Dysfunctional cortical connectivity during the auditory oddball task in patients with schizophrenia

Abstract

Background: We studied the imaginary coherence (IC) of gamma frequency oscillations between brain regions of male schizophrenia patients during an auditory oddball task using magnetoencephalography (MEG) and electroencephalography (EEG).

Methods: Subjects were 10 right-handed male schizophrenia patients, evaluated by the positive and negative symptom scale (PANSS), and 10 healthy controls. Functional connectivity during the auditory oddball task was reconstructed in low (30-50 Hz) and high (50-100 Hz) gamma bands, and represented by imaginary coherence (IC) based on significant oscillatory power changes. We calculated correlations between PANSS scores and IC.

Results: In the high gamma band, IC between left occipital and right prefrontal lobe areas during the time window 750-1000 ms from stimulus onset showed negative correlations with total negative scores, total positive scores, the sum of positive and negative scores in PANSS, conceptual disorganization, and social avoidance scores. In the low gamma band, IC between the same areas from 250-500 ms also showed a negative correlation with the conceptual disorganization score. In the same time window, IC between left occipital and right frontoparietal lobe areas in the low gamma band showed a positive correlation with hallucinatory behavior; IC between right temporal pole and left prefrontal lobe areas showed a positive correlation with delusion scores, although these ICs were decreased relative to controls.

Conclusions: Functional disconnection of high and low gamma bands in auditory oddball task may play an important role in the auditory processing in schizophrenia patients.

Keywords: Magnetoencephalography; P300.; PANSS; functional connectivity; gamma band; schizophrenia.

Fig. (1)

MEG examination shows deviation of ERD power corresponding to target stimuli in the low (30-50 Hz) and high (50-100 Hz) gamma bands in patients with schizophrenia compared to normal controls (A paired test, FWE p < 0.005). A: Low gamma ERD (30-50 Hz) power is significantly decreased in the right inferior temporal and a small area on the left of the midline frontal lobes at 0-250 ms. B: Low gamma ERD power is significantly decreased in the left midline dorsal frontal area, a bilateral small midline parietofrontal area, and a small area of the left upper temporal lobes at 250-500 ms. C: High gamma ERD (50-100 Hz) power was significantly decreased in a small area of the left occipital lobe at 500-750 ms.

Fig. (2)

MEG examination shows decreased imaginary coherence (IC) between seeds and target areas in the brain during the auditory oddball task (FWE: p0.05) for each of four time windows. A-D: low gamma band. E-H: high gamma band. A. IC decreases can be seen in low the gamma band between left midline dorsal frontal (seeds: L. MDF) and right occipital (targets: R O) areas and between right inferior temporal (seeds: R. IT) and left lateral prefrontal (targets: L. LP) areas from 0-250 ms. B. For the low gamma band, no IC decreases can be seen during the 250-500 ms time window. C. IC decreases can be seen in the low gamma band between left occipital (seeds; L. O) and right midline frontal (targets: R. MF) areas (500-750 ms). D: 750-100 ms time window. IC decreases in the low gamma band are seen between left occipital (seeds: L. O) and right frontoparietal (targets; R. FP); between left occipital (seeds: L. O) and right occipital (targets: R. O); between left midline dorsal frontal (seeds: L. MDF) and right lateral temporal (targets: R. LT); and between right inferior temporal (seeds: R. IT) and left midline frontal (targets: L MF) areas. E: IC decreases can be seen in the high gamma band between the left midline dorsal frontal (seeds: L. MDF) and right occipital (targets: R.O) areas during the 0-250 ms window. F: IC decreases can be seen in the high gamma band between left occipital (seeds: L. O) and right lateral prefrontal (targets R. LPF) areas from 250-500 ms. G: IC decreases can be seen in the high gamma band between right inferior temporal (seeds; R. IT) and right occipital (targets; R. O) areas from 500-750 ms. H: IC decreases can be seen in the high gamma band between left occipital (seeds; L. O) and right anterior prefrontal (targets: R. APF) areas, between left occipital (seeds: Lt. O) and right frontoparietal (targets; R. FP) areas during 750-1000 ms.

Fig. (3)

Correlation coefficients between PANSS scores IC in the high gamma band (50-100 Hz) during the auditory oddball task. Only significant correlations are shown. A. IC between left occipital lobe (L. O) (seeds; MNI: X=-13, Y=-98, Z=26) and right lateral prefrontal lobe (R. LPF) areas (targets) was measured in the high gamma band during the 750-1000 ms window. This IC was used for all correlations in this figure. B. Conceptual disorganization scores and IC (r=-0.701; p=0.024). C. Active social avoidance in PANSS scores and IC (r=-0.807; p=0.005). D: Sum of positive scale scores in PANSS and IC (r=-0.715; p =0.02). E: Sum of negative scale scores in PANSS and IC (r=-0.724; p =0.018). F: Sum of negative and positive scale scores in PANSS and IC (r=-0.773; p =0.009).

Fig. (4)

Correlation coefficients between hallucinatory behavior IC in the low gamma band during the auditory oddball task. A. IC between left occipital (L. O) (seeds in MNI coordinates: X=- 13, Y=-98, Z=26) and right lateral prefrontal lobe (targets: R. LPF) areas are measured in the low gamma band during 250-500 ms. B: Conceptual disorganization and IC (r=-0.706; p =0.023).

Fig. (5)

Correlation coefficients between hallucinatory behavior scores and IC in the low gamma band during the auditory oddball task. A. IC between left occipital (L. O) (seeds in MNI coordinates: X=- 13, Y=-98, Z=26) and right frontoparietal (targets: R. FP) lobe areas during the time window from 500-750ms. B. Positive correlation between hallucinatory behavior and IC. (r=0.666; p =0.035).

Fig. (6)

Correlation coefficients between delusion and IC in the low gamma band during the auditory oddball task. A. IC between right inferior temporal pole (R. IT) (seeds in MNI coordinates: X=50, Y=14, Z=-32) and left lateral prefrontal (targets: L. LP) lobe areas are measured during 0-250 ms. B. Positive correlation between delusion and IC between right temporal pole and left prefrontal lobe areas (r=0.655 p=0.04).