Misbinding of Color and Motion in Human Visual Cortex

A fundamental challenge for the visual system is to integrate visual features into a coherent scene, known as the binding problem. The neural mechanisms of feature binding are hard to identify because of difficulties in separating active feature binding from feature co-occurrence. In previous studies on feature binding [1Holcombe A.O. Cavanagh P. Early binding of feature pairs for visual perception.Nat. Neurosci. 2001; 4: 127-128Crossref PubMed Scopus (130) Google Scholar, 2Wolfe J.M. Cave K.R. The psychophysical evidence for a binding problem in human vision.Neuron. 1999; 24 (111–125): 11-17Abstract Full Text Full Text PDF PubMed Scopus (151) Google Scholar, 3Stromeyer 3rd, C.F. Contour-contingent color aftereffects: retinal area specificity.Am. J. Psychol. 1972; 85: 227-235Crossref PubMed Scopus (27) Google Scholar, 4Mayhew J.E.W. Anstis S.M. Movement after-effects contingent on color, intensity and pattern.Percept. Psychophys. 1972; 12: 77-85Crossref Scopus (103) Google Scholar, 5Blaser E. Papathomas T. Vidnyánszky Z. Binding of motion and colour is early and automatic.Eur. J. Neurosci. 2005; 21: 2040-2044Crossref PubMed Scopus (27) Google Scholar], visual features were superimposed and presented simultaneously. Neurons throughout the visual cortex are known to code multiple features [6Gegenfurtner K.R. Kiper D.C. Fenstemaker S.B. Processing of color, form, and motion in macaque area V2.Vis. Neurosci. 1996; 13: 161-172Crossref PubMed Scopus (165) Google Scholar]. Therefore, the observed binding effects could be due to the physical co-occurrence of features and the sensory representation of feature pairings. It is uncertain whether the mechanisms responsible for perceptual binding were actually recruited [7Di Lollo V. The feature-binding problem is an ill-posed problem.Trends Cogn. Sci. 2012; 16: 317-321Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar, 8Whitney D. Neuroscience: toward unbinding the binding problem.Curr. Biol. 2009; 19: R251-R253Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar]. To address this issue, we performed psychophysical and fMRI experiments to investigate the neural mechanisms of a steady-state misbinding of color and motion [9Wu D.A. Kanai R. Shimojo S. Vision: steady-state misbinding of colour and motion.Nature. 2004; 429: 262Crossref PubMed Scopus (61) Google Scholar], because feature misbinding is probably the most striking evidence for the active existence of the binding mechanisms [10Treisman A. Schmidt H. Illusory conjunctions in the perception of objects.Cognit. Psychol. 1982; 14: 107-141Crossref PubMed Scopus (875) Google Scholar]. We found that adapting to the color-motion misbinding generated the color-contingent motion aftereffect, as well as the color-contingent motion adaptation effect in visual cortex. Notably, V2 exhibited the strongest adaptation effect, which significantly correlated with the aftereffect across subjects. Furthermore, effective connectivity analysis using dynamic causal modeling showed that the misbinding was closely associated with enhanced feedback from V4 and V5 to V2. These findings provide strong evidence for active feature binding in early visual cortex and suggest a critical role of reentrant connections from specialized intermediate areas to early visual cortex in this process.