A tonic hyperpolarization underlying contrast adaptation in cat visual cortex

Science

Volumn 276, Issue 5314, 1997, Pages 949-952

  Carandini, Matteo ^a,b   Ferster, David ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; HYPERPOLARIZATION; NERVE CELL MEMBRANE POTENTIAL; PRIORITY JOURNAL; VISION; VISUAL ADAPTATION; VISUAL CORTEX; VISUAL STIMULATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CATS; CONTRAST SENSITIVITY; EVOKED POTENTIALS, VISUAL; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; VISUAL CORTEX;

EID: 0030901850     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5314.949     Document Type: Article

References (35)

1. L. Maffei, A. Fiorentini, S. Bisti, Science 182, 1036, (1973); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984).
2. L. Maffei, A. Fiorentini, S. Bisti, Science 182, 1036, (1973); D. G. Albrecht, S. B. Farrar, D. B. Hamilton, J. Physiol. (London) 347, 713 (1984).
3. R. G. Vautin and M. A. Berkeley, J. Neurophysiol. 40, 1051 (1977).
4. J. A. Movshon and P. Lennie, Nature 278, 850 (1979).
5. I. Ohzawa, G. Sclar, R. D. Freeman, ibid. 298, 266 (1982); J. Neurophysiol. 54, 651 (1985).
6. I. Ohzawa, G. Sclar, R. D. Freeman, ibid. 298, 266 (1982); J. Neurophysiol. 54, 651 (1985).
7. This phenomenon is uniquely cortical because it is essentially absent at earlier stages of visual processing (4) [T. Shou, X. Li, Y. Zhou, B. Hu, Visual Neurosci. 13, 605 (1996)], and stimulation of one eye reduces the responses of cortical cells to stimulation of the other eye [L. Maffei, N. Berardi, S. Bisti, J. Neurophysiol. 55, 966 (1986)).
8. This phenomenon is uniquely cortical because it is essentially absent at earlier stages of visual processing (4) [T. Shou, X. Li, Y. Zhou, B. Hu, Visual Neurosci. 13, 605 (1996)], and stimulation of one eye reduces the responses of cortical cells to stimulation of the other eye [L. Maffei, N. Berardi, S. Bisti, J. Neurophysiol. 55, 966 (1986)).
9. H. B. Barlow, in Vision: Coding and Efficiency, C. Blakemore, Ed. (Cambridge Univ. Press, Cambridge, 1990); M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B, in press.
10. H. B. Barlow, in Vision: Coding and Efficiency, C. Blakemore, Ed. (Cambridge Univ. Press, Cambridge, 1990); M. Carandini, H. B. Barlow, L. P. O'Keefe, A. B. Poirson, J. A. Movshon, Philos. Trans. R. Soc. London Ser. B, in press.
11. 2) of optimal orientation, direction, spatial and temporal frequency, and window size were presented monocularty on an oscilloscope screen with an image generator (lnnisfree, Cambridge, MA).
12. J. A. Movshon, I. D. Thompson, D. J. Tolhurst, J. Physiol. (London) 283, 53 (1978).
13. D. G. Albrecht and D. B. Hamilton, J. Neurophysiol. 48, 217 (1982).
14. This increase in the mean membrane potential with increasing contrast represents a nonlinearity in the responses of simple cells. We propose that it is caused by a differential contrast sensitivity of the excitatory and inhibitory inputs known to underlie the responses of simple cells (12). In this scenario, the responses at low contrasts are dominated by excitation, and inhibition appears only at higher contrasts. At low contrasts, increases in contrast cause increases in excitation that are relatively unopposed by increases in inhibition; as a result, the mean membrane potential increases with contrast. At higher contrasts, the inhibitory inputs begin to respond strongly, opposing the effects of increasing excitation and causing the mean potential to stop growing with contrast or even to decrease slightly.
