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Adaptation changes the direction tuning of macaque MT neurons

Abstract

Prolonged exposure to a stimulus, called 'adaptation', reduces cortical responsiveness. Adaptation has been studied extensively in primary visual cortex (V1), where responsivity is usually reduced most when the adapting and test stimuli are well matched. Theories about the functional benefits of adaptation have relied on this specificity, but the resultant changes in neuronal tuning are of the wrong type to account for well-documented perceptual aftereffects. Here we have used moving sinusoidal gratings to study the effect of adaptation on the direction tuning of neurons in area MT in macaques. Responsivity in MT is maintained best in the adapted direction and is strongly reduced for nearby directions. Consequently, adaptation in the preferred direction reduces the direction-tuning bandwidth, whereas adaptation at near-preferred directions causes tuning to shift toward the adapted direction. This previously unknown effect of adaptation is consistent with perceptual aftereffects and indicates that different cortical regions may adjust to constant sensory input in distinct ways.

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Figure 1: Diagram of the adaptation protocol.
Figure 2: Effect of adaptation in the preferred direction on the direction tuning of MT cells.
Figure 3: Effect of flank adaptation on the direction tuning of MT cells.
Figure 4: Effects of flank adaptation on responses to targets of different contrast.
Figure 5: Flank adaptation of V1 complex cells does not cause shifts in tuning.
Figure 6: End-of-flank and null adaptation in MT cells.
Figure 7: Changes in MT direction tuning as a function of adapting direction.
Figure 8: Changes in MT direction tuning after adaptation are consistent with perceptual effects.

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References

  1. Gibson, J.J. & Radner, M. Adaptation, aftereffect, and contrast in the perception of tilted lines. I. Quantitative results. J. Exp. Psychol. 20, 453–467 (1937).

    Article  Google Scholar 

  2. Clifford, C.W. Perceptual adaptation: motion parallels orientation. Trends Cogn. Sci. 6, 136–143 (2002).

    Article  Google Scholar 

  3. Gibson, J.J. Adaptation, after-effect and contrast in the perception of curved lines. J. Exp. Psychol. 16, 1–31 (1933).

    Article  Google Scholar 

  4. Kohler, W. & Wallach, H. Figural after-effects. Proc. Am. Phil. Soc. 88, 269–357 (1944).

    Google Scholar 

  5. Blakemore, C., Nachmias, J. & Sutton, P. The perceived spatial frequency shift: evidence for frequency-selective neurones in the human brain. J. Physiol. (Lond.) 210, 727–750 (1970).

    Article  CAS  Google Scholar 

  6. Levinson, E. & Sekuler, R. Adaptation alters perceived direction of motion. Vision Res. 16, 779–781 (1976).

    Article  CAS  Google Scholar 

  7. Patterson, R. & Becker, S. Direction-selective adaptation and simultaneous contrast induced by stereoscopic (cyclopean) motion. Vision Res. 36, 1773–1781 (1996).

    Article  CAS  Google Scholar 

  8. Schrater, P.R. & Simoncelli, E.P. Local velocity representation: evidence from motion adaptation. Vision Res. 38, 3899–3912 (1998).

    Article  CAS  Google Scholar 

  9. Movshon, J.A. & Lennie, P. Pattern-selective adaptation in visual cortical neurones. Nature 278, 850–852 (1979).

    Article  CAS  Google Scholar 

  10. Saul, A.B. & Cynader, M.S. Adaptation in single units in visual cortex: the tuning of aftereffects in the spatial domain. Vis. Neurosci. 2, 593–607 (1989).

    Article  CAS  Google Scholar 

  11. Saul, A.B. & Cynader, M.S. Adaptation in single units in visual cortex: the tuning of aftereffects in the temporal domain. Vis. Neurosci. 2, 609–620 (1989).

    Article  CAS  Google Scholar 

  12. Muller, J.R., Metha, A.B., Krauskopf, J. & Lennie, P. Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408 (1999).

