The Spatiotemporal Dynamics of Illusory Contour Processing: Combined High-Density Electrical Mapping, Source Analysis, and Functional Magnetic Resonance Imaging

Department of Psychiatry & Behavioral Sciences, Albert Einstein College of Medicine, New York, New York, United States
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 07/2002; 22(12):5055-73.
Source: PubMed


Because environmental information is often suboptimal, visual perception must frequently rely on the brain's reconstruction of contours absent from retinal images. Illusory contour (IC) stimuli have been used to investigate these "filling-in" processes. Intracranial recordings and neuroimaging studies show IC sensitivity in lower-tier area V2, and to a lesser extent V1. Some interpret these data as evidence for feedforward processing of IC stimuli, beginning at lower-tier visual areas. On the basis of lesion, visual evoked potentials (VEP), and neuroimaging evidence, others contend that IC sensitivity is a later, higher-order process. Whether IC sensitivity seen in lower-tier areas indexes feedforward or feedback processing remains unresolved. In a series of experiments, we addressed the spatiotemporal dynamics of IC processing. Centrally presented IC stimuli resulted in early VEP modulation (88-100 msec) over lateral-occipital (LOC) scalp--the IC effect. The IC effect followed visual response onset by 40 msec. Scalp current density topographic mapping, source analysis, and functional magnetic resonance imaging results all localized the IC effect to bilateral LOC areas. We propose that IC sensitivity described in V2 and V1 may reflect predominantly feedback modulation from higher-tier LOC areas, where IC sensitivity first occurs. Two additional observations further support this proposal. The latency of the IC effect shifted dramatically later (approximately 120 msec) when stimuli were laterally presented, indicating that retinotopic position alters IC processing. Immediately preceding the IC effect, the VEP modulated with inducer eccentricity--the configuration effect. We interpret this to represent contributions from global stimulus parameters to scene analysis. In contrast to the IC effect, the topography of the configuration effect was restricted to central parieto-occipital scalp.

