Abstract
The brain is able to adapt rapidly and continually to the surrounding environment, becoming increasingly sensitive to important and frequently encountered stimuli1,2,3,4. It is often claimed that this adaptive learning is highly task-specific, that is, we become more sensitive to the critical signals in the tasks we attend to5,6,7,8,9,10,11,12,13,14,15. Here, we show a new type of perceptual learning, which occurs without attention, without awareness and without any task relevance. Subjects were repeatedly presented with a background motion signal so weak that its direction was not visible; the invisible motion was an irrelevant background to the central task that engaged the subject's attention. Despite being below the threshold of visibility and being irrelevant to the central task, the repetitive exposure improved performance specifically for the direction of the exposed motion when tested in a subsequent suprathreshold test. These results suggest that a frequently presented feature sensitizes the visual system merely owing to its frequency, not its relevance or salience.
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References
Gilbert, C. D. Plasticity in visual perception and physiology. Curr. Opin. Neurobiol. 6, 269–274 (1996).
Vaina, L. M., Belliveau, J. W., des Roziers, E. B. & Zeffiro, T. A. Neural systems underlying learning and representation of global motion. Proc. Natl Acad. Sci. USA 95, 12657–12662 (1998).
Grossberg, S. How does the cerebral cortex work? Learning, attention, and grouping by the laminar circuits of visual cortex. Spat. Vis. 12, 163–185 (1999).
Zohary, E., Celebrini, S., Britten, K. H. & Newsome, W. T. Neuronal plasticity that underlies improvement in perceptual performance. Science 263, 1289–1292 (1994).
Ramachandran, V. S. & Braddick, O. Orientation-specific learning in stereopsis. Perception 2, 371–376 (1973).
Fiorentini, A. & Berardi, N. Perceptual learning specific for orientation and spatial frequency. Nature 287, 43–44 (1980).
Ball, K. & Sekuler, R. Direction-specific improvement in motion discrimination. Vision Res. 27, 953–965 (1987).
Shiu, L. P. & Pashler, H. Improvement in line orientation discrimination is retinally local but dependent on cognitive set. Percept. Psychophys. 52, 582–588 (1992).
Karni, A. & Sagi, D. The time course of learning a visual skill. Nature 365, 250–252 (1993).
Fahle, M. & Edelman, S. Long-term learning in vernier acuity: effects of stimulus orientation, range and of feedback. Vision Res. 33, 397–412 (1993).
Ahissar, M. & Hochstein, S. Attentional control of early perceptual learning. Proc. Natl Acad. Sci. USA 90, 5718–5722 (1993).
Sagi, D. & Tanne, D. Perceptual learning: learning to see. Curr. Opin. Neurobiol. 4, 195–199 (1994).
Ito, M., Westheimer, G. & Gilbert, C. D. Attention and perceptual learning modulate contextual influences on visual perception. Neuron 20, 1191–1197 (1998).
Crist, R. E., Li, W. & Gilbert, C. D. Learning to see: experience and attention in primary visual cortex. Nature Neurosci. 4, 519–525 (2001).
Koyama, S. & Watanabe, T. Different mechanisms for the learning of motion detection vs. the learning of motion direction discrimination. J. Vis. (Suppl.) (in the press).
Newsome, W. T. & Pare, E. B. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J. Neurosci. 8, 2201–2211 (1988).
Joseph, J. S., Chun, M. M. & Nakayama, K. Attentional requirements in a ‘preattentive’ feature search task. Nature 387, 805–807 (1997).
Treue, S. & Maunsell, J. H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).
Watanabe, T. et al. Task-dependent influences of attention on the activation of human primary visual cortex. Proc. Natl Acad. Sci. USA 95, 11489–11492 (1998).
Watanabe, T. et al. Attention-regulated activity in human primary visual cortex. J. Neurophysiol. 79, 2218–2221 (1998).
Somers, D. C., Dale, A. M., Seiffert, A. E. & Tootell, R. B. Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc. Natl Acad. Sci. USA 96, 1663–1668 (1999).
Gandhi, S. P., Heeger, D. J. & Boynton, G. M. Spatial attention affects brain activity in human primary visual cortex. Proc. Natl Acad. Sci. USA 96, 3314–3319 (1999).
Nakayama, K. & Shimojo, S. Experiencing and perceiving visual surfaces. Science 257, 1357–1363 (1992).
Saffran, J. R., Aslin, R. N. & Newport, E. L. Statistical learning by 8-month-old infants. Science 274, 1926–1928 (1996).
Albert, M. K. & Hoffman, D. D. The generic-viewpoint assumption and illusory contours. Perception 29, 303–312 (2000).
Slemmer, J. A., Kirkham, N. G. & Johnson, S. P. Visual statistical learning in infancy. J. Vis. (Suppl.) (in the press).
Bar, M. & Biederman, I. Subliminal visual priming. Psychol. Sci. 9, 464–469 (1998).
Chun, M. M. Contextual cueing of visual attention. Trends Cogn. Sci. 4, 170–178 (2000).
Barlow, H. B. in Vision: Coding and Efficiency (ed. Blakemore, C.) (Cambridge Univ. Press, Cambridge, 1989).
Acknowledgements
We thank M. Ahissar, P. Cavanagh, S. Hochstein, W. T. Newsome, R. Raizada and R. Sekuler for their comments on this or related study. This work was supported by an NSF (SBES, HCP) grant to T.W. and by Chiba University and JSPS fellowship to Y.S.
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Watanabe, T., Náñez, J. & Sasaki, Y. Perceptual learning without perception. Nature 413, 844–848 (2001). https://doi.org/10.1038/35101601
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DOI: https://doi.org/10.1038/35101601
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