An event-related potential examination of contour integration deficits in schizophrenia

Abstract

Perceptual organization, which refers to the ability to integrate fragments of stimuli to form a representation of a whole edge, part, or object, is impaired in schizophrenia. A contour integration paradigm, involving detection of a set of Gabor patches forming an oval contour pointing to the right or left embedded in a field of randomly oriented Gabors, has been developed for use in clinical trials of schizophrenia. The purpose of the present study was to assess contributions of early and later stages of processing to deficits in contour integration, as well as to develop an event-related potential (ERP) analog of this task. Twenty-one patients with schizophrenia and 28 controls participated. The Gabor elements forming the contours were given a low or high degree of orientational jitter, making it either easy or difficult to identify the direction in which the contour was pointing. ERP results showed greater negative peaks at ~165 (N1 component) and ~270 ms for the low-jitter versus the high-jitter contours, with a much greater difference between jitter conditions at 270 ms. This later ERP component was previously termed Ncl for closure negativity. Source localization identified the Ncl in the lateral occipital object recognition area. Patients showed a significant decrease in the Ncl, but not N1, compared to controls, and this was associated with impaired behavioral ability to identify contours. In addition, an earlier negative peak was found at ~120 ms (termed N120) that differentiated jitter conditions, had a dorsal stream source, and differed between patients and controls. Patients also showed a deficit in the dorsal stream sensory P1 component. These results are in accord with impairments in distributed circuitry contributing to perceptual organization deficits and provide an ERP analog to the behavioral contour integration task.

The time course of pattern discrimination in the human brain

“…Executing of this task suggests activation of mechanisms of visual integration by grouping spatially integrated elements into a global structure rather than discrimination of the local features as in the Collinearity task. A similar increase in the negative wave of ERP in this time window was observed when a global Gabor contour was embedded in an array of randomly oriented Gabor patches (Butler et al, 2013;Machilsen, Novitskiy, Vancleef, & Wagemans, 2011;Shpaner, Molholm, Forde, & Foxe, 2013). An increase in the N1-amplitude peaking $100-170 ms after stimulus onset is also often found when participants observe an illusory contour such as a Kanizsa square which is associated with the emergence of a global shape (Herrmann & Bosch, 2001;Murray et al, 2002;Proverbio & Zani, 2002).…”

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

“…Performance is normal when perceptual organization can be easily achieved by pre-specified feature hierarchies. Perceptual organization impairments in schizophrenia have been demonstrated using fMRI (showing reduced activation in occipital areas regions sensitive to grouping but normal V1 activity; Silverstein et al, 2009), event related potentials such as closure negativity (Ncl; Butler et al, 2013), and EEG measures such as gamma power and gamma synchrony (reviewed in Uhlhaas & Singer, 2010. A version of the contour integration paradigm in which figure-ground segregation is cued by onset asynchrony also shows that both schizophrenia and schizotypy are associated with substantially reduced temporal resolution at gamma frequencies (Hancock et al, 2008).…”

Cortical contributions to impaired contour integration in schizophrenia

“…With the JOVI and other similar CI tasks, studies have shown that people with schizophrenia are less able to detect and make shape judgments about fragmented contours when compared to various healthy and psychiatric control groups (Butler et al, 2013; Feigenson, Keane, Roche, & Silverstein, 2014; Keane, Erlikhman, Kastner, Paterno, & Silverstein, 2014; Keane et al, 2012; Kozma-Weibe et al, 2006; Schallmo, Sponheim, & Olman, 2013a, 2013b; Schenkel, Spaulding, DiLillo, & Silverstein, 2005; Schenkel, Spaulding, & Silverstein, 2005; Silverstein et al, 2009; Silverstein et al, 2006; Silverstein et al, 2012; Silverstein, Kovacs, Corry, & Valone, 2000; Uhlhaas, Phillips, Schenkel, & Silverstein, 2006; Uhlhaas, Phillips, & Silverstein, 2005). Past CI studies in schizophrenia have also demonstrated that, while performance does not vary from the acute to stabilization phases of illness in briefly hospitalized (i.e., ~2 weeks) patients (Feigenson et al, 2014), it becomes worse with longer illness chronicity and a lower level of functioning (Schenkel, Spaulding, & Silverstein, 2005; Silverstein et al, 2006; Uhlhaas et al, 2005).…”

“…Despite the many demonstrations of CI impairment in schizophrenia, exploration of its brain bases has been limited to one ERP study of closure negativity (Ncl) (Butler et al, 2013) and one fMRI study (Silverstein et al, 2009). Both of these identified reduced processing, compared to healthy controls, in visual regions known to subserve CI, based on prior studies from healthy humans and monkeys (Altmann, Bulthoff, & Kourtzi, 2003; Kourtzi, Tolias, Altmann, Augath, & Logothetis, 2003; Volberg & Greenlee, 2014) [e.g., V2, V3, V4, lateral occipital complex (LOC)].…”