    Article  CAS  Google Scholar 

  13. Dragoi, V., Sharma, J. & Sur, M. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28, 287–298 (2000).

    Article  CAS  Google Scholar 

  14. Dragoi, V., Sharma, J., Miller, E.K. & Sur, M. Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat. Neurosci. 5, 883–891 (2002).

    Article  CAS  Google Scholar 

  15. Felsen, G. et al. Dynamic modification of cortical orientation tuning mediated by recurrent connections. Neuron 36, 945–954 (2002).

    Article  CAS  Google Scholar 

  16. Dragoi, V., Rivadulla, C. & Sur, M. Foci of orientation plasticity in visual cortex. Nature 411, 80–86 (2001).

    Article  CAS  Google Scholar 

  17. Gilbert, C.D. & Wiesel, T.N. The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res. 30, 1689–1701 (1990).

    Article  CAS  Google Scholar 

  18. Fu, Y.X. et al. Temporal specificity in the cortical plasticity of visual space representation. Science 296, 1999–2003 (2002).

    Article  CAS  Google Scholar 

  19. Sur, M., Schummers, J. & Dragoi, V. Cortical plasticity: time for a change. Curr. Biol. 12, R168–170 (2002).

    Article  CAS  Google Scholar 

  20. Wainwright, M.J. Visual adaptation as optimal information transmission. Vision Res. 39, 3960–3974 (1999).

    Article  CAS  Google Scholar 

  21. Wainwright, M.J., Schwartz, O. & Simoncelli, E.P. Natural image statistics and divisive normalization: modeling nonlinearity and adaptation in cortical neurons. In Probabilistic Models of the Brain: Perception and Neural Function (eds. Rao, R., Olshausen, B.A. & Lewicki, M.S.) 203–222 (MIT Press, Cambridge, 2002).

    Google Scholar 

  22. Barlow, H.B. A theory about the functional role and synaptic mechanisms of visual after-effects. In Vision: Coding and Efficiency (ed. Blakemore, C.) 363–375 (Cambridge Univ. Press, New York, 1990).

    Google Scholar 

  23. Barlow, H.B. & Foldiak, P. Adaptation and decorrelation in the cortex. In The Computing Neuron (eds. Durbin, R., Miall, C. & Mitchinson, G.) 54–72 (Addison-Wesley, New York, 1989).

    Google Scholar 

  24. Zeki, S.M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol. (Lond.) 236, 549–573 (1974).

    Article  CAS  Google Scholar 

  25. Maunsell, J.H. & Van Essen, D.C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J. Neurophysiol. 49, 1127–1147 (1983).

    Article  CAS  Google Scholar 

  26. Newsome, W.T., Britten, K.H. & Movshon, J.A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989).

    Article  CAS  Google Scholar 

  27. Salzman, C.D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).

    Article  CAS  Google Scholar 

  28. Thiele, A., Dobkins, K.R. & Albright, T.D. Neural correlates of contrast detection at threshold. Neuron 26, 715–724 (2000).

    Article  CAS  Google Scholar 

  29. Kohn, A. & Movshon, J.A. Neuronal adaptation to visual motion in area MT of the macaque. Neuron 39, 681–691 (2003).

    Article  CAS  Google Scholar 

  30. Leventhal, A.G., Thompson, K.G., Liu, D., Zhou, Y. & Ault, S.J. Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. J. Neurosci. 15, 1808–1818 (1995).

    Article  CAS  Google Scholar 

  31. Snowden, R.J., Treue, S., Erickson, R.G. & Andersen, R.A. The response of area MT and V1 neurons to transparent motion. J. Neurosci. 11, 2768–2785 (1991).

    Article  CAS  Google Scholar 

  32. Qian, N. & Andersen, R.A. Transparent motion perception as detection of unbalanced motion signals. II. Physiology. J. Neurosci. 14, 7367–7380 (1994).

