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Functional Neuroimaging Findings on the Human Perception of Illusory Neuroscience and Biobehavioral Reviews 30 (2006) 595–612 www.elsevier.com/locate/neubiorev Review Functional neuroimaging findings on the human perception of illusory contours M.L. Seghier a,b,*, P. Vuilleumier a,c a Laboratory for Neurology and Imaging of Cognition, Clinic of Neurology and Department of Neurosciences, University Medical Center of Geneva, Michel-Servet 1, Geneva 1211, Switzerland b Department of Radiology, University Hospital of Geneva (HUG), Micheli-du-Crest 24, 1211 Geneva, Switzerland c Department of Psychology, University of Geneva, Geneva, Switzerland Received 31 January 2005; received in revised form 14 September 2005; accepted 21 November 2005 Abstract Illusory contours (IC) have attracted a considerable interest in recent years to derive models of how sensory information is processed and integrated within the visual system. In addition to various findings from neuropsychology, neurophysiology, and psychophysics, several recent studies have used functional neuroimaging to identify the cerebral substrates underlying human perception of IC (in particular Kanizsa figures). In this paper, we review the results from more than 20 neuroimaging studies on IC perception and highlight the great diversity of findings across these studies. We then provide a detailed discussion about the localization (‘where’ debate) and the timing (‘when’ debate) of IC processing as suggested by functional neuroimaging. Cortical responses involving visual areas as early as V1/V2 and latencies as rapid as 100 ms have been reported in several studies. Particular issues concerning the role of the right hemisphere and the retinotopic encoding of IC are also discussed. These different findings are tentatively brought together to propose different hypothetical cortical mechanisms that might be responsible for the visual formation of IC. Several remaining questions on IC processing that could potentially be explored with functional neuroimaging techniques are finally emphasized. q 2005 Elsevier Ltd. All rights reserved. Keywords: Illusory contours; Kanizsa figure; Functional neuroimaging; Visual areas; V1; V2; LOC; Segmentation and grouping mechanisms; Feedback connections; Low and high level vision Contents 1. Introduction .................................................................................... 596 2. Methodological issues ............................................................................. 598 2.1. Imaging techniques .......................................................................... 598 2.2. Data analysis methods ........................................................................ 598 2.3. The subject factor ........................................................................... 599 2.4. Stimuli ................................................................................... 599 3. IC processing: The ‘where’ debate .................................................................... 600 3.1. V1/V2 areas . .............................................................................. 600 3.2. The lateral occipital complex (LOC) ............................................................. 602 3.3. Other cortical regions ........................................................................ 603 3.4. Retinotopy of IC ............................................................................ 603 3.5. IC perception and the right hemisphere ........................................................... 604 4. IC processing: The ‘when’ debate .................................................................... 604 * Corresponding author. Address: Department of Radiology, University Hospital of Geneva (HUG), Micheli-du-Crest 24, 1211 Geneva, Switzerland. Tel.: C41 22 379 5361; fax: C41 22 372 7072. E-mail address: [email protected] (M.L. Seghier). 0149-7634/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2005.11.002 596 M.L. Seghier, P. Vuilleumier / Neuroscience and Biobehavioral Reviews 30 (2006) 595–612 5. Possible mechanisms inferred from neuroimaging findings .................................................. 605 5.1. The fast-local low-level mechanism .............................................................. 605 5.2. The late-global high-level mechanism ............................................................ 606 5.3. Beyond the occipital lobe ..................................................................... 606 6. Remaining questions .............................................................................. 607 Acknowledgements ............................................................................... 608 References . .................................................................................. 608 1. Introduction Watanabe and Oyama, 1988) have attempted to elucidate the mystery of ‘human perception of illusory contours with real The segregation of sensory visual inputs into coherent neurons’ (Westheimer, 1994). According to Halpern (1981),at objects is one of the essential operations carried out by the least eight different hypotheses have been proposed to explain visual system. This process requires the identification of the perception of illusory contours. Among phenomenological borders between different components and surfaces, as well as approaches, the ‘cues-to-depth’ hypothesis suggests that IC the selection and grouping of individual visual elements in a might be perceived as an elevated surface plane above the complex scene. Differences in luminance, texture, and/or background plane generated by visual inducers, as can be chrominance are the major cues used to define object boundary. apparent when observers use the monocular depth cue of These real boundaries are physically present in the scene and perceived interposition (Coren, 1972; Coren and Porac, 1983). very efficiently identified by the visual system. Behaviorally, On the other hand, the ‘object-cue’ hypothesis or the the time needed to identify such contours may be as short as ‘cognitive’ model argues that IC might be perceived on the 50 ms (Werner, 1935). On the other hand, contours can also be basis of inferences that the observer can make about objects perceived in the absence of ‘real’ physical discontinuity and their spatial relationships in the world (Gregory, 1972; (Ginsburg, 1975; Petry and Meyer, 1987). These contours are Piggins, 1975; Rock and Anson, 1979). Another phenomen- usually called illusory contours (IC), but have also been ological account is based on the ‘Gestalt completion’ referred to using many other names, including subjective hypothesis that suggests an important role of illusory surface contours, phenomenal contours, cognitive contours, anomalous perception, with a secondary completion of the perceived contours, quasiperceptive contours, unfinished contours, surface by forming transitions and contours (Kanizsa, 1976). In incomplete contours, virtual contours, contours without addition, two main categories of explanations have been gradients, and apparent contours (for additional details, see proposed on the basis of physiological hypotheses. One is the Kanizsa, 1979; Petry and Meyer, 1987; Purghe´ and Coren, ‘brightness–contrast’ hypothesis which claims that IC for- 1992). mation is a consequence of the perception of brightness One class of illusory contours, called Kanizsa figures, can be differences between the illusory figure and its background generated by a particular configuration of distant high-contrast (Brigner and Gallagher, 1974; Jory and Day, 1979). The other borders, such as incomplete and co-aligned white (or black) is the ‘feature-edge detection’ hypothesis that gives a circles that induce the illusory perception of a dark (or light) preponderant role to orientation-specific units in the visual shape, placed over the white (or black) circles (Kanizsa, 1979). cortex, which might be triggered by real edges along the The perception of such figures arises very naturally and inducers and lead to illusory perception of contours beyond effortlessly although we are well aware that they are not real these real edges by propagation and interpolation processes (e.g. Ware and Kennedy, 1978). This type of IC has attracted (Smith and Over, 1975, 1977). Note that sophisticated considerable interest in recent years and has been used to mathematical models have also been proposed to simulate derive influential models of how sensory information is the neural networks underlying the formation of IC according processed within the visual system, mostly in the perspective to these different perspectives (e.g. Brigner, 1982; Sarti et al., of constructive aspects of human vision (for review, see Purghe´ 2000). and Coren, 1992; Spillmann and Dresp, 1995; Zeki, 2004). In These accounts of IC have been extensively tested with particular, much interest has focused on visual mechanisms psychophysical experiments in healthy human subjects. involved in perceptual grouping and segmentation (Marr, Results have generally confirmed at least some validity of 1982). However, the cortical networks involved in such visual several of the different hypotheses, which seem able to processes are only beginning to be identified, as we review successfully explain a range of illusions and effects, although here. not necessarily all possible illusory figures. But the possibility Different functional hypotheses based on psychophysics to see IC in some cases without any appearance of visual have been put forward in the past to account for IC perception, occlusion (Purghe,
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