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Available from: John J Foxe
    • "While lower-level visual areas with feed-forward driven signals may be able to preserve the given frequency tag, the feedback projections from higher-level visual areas to lower-level areas with longer latencies may disturb the synchrony of the higher frequency signals more. This feedback might be critical for illusory surface perception, as discussed in the introduction , with the higher-level signaling the overall configuration of the image while the lower-level articulates the position and orientation of the illusory contours (Cox et al., 2013; Lee & Nguyen, 2001; Mendola et al., 1999; Murray et al., 2002; Stanley & Rubin, 2003). Thus, using lower frequency tags for elements as used here may help eliciting IM components. "
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    ABSTRACT: The human visual system integrates separate visual inputs into coherently organized percepts, going beyond the information given. A striking example is the perception of an illusory square when physically separated inducers are positioned and oriented in a square-like configuration (illusory condition). This illusory square disappears when the specific configuration is broken, for instance, by rotating each inducer (non-illusory condition). Here we used frequency tagging and electroencephalography (EEG) to identify an objective neural signature of the global integration required for illusory surface perception. Two diagonal inducers were contrast-modulated at different frequency rates f1 and f2, leading to EEG responses exactly at these frequencies over the occipital cortex. Most importantly, nonlinear intermodulation (IM) components (e.g., f1 + f2) appeared in the frequency spectrum, and were much larger in response to the illusory square figure than the non-illusory control condition. Since the IMs reflect long-range interactions between the signals from the inducers, these data provide an objective (i.e., at a precise and predicted EEG frequency) signature of neural processes involved in the emergence of illusory surface perception. More generally, these findings help to establish EEG frequency-tagging as a highly valuable approach to investigate the underlying neural mechanisms of subjective Gestalt phenomena in an objective and quantitative manner, at the system level in humans.
    No preview · Article · Apr 2016 · Brain and Cognition
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    • "Higher-order visual cortex substrates for IC sensitivity are thus also supported by the progressive increase in neural receptive field size and interhemispheric connectivity across visual cortices from V1 through to the LOC (Smith et al., 2001; see also Box 3 inMurray and Herrmann, 2013). While prior work would indicate that placing all of the inducer elements within one visual hemifield delays the IC effect by approximately 120ms (Brandeis and Lehmann, 1989;Murray et al., 2002), it may be possible to further dissociate circuits for IC sensitivity by capitalising on knowledge concerning photoreceptor distribution across the peripheral retina where it may be more readily possible to target rod-driven IC effects (Ahnelt, 1998). More generally, the current findings enrich the extant literature in several important ways. "
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    ABSTRACT: Objects’ borders are readily perceived despite absent contrast gradients, e.g. due to poor lighting or occlusion. In humans, a visual evoked potential (VEP) correlate of illusory contour (IC) sensitivity, the “IC effect”, has been identified with an onset at ~90ms and generators within bilateral lateral occipital cortices (LOC). The IC effect is observed across a wide range of stimulus parameters, though until now it always involved high-contrast achromatic stimuli. Whether IC perception and its brain mechanisms differ as a function of the type of stimulus cue remains unknown. Resolving such will provide insights on whether there is a unique or multiple solutions to how the brain binds together spatially fractionated information into a cohesive perception. Here, participants discriminated IC from no-contour (NC) control stimuli that were either comprised of low-contrast achromatic stimuli or instead isoluminant chromatic contrast stimuli (presumably biasing processing to the magnocellular and parvocellular pathways, respectively) on separate blocks of trials. Behavioural analyses revealed that ICs were readily perceived independently of the stimulus cue – i.e. when defined by either chromatic or luminance contrast. VEPs were analysed within an electrical neuroimaging framework and revealed a generally similar timing of IC effects across both stimulus contrasts (i.e. at ~90ms). Additionally, an overall phase shift of the VEP on the order of ~30ms was consistently observed in response to chromatic vs. luminance contrast independently of the presence/absence of ICs. Critically, topographic differences in the IC effect were observed over the ~110-160ms period; different configurations of intracranial sources contributed to IC sensitivity as a function of stimulus contrast. Distributed source estimations localized these differences to LOC as well as V1/V2. The present data expand current models by demonstrating the existence of multiple, cue-dependent circuits in the brain for generating perceptions of illusory contours.
    Full-text · Article · Jan 2016 · NeuroImage
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    • "In addition, event-related potentials (ERPs) provide a complementary view of the temporal processing dynamics of illusory-figure processing and a means to investigate how pre-selective global shape integration influences subsequent attentional processing stages. ERPs in response to illusory figures start to differ in the time range of the posterior N1, which is typically enhanced for Kanizsa figures compared to local-level baseline configurations (e.g., Herrmann and Bosch, 2001; Murray, Foxe, Javitt, & Foxe, 2004; Proverbio and Zani, 2002; Senkowski, Röttger, Grimm, Foxe, & Herrmann, 2005; see Murray et al., 2002, for even earlier effects). In accordance with the imaging literature, the global-local N1 effect has been interpreted to reflect global shape processing in the LOC (He, Fan, Zhou, & Chen, 2004; Martinez, Ramanathan, Foxe, Javitt, & Hillyard, 2007; Murray, Imber, Javitt, & Foxe, 2006). "
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    ABSTRACT: Visual selection of illusory 'Kanizsa' figures, an assembly of local elements that induce the percept of a whole object, is facilitated relative to configurations composed of the same local elements that do not induce a global form - an instance of 'global precedence' in visual processing. Selective attention, i.e., the ability to focus on relevant and ignore irrelevant information, declines with increasing age; however, how this deficit affects selection of global vs. local configurations remains unknown. On this background, the present study examined for age-related differences in a global-local task requiring selection of either a 'global' Kanisza- or a 'local' non-Kanisza configuration (in the presence of the respectively other configuration) by analyzing event-related lateralizations (ERLs). Behaviorally, older participants showed a more pronounced global-precedence effect. Electrophysiologically, this effect was accompanied by an early (150-225ms) 'positivity posterior contralateral' (PPC), which was elicited for older, but not younger, participants, when the target was a non-Kanizsa configuration and the Kanizsa figure a distractor (rather than vice versa). In addition, timing differences in the subsequent (250-500ms) posterior contralateral negativity (PCN) indicated that attentional resources were allocated faster to Kanisza, as compared to non-Kanisza, targets in both age groups, while the allocation of spatial attention seemed to be generally delayed in older relative to younger age. Our results suggest that the enhanced global-local asymmetry in the older age group originated from less effective suppression of global distracter forms on early processing stages - indicative of older observers having difficulties with disengaging from a global default selection mode and switching to the required local state of attentional resolution.
    Full-text · Article · Oct 2015 · Biological Psychology
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