Neuronal oscillations form parietal/frontal networks during contour integration

Abstract

The ability to integrate visual features into a global coherent percept that can be further categorized and manipulated are fundamental abilities of the neural system. While the processing of visual information involves activation of early visual cortices, the recruitment of parietal and frontal cortices has been shown to be crucial for perceptual processes. Yet is it not clear how both cortical and long-range oscillatory activity leads to the integration of visual features into a coherent percept. Here, we will investigate perceptual grouping through the analysis of a contour categorization task, where the local elements that form contour must be linked into a coherent structure, which is then further processed and manipulated to perform the categorization task. The contour formation in our visual stimulus is a dynamic process where, for the first time, visual perception of contours is disentangled from the onset of visual stimulation or from motor preparation, cognitive processes that until now have been behaviorally attached to perceptual processes. Our main finding is that, while local and long-range synchronization at several frequencies seem to be an ongoing phenomena, categorization of a contour could only be predicted through local oscillatory activity within parietal/frontal sources, which in turn, would synchronize at gamma (>30 Hz) frequency. Simultaneously, fronto-parietal beta (13–30 Hz) phase locking forms a network spanning across neural sources that are not category specific. Both long range networks, i.e., the gamma network that is category specific, and the beta network that is not category specific, are functionally distinct but spatially overlapping. Altogether, we show that a critical mechanism underlying contour categorization involves oscillatory activity within parietal/frontal cortices, as well as its synchronization across distal cortical sites.

Cortical contributions to impaired contour integration in schizophrenia

“…In addition to disturbances in visual cortex, however, the one prior fMRI study of SCZ demonstrated reduced prefrontal cortex and parietal lobe processing in patients. These data are consistent with recent findings indicating that in addition to visual cortex, frontal-parietal connectivity and other mechanisms supporting higher-level top-down control are involved in contour integration and object processing (Castellano, Plochl, Vicente, & Pipa, 2014; Hanslmayr, Volberg, Wimber, Dalal, & Greenlee, 2013; Li, Piech, & Gilbert, 2008; Sun et al, 2012; Volberg, Wutz, & Greenlee, 2013). The CI data reviewed above are supported by data from studies of perceptual closure, where subjects view fragmented line drawings of familiar objects.…”

“…Parietal ROIs included: 1) the superior parietal lobules, which are involved in the distribution of visual-spatial attention and the binding of visual features (Robertson, 2003), and which were associated with reduced CI in schizophrenia in our past study (Silverstein et al, 2009); and 2) the angular gyrus, which is involved in integrating visual information with the verbal and spatial concepts of left and right during left-right discrimination (Hirnstein, Bayer, Ellison, & Hausmann, 2011; Seghier, 2013), a process essential for accurate JOVI performance. Frontal ROIs were the middle and inferior frontal gyri (including the pars triangularis and pars operculum regions), which are involved in perceptual organization and perceptual decision making (Ploran et al, 2007; Sun et al, 2012), as was recently shown using a CI task similar to the JOVI in healthy subjects in a study of neuronal oscillations (Castellano et al, 2014). …”

Synchronization of fronto-parietal beta and theta networks as a signature of visual awareness in neglect

“…Sutoyo and Srinivasan (2009) have elicited enhanced responses to conscious binding of congruent information from complementary hemi-fields into a coherent percept. Although their findings cannot be directly linked to the present results, they strongly imply that early beta synchronization is sensitive to the integration of visual information from the two hemi-fields (Mima et al, 2001;Phillips and Takeda, 2009;Phillips et al, 2012;Busch et al, 2004;Castellano et al, 2014). As indicated by the stimulus-type effect in controls, binding congruent information into a coherent fullfield percept is associated with stronger beta synchronization between right parietal and frontal regions, which, however, was specifically impaired in the N+ group (Fig.…”

“…Hipp et al (2011) have identified large scale beta synchronization in a distinctive network of frontal, parietal and extrastriate visual areas in relation to visual perceptual organization. Fronto-parietal synchrony in the beta band also has been associated with visual search (Buschman and Miller, 2007), integration of visual information and perceptual grouping (Srinivasan et al, 1999;Phillips and Takeda, 2009;Phillips et al, 2012;Volberg and Greenlee, 2014;Castellano et al, 2014), visual attention (Gross et al, 2004;Marois et al, 2000;Wróbel, 2000), and visual object recognition (Sehatpour et al, 2008;Castellano et al, 2014). These previous studies, however, point to the existence of ongoing fronto-parietal beta synchronization that modulates brain responses to visual input (Gross et al, 2004;Liang et al 2002;Hipp et al, 2011), or beta synchrony at later stages (150-300 ms) of visual stimulus processing (Phillips et al, 2012;Sehatpour et al, 2008;Dehaene and Changeux, 2011).…”

On the functions, mechanisms, and malfunctions of intracortical contextual modulation

“…For example, it has been shown that detection of the figure involves synchronization at gamma frequencies within early visual regions, whereas categorization of the orientation of the egg-shaped figure formed by the contour involves synchronization at beta frequencies across a network that includes frontal and parietal regions (Castellano et al, 2014).…”