Cue-Invariant Networks for Figure and Background Processing in Human Visual Cortex

Abstract

Lateral occipital cortical areas are involved in the perception of objects, but it is not clear how these areas interact with first tier visual areas. Using synthetic images portraying a simple texture-defined figure and an electrophysiological paradigm that allows us to monitor cortical responses to figure and background regions separately, we found distinct neuronal networks responsible for the processing of each region. The figure region of our displays was tagged with one temporal frequency (3.0 Hz) and the background region with another (3.6 Hz). Spectral analysis was used to separate the responses to the two regions during their simultaneous presentation. Distributed source reconstructions were made by using the minimum norm method, and cortical current density was measured in a set of visual areas defined on retinotopic and functional criteria with the use of functional magnetic resonance imaging. The results of the main experiments, combined with a set of control experiments, indicate that the figure region, but not the background, was routed preferentially to lateral cortex. A separate network extending from first tier through more dorsal areas responded preferentially to the background region. The figure-related responses were mostly invariant with respect to the texture types used to define the figure, did not depend on its spatial location or size, and mostly were unaffected by attentional instructions. Because of the emergent nature of a segmented figure in our displays, feedback from higher cortical areas is a likely candidate for the selection mechanism by which the figure region is routed to lateral occipital cortex.Key words: visual cortex; object processing; figure/ground; cue invariance; lateral occipital complex; source imaging IntroductionObject recognition mechanisms must be able to extract shape independently of the surface cues that are present. Local estimates of surface cues such as texture grain or orientation, although necessary as inputs to the recognition process, convey little sense of object shape. Rather it is the pattern of cue similarity across regions and cue discontinuity across borders that must be integrated to recover object shape.The process of cue-invariant shape processing begins at an early stage of visual cortex and extends deep into extrastriate cortex and the temporal lobe. Cue invariance first is seen as early as V2, where some cells have a similar orientation or direction tuning for borders defined by different feature discontinuities (Leventhal et al., 1998;Marcar et al., 2000;Ramsden et al., 2001;Zhan and Baker, 2006). At higher levels of the visual system, such as inferotemporal cortex (Sary et al., 1993) and medial superior temporal area (Geesaman and Andersen, 1996), cells show shape selectivity that is mostly independent of the defining cues and spatial position. Functional magnetic resonance imaging (fMRI) studies in humans have implicated homologous extrastriate regions, in particular the lateral occipital complex (LOC), as sites of category-specific, cue-...

The time course of shape discrimination in the human brain

“…The shape representation in the LOC is also tuned for small shape changes in the outline of objects (Gillebert et al, 2009;Panis et al, 2008). Our previous source-imaging studies using frequency tagging have suggested that the LOC is tuned for the configuration of a small figure on a larger background (Appelbaum et al, 2010) and that LOC responses to figures are largely cue-invariant (Appelbaum et al, 2006(Appelbaum et al, , 2012. Cue-invariance in LOC has also been found with fMRI (Grill-Spector et al, 1998).…”

“…In the interest of brevity, we provide an overview of these methods, and reference the reader to our previous work (Ales and Norcia, 2009;Appelbaum and Norcia, 2009;Appelbaum et al, 2006Appelbaum et al, , 2008 for a more a more detailed description.…”

“…Differences between the experimental conditions were identified by a permutation test based on methods devised by Blair and Karniski (1993) and described in detail in Appelbaum et al (2006). Briefly, the null hypothesis that no differences were present between experimental conditions was tested by making synthetic datasets in which the condition labels for an individual subject's data were randomly permuted.…”

The Selectivity of Task-Dependent Attention Varies with Surrounding Context

“…To test our hypothesis, we combined high-density electroencephalography (EEG) with anatomical and functional magnetic resonance imaging (fMRI) to characterize the population responses to these configurations in different regions of interest (ROIs; Appelbaum et al, 2006;Cottereau et al, 2011a,b). Observers were cued to attend to one of two target-surround stimuli that were presented to the left and right of fixation (Fig.…”

Perceiving the Tree in the Woods: Segregating Brain Responses to Stimuli Constituting Natural Scenes

“…The SSVEP, the oscillatory response of the cortex to a flickering stimulus with the same temporal frequency as the initiating stimulus, provides a continuous measure of cortical activation patterns related to the processing of a frequency-tagged stimulus (Mü ller and Hillyard, 2000). Importantly, stimuli presented at different driving frequencies (in our case, background and object) evoke unique and separable brain responses (Appelbaum et al, 2006). SSVEPs have been used to investigate fundamental visual processes (Nakayama and Mackeben, 1982), visual attention , and object recognition (Kaspar et al, 2010).…”