelis, R. D. Freeman, I. Ohzawa, J. Neurophysiol. 71, 347 (1994); A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, J. Davis, Nature 378, 492 (1995); J. B. Levitt and J. S. Lund, ibid. 387, 73 (1997).
48. L. Maffei and A. Fiorentini, Vision Res. 16, 1131 (1976); J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); G. C. DeAngelis, R. D. Freeman, I. Ohzawa, J. Neurophysiol. 71, 347 (1994); A. M. Sillito, K. L. Grieve, H. E. Jones, J. Cudeiro, J. Davis, Nature 378, 492 (1995); J. B. Levitt and J. S. Lund, ibid. 387, 73 (1997).
49. Sharpened orientation selectivity has been suggested [J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); C. Blakemore and E. A. Tobin, Exp. Brain Res. 15, 439 (1972)] and is among the constellation of changes in orientation selectivity reported by Gilbert and Wiesel [C. D. Gilbert and T. N. Wiesel, Vision Res. 30, 1689 (1990)].
50. Sharpened orientation selectivity has been suggested [J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); C. Blakemore and E. A. Tobin, Exp. Brain Res. 15, 439 (1972)] and is among the constellation of changes in orientation selectivity reported by Gilbert and Wiesel [C. D. Gilbert and T. N. Wiesel, Vision Res. 30, 1689 (1990)].
51. Sharpened orientation selectivity has been suggested [J. I. Nelson and B. J. Frost, Brain Res. 139, 359 (1978); C. Blakemore and E. A. Tobin, Exp. Brain Res. 15, 439 (1972)] and is among the constellation of changes in orientation selectivity reported by Gilbert and Wiesel [C. D. Gilbert and T. N. Wiesel, Vision Res. 30, 1689 (1990)].
52. L. Maffei and A. Fiorentini [Vision Res. 16, 1131 (1976)] suggested that adaptation sharpens spatial frequency tuning.
53. See, for example, A. T. Bahill, D. Adler, L. Stark, Invest. Ophthalmol. 14, 468 (1975). The distribution of saccade sizes is heavily task-dependent [for example, M. F. Land and S. Furneaux, Philos. Trans. R. Soc. London Ser. B 352, 1231 (1997)].
54. See, for example, A. T. Bahill, D. Adler, L. Stark, Invest. Ophthalmol. 14, 468 (1975). The distribution of saccade sizes is heavily task-dependent [for example, M. F. Land and S. Furneaux, Philos. Trans. R. Soc. London Ser. B 352, 1231 (1997)].
55. M. Carandini and D. Ferster, Science 276, 949 (1997).
56. M. Carandini, personal communication.
57. H. Markram and M. Tsodyks, Nature 382, 807 (1996); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998); L. F. Abbott, J. A. Varela, K. Sen, S. B. Nelson, Science 275, 220 (1997).
58. H. Markram and M. Tsodyks, Nature 382, 807 (1996); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998); L. F. Abbott, J. A. Varela, K. Sen, S. B. Nelson, Science 275, 220 (1997).
59. H. Markram and M. Tsodyks, Nature 382, 807 (1996); F. S. Chance, S. B. Nelson, L. F. Abbott, J. Neurosci. 18, 4785 (1998); L. F. Abbott, J. A. Varela, K. Sen, S. B. Nelson, Science 275, 220 (1997).
60. A surrounding grating brought about significant changes in orientation tuning in almost half of the complex cells we studied.
61. All animal procedures were approved by the University of Rochester committee for the care and use of laboratory animals. Funded by NIH grants EY04440, EY01319, EY06638, and EY07125.