Impaired Visual Object Processing Across an Occipital-Frontal-Hippocampal Brain Network in Schizophrenia

Abstract

Background Perceptual closure refers to the ability to identify objects with partial information. Deficits in schizophrenia are indexed by impaired generation of the closure-related negativity (NCL) from ventral stream visual cortex (lateral occipital complex, LOC), as part of a network of brain regions that also includes dorsal stream visual regions, prefrontal cortex (PFC) and hippocampus. This study evaluates network-level interactions during perceptual closure in schizophrenia using parallel ERP, fMRI and neuropsychological assessment. Methods ERP were obtained from 24 patients and 20 healthy volunteers in response to fragmented (closeable) and control scrambled (noncloseable) line drawings. fMRI were obtained from 11 patients and 12 controls. Patterns of between group differences for predefined ERP components and fMRI regions of interest were determined using both analysis of variance and structural equation modeling. Global neuropsychological performance was assessed using elements of the WAIS-III, WMS-III and MATRICS batteries. Results Patients showed impaired visual P1 generation, reflecting dorsal stream dysfunction, along with impaired generation of NCL components over PFC and LOC. In fMRI, patients showed impaired activation of dorsal and ventral visual regions, PFC and hippocampus. Impaired activation of dorsal stream visual regions contributed significantly to impaired PFC activation. Impaired PFC activation contributed significantly to impaired activation of hippocampus and LOC. Impaired LOC and hippocampal activation contributed significantly to deficits on WAIS-III Perceptual Organization Index (POI) and other tests of impaired perceptual processing in schizophrenia. Conclusion Schizophrenia is associated with severe activation deficits across a distributed network of sensory and higher order cognitive regions. Deficit in early visual processing within the dorsal visual stream contributes significantly to impaired frontal activation which, in turn, leads to dysregulation of hippocampus and ventral visual stream. Dysfunction within this network underlies impairment in more traditional measures of neurocognitive dysfunction such as POI, supporting distributed models of brain dysfunction in schizophrenia.

Neural activity during object perception in schizophrenia patients is associated with illness duration and affective symptoms

“…When this factor was controlled for, significant cluster level activation in the left and right middle occipital gyrus was observed in patients. Illness duration might similarly contribute to the under-activation or alteration of the lateral occipital complex and visual cortex reported in this population (Green et al, 2009;Schultz et al, 2013;Sehatpour et al, 2010;Silverstein et al, 2009). Our findings highlight the importance of considering the number of years suffering the disease as a potential cause of decreased brain activation in schizophrenia.…”

“…This area is involved in object perception and recognition (Cichy et al, 2012;Grill-Spector et al, 2001;Macevoy, 2013). Alterations were also observed in various areas of the visual cortex (Schultz et al, 2013;Sehatpour et al, 2010;Silverstein et al, 2009). At the clinical level, visual abnormalities in patients with schizophrenia have been related to negative symptomatology (Bedwell et al, 2011;Green et al, 2011;Lee et al, 2010;Perez et al, 2012;Slaghuis and Curran, 1999).…”

The 5-HT2A/1A Agonist Psilocybin Disrupts Modal Object Completion Associated with Visual Hallucinations

“…In some previous studies the presentation of Kanizsa-figures, compared to control figures, have additionally been associated with an enhancement of the earlier P1 (26) and the subsequent closure negativity (N cl ) component (22). However, as the N cl component is more reliably induced by more complex fragmented images and reflects successful recognition of complex images (27,28) it is unlikely to be as relevant to the processing of the simple Kanizsa-figures used in the current experiment.…”

Has an Angel Shown the Way? Etiological and Therapeutic Implications of the PCP/NMDA Model of Schizophrenia

“…In the auditory system, structural and functional disturbances at the level of primary auditory cortex correlate with impairments in higher auditory auditory function such as auditory emotion recognition 73 (A). In the visual system, deficits in early visual activation lead to impairments in frontal activation during tasks such as perceptual closure 40 (B) or AX-type continuous performance task (C) 41 performance.…”