15. C. Blakemore and F. W. Campbell, J. Physiol. (London) 203, 237 (1969).
16. The depolarized portions of the visually driven membrane potential responses of a simple cell are attributable to increases in excitation as well as decreases in inhibition. Similarly, the hyperpolarized portions of these responses are attributable to decreases in excitation as well as increases in inhibition [D. Ferster, J. Neurosci. 8, 1172 (1988)].
17. A. B. Bonds, Visual Neurosci. 6, 239 (1991).
18. J. J. Kulikowski, V. M. Rao, T. R. Vidyasagar, J. Physiol. (London) 318, 21P (1981); A. B. Saul and M. S. Cynader, Visual Neurosci. 2, 593 (1989); S. Marlin, R. Douglas, M. Cynader, J. Neurophysiol. 69, 2209 (1993).
19. J. J. Kulikowski, V. M. Rao, T. R. Vidyasagar, J. Physiol. (London) 318, 21P (1981); A. B. Saul and M. S. Cynader, Visual Neurosci. 2, 593 (1989); S. Marlin, R. Douglas, M. Cynader, J. Neurophysiol. 69, 2209 (1993).
20. J. J. Kulikowski, V. M. Rao, T. R. Vidyasagar, J. Physiol. (London) 318, 21P (1981); A. B. Saul and M. S. Cynader, Visual Neurosci. 2, 593 (1989); S. Marlin, R. Douglas, M. Cynader, J. Neurophysiol. 69, 2209 (1993).
21. J. A. Movshon, I. D. Thompson, D. J. Tolhurst, J. Physiol. (London) 283, 79 (1978).
22. Other possible mechanisms include a long-lasting after-hyperpolarization [P. C. Schwindt et al., J. Neurophysiol. 59, 424 (1988)], an electrogenic pump, and a neuromodulatory effect on voltage-gated channels. Because adaptation could also be observed in the absence of spikes in the recorded cell, we doubt that the first mechanism is at work. It is doubtful that the second mechanism could produce hyperpolarizations as large as 15 mV. Our results, however, would be consistent with the third mechanism.
23. J. McLean and L. A. Palmer, Visual Neorosci. 13, 1069 (1996).
24. E. J. DeBruyn and A. B. Bonds, Brain Res. 383, 339 (1986); T. R. Vidyasagar, Neuroscience 36, 175 (1990).
25. E. J. DeBruyn and A. B. Bonds, Brain Res. 383, 339 (1986); T. R. Vidyasagar, Neuroscience 36, 175 (1990).
26. A. B. Saul, Visual Neurosci. 12, 191 (1995).
27. R. S. Dealy and D. J. Tolhurst, J. Physiol. (London) 241, 261 (1974); D. J. Heeger, Visual Neurosci. 9, 181 (1992).
28. R. S. Dealy and D. J. Tolhurst, J. Physiol. (London) 241, 261 (1974); D. J. Heeger, Visual Neurosci. 9, 181 (1992).
29. in.
30. R. J. Douglas, K. A. C. Martin, D. Whitteridge, Nature 332, 642 (1988).
31. D. Ferster and B. Jagadeesh, J. Neurosci. 12, 1262 (1992).
32. S. B. Nelson, J. A. Varela, K. Sen, L. F. Abbott, in The Neurobiology of Computation, J. Bower, Ed. (Kluwer Academic, Boston, in press); E. V. Todorov, A. G. Siapas, D. C. Somers, S. B. Nelson, ibid.
33. S. B. Nelson, J. A. Varela, K. Sen, L. F. Abbott, in The Neurobiology of Computation, J. Bower, Ed. (Kluwer Academic, Boston, in press); E. V. Todorov, A. G. Siapas, D. C. Somers, S. B. Nelson, ibid.
34. R. J. Douglas, C. Koch, M. Mahowald, K. A. C. Martin, H. H. Suarez, Science 269, 981 (1995).
35. We thank S. Chung for her contribution to the experiments and N. Spruston for his comments on the manuscript. Supported by National Eye Institute grant EY04726.