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The Journal of Neuroscience, March 26, 2008, 28(13):3374-3383; doi:10.1523/JNEUROSCI.0182-08.2008

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Behavioral/Systems/Cognitive
Adaptation across the Cortical Hierarchy: Low-Level Curve Adaptation Affects High-Level Facial-Expression Judgments

Hong Xu,¹ Peter Dayan,² Richard M. Lipkin,¹ and Ning Qian¹

¹Department of Neuroscience, Columbia University, New York, New York 10032, and ²Gatsby Computational Neuroscience Unit, University College London, London WC1N 3AR, United Kingdom

Correspondence should be addressed to Dr. Ning Qian, Department of Neuroscience, Columbia University/New York State Psychiatric Institute, 1051 Riverside Drive, Kolb Annex 519, New York, NY 10032. Email: nq6{at}columbia.edu

Adaptation is ubiquitous in sensory processing. Although sensory processing is hierarchical, with neurons at higher levels exhibiting greater degrees of tuning complexity and invariance than those at lower levels, few experimental or theoretical studies address how adaptation at one hierarchical level affects processing at others. Nevertheless, this issue is critical for understanding cortical coding and computation. Therefore, we examined whether perception of high-level facial expressions can be affected by adaptation to low-level curves (i.e., the shape of a mouth). After adapting to a concave curve, subjects more frequently perceived faces as happy, and after adapting to a convex curve, subjects more frequently perceived faces as sad. We observed this multilevel aftereffect with both cartoon and real test faces when the adapting curve and the mouths of the test faces had the same location. However, when we placed the adapting curve 0.2° below the test faces, the effect disappeared. Surprisingly, this positional specificity held even when real faces, instead of curves, were the adapting stimuli, suggesting that it is a general property for facial-expression aftereffects. We also studied the converse question of whether face adaptation affects curvature judgments, and found such effects after adapting to a cartoon face, but not a real face. Our results suggest that there is a local component in facial-expression representation, in addition to holistic representations emphasized in previous studies. By showing that adaptation can propagate up the cortical hierarchy, our findings also challenge existing functional accounts of adaptation.

Key words: multilevel adaptation; cross-level aftereffect; local feature; global representation; inverted face adaptation; cross-adaptation between curves and faces

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Received Jan. 15, 2008; accepted Feb. 13, 2008.

Correspondence should be addressed to Dr. Ning Qian, Department of Neuroscience, Columbia University/New York State Psychiatric Institute, 1051 Riverside Drive, Kolb Annex 519, New York, NY 10032. Email: nq6{at}columbia.edu

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