    Article  CAS  Google Scholar 

  33. Petersen, S.E., Baker, J.F. & Allman, J.M. Direction-specific adaptation in area MT of the owl monkey. Brain Res. 346, 146–150 (1985).

    Article  CAS  Google Scholar 

  34. Movshon, J.A. & Newsome, W.T. Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J. Neurosci. 16, 7733–7741 (1996).

    Article  CAS  Google Scholar 

  35. Albrecht, D.G., Farrar, S.B. & Hamilton, D.B. Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. J. Physiol. (Lond.) 347, 713–739 (1984).

    Article  CAS  Google Scholar 

  36. Ohzawa, I., Sclar, G. & Freeman, R.D. Contrast gain control in the cat's visual system. J. Neurophysiol. 54, 651–667 (1985).

    Article  CAS  Google Scholar 

  37. Maunsell, J.H. & Van Essen, D.C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J. Neurosci. 3, 2563–2586 (1983).

    Article  CAS  Google Scholar 

  38. Carandini, M. & Ferster, D. A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276, 949–952 (1997).

    Article  CAS  Google Scholar 

  39. 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).

    Article  CAS  Google Scholar 

  40. Teich, A.F. & Qian, N. Learning and adaptation in a recurrent model of V1 orientation selectivity. J. Neurophysiol. 89, 2086–2100 (2003).

    Article  Google Scholar 

  41. Thomson, A.M. & Deuchars, J. Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510–522 (1997).

    Article  CAS  Google Scholar 

  42. Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome W.T. The analysis of moving visual patterns. In Pattern Recognition Mechanisms (eds. Chagas, C., Gattass, R. & Gross, C.) 117–151 (Vatican Press, Rome, 1985).

    Chapter  Google Scholar 

  43. Stoner, G.R. & Albright, T.D. Neural correlates of perceptual motion coherence. Nature 358, 412–414 (1992).

    Article  CAS  Google Scholar 

  44. Van Wezel, R.J. & Britten, K.H. Motion adaptation in area MT. J. Neurophysiol. 88, 3469–3476 (2002).

    Article  Google Scholar 

  45. Chaudhuri, A. Modulation of the motion aftereffect by selective attention. Nature 344, 60–62 (1990).

    Article  CAS  Google Scholar 

  46. Lehmkuhle, S.W. & Fox, R. Effect of binocular rivalry suppression on the motion aftereffect. Vision Res. 15, 855–859 (1975).

    Article  CAS  Google Scholar 

  47. Wiesenfelder, H. & Blake, R. The neural site of binocular rivalry relative to the analysis of motion in the human visual system. J. Neurosci. 10, 3880–3888 (1990).

    Article  CAS  Google Scholar 

  48. Chance, F.S., Nelson, S.B. & Abbott, L.F. Synaptic depression and the temporal response characteristics of V1 cells. J. Neurosci. 18, 4785–4799 (1998).

    Article  CAS  Google Scholar 

  49. Cavanaugh, J.R., Bair, W. & Movshon, J.A. Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. J. Neurophysiol. 88, 2530–2546 (2002).

    Article  Google Scholar 

  50. Chandler, J.P. Subroutine STEPIT: finds local minima of a smooth function of several parameters. Behav. Sci. 14, 81–82 (1969).

    Google Scholar 

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Acknowledgements

We thank W. Bair, S. Solomon, E. Simoncelli and N. Rust for comments on the manuscript; M. Smith and N. Majaj for assistance with data collection; and M. Hou and N. Doron for histology. This work was supported by a grant from the National Institutes of Health (EY02017) and by an Howard Hughes Medical Institute Investigatorship to J.A.M.

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Correspondence to Adam Kohn.

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Supplementary information

Supplementary Figure 1

Predicted shifts in perceived direction for a range of changes in neuronal tuning. (PDF 260 kb)

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Kohn, A., Movshon, J. Adaptation changes the direction tuning of macaque MT neurons. Nat Neurosci 7, 764–772 (2004). https://doi.org/10.1038/nn1267

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