Delta EEG band as a marker of left hypofrontality for language in schizophrenia patients

Abstract

Frontal hypoactivation has consistently been demonstrated in schizophrenia patients. We hypothesized that this well-known deficit is asymmetrical, ie, centered over left frontal locations and, in-line with Crow's theory, associated with both loss of linguistic asymmetry and correlated with positive symptoms. Electroencephalography delta band was used as a quantitative index of cortical inhibition in 17 paranoid schizophrenia patients with prevailing positive symptoms and 17 matched control subjects. Delta amplitude was measured by 38 electrodes, while participants performed 3 linguistic tasks, visuoperceptual, rhyming, and semantic judgment. Compared with control subjects, patients did not show overall delta band differences, revealing no detrimental effects of pharmacological treatment. In healthy participants, analysis of 4 quadrants/regions of interest revealed higher delta amplitude in right vs left anterior sites, indicating significant left anterior disinhibition during linguistic processing. Instead, patients showed bilateral delta band distribution and, compared with control subjects, significant greater delta amplitude (ie, brain inhibition) in linguistic left anterior centers. Patients' left hypofrontality was functionally related to their lack of hemispheric specialization for language and was positively correlated with higher levels of delusions (P1) and conceptual disorganization (P2) Positive and Negative Syndrome Scale subscales. Results suggest, in schizophrenia patients, a functional deficit of Broca's area, a region playing a fundamental hierarchical role between and within hemispheres by integrating many basic processes in linguistic and conceptual organization. The significant correlation between lack of anterior asymmetry and increased positive symptoms is in-line with Crow's hypothesis postulating the etiological role of disrupted linguistic frontal asymmetry on the onset of the key symptoms of schizophrenia.

Fig. 1.

Response Time Analysis (a) Showed Significant Main Effects of Group and Task Factors. Error rate analysis (b) revealed 2-way group-by-task interaction. Asterisks indicate significant post hoc comparisons.

Fig. 2.

Spline Maps of Differences Between Delta Percentage Values for Control Subjects and Patients. Dark levels, patients' greater delta activity; clear levels, control subjects' higher delta activity. Panels: left, orthographic task; central, phonological task; and right, semantic task.

Fig. 3.

Delta Band Analysis: Significant 3-Way Group-by-Region-by-Laterality Interaction. Control subjects’ and patients' delta distributions (black and dotted lines, respectively) are shown for anterior (left panel) and posterior brain regions (right panel). Asterisks indicate significant post hoc comparisons.

Fig. 4.

Delta Band Analysis: Significant 4-Way Group-by-Task-by-Region-by-Laterality Interaction. (a) Orthographic, (b) phonological, and (c) semantic tasks in control subjects (black line) and schizophrenia patients (dotted black line) in anterior (left) and posterior sites (right).

Fig. 5.

Pearson Correlations Between First Construct (P1) of Positive Subscale of the Positive and Negative Syndrome Scale (Delusions) and Delta Anterior Laterality (Left Minus Right Delta Amplitude) in Orthographic (Black Squares), Phonological (Dark Gray Circles), and Semantic Tasks (Light Gray Triangles).