Reduced Theta-Band Power and Phase Synchrony during Explicit Verbal Memory Tasks in Female, Non-Clinical Individuals with Schizotypal Traits

Abstract

The study of non-clinical individuals with schizotypal traits has been considered to provide a promising endophenotypic approach to understanding schizophrenia, because schizophrenia is highly heterogeneous, and a number of confounding factors may affect neuropsychological performance. Here, we investigated whether deficits in explicit verbal memory in individuals with schizotypal traits are associated with abnormalities in the local and inter-regional synchrony of brain activity. Memory deficits have been recognized as a core problem in schizophrenia, and previous studies have consistently shown explicit verbal memory impairment in schizophrenic patients. However, the mechanism of this impairment has not been fully revealed. Seventeen individuals with schizotypal traits and 17 age-matched, normal controls participated. Multichannel event-related electroencephalograms (EEGs) were recorded while the subjects performed a continuous recognition task. Event-related spectral perturbations (ERSPs) and inter-regional theta-band phase locking values (TPLVs) were investigated to determine the differences in local and global neural synchrony between the two subject groups. Additionally, the connection patterns of the TPLVs were quantitatively analyzed using graph theory measures. An old/new effect was found in the induced theta-band ERSP in both groups. However, the difference between the old and new was larger in normal controls than in schizotypal trait group. The tendency of elevated old/new effect in normal controls was observed in anterior-posterior theta-band phase synchrony as well. Our results suggest that explicit memory deficits observed in schizophrenia patients can also be found in non-clinical individuals with psychometrically defined schizotypal traits.

Fig 1. Event-related spectral perturbation (ERSP) in the theta band.

Time-frequency activation patterns for the 1–60 Hz signal for the new and old words and the contrast between them (old-new) for the (a) schizotypal trait group and (b) control group. Each ERSP map was obtained by averaging the ERSPs at three central electrodes (C3, Cz, and C4). The rightmost panels show the time courses of the averaged induced TBA (averaged from 4–7 Hz) for the new and old words (***: p<0.005, *: p<0.05, post hoc pairwise comparison with FDR correction). The induced TBA started to increase at ~100 ms and peaked at ~400–500 ms post-stimulus. Prominent differences in the induced TBA between the old and new words were observed throughout the five 100 ms time intervals over the period from 250 to 750 ms in both groups. However, the difference in TBA between the old and new words was altered at ~650 ms. (The old words elicited higher TBA at 250–650 ms but lower TBA at 650–750 ms compared to the new words.) As the contrast ERSP maps (3^rd columns) show, during the 250–550 ms interval, a prominent old/new difference was observed in both groups. However, the difference seemed to be much weaker for the schizotypal trait group, as indicated by the red arrows.

Fig 2. Topographical distributions of theta-band activity (TBA).

Topographical maps of induced TBA for the new and old words and the contrast between them (old-new) during the 350–450 and 650–750 ms intervals in the (a) schizotypal trait and (b) control groups. The induced TBA was centered in the frontocentral region. The largest old/new difference was observed in the frontocentral area during an early period (350–450 ms) and in the frontal and parietal areas during later periods (650–750 ms).

Fig 3. Inter-regional theta-band PLVs (TPLVs).

Spatiotemporal pattern of TPLVs for the new and old words for (a) the schizotypal trait group and (b) the control group. Red: significant TPLVs between anterior and posterior regions (the Fp1, Fp2, F7, F3, Fz, F4, F8, T5, P3, Pz, P4, T6, O1, Oz, and O2 electrodes were used); gray: among other regions. The time (in ms) written below each map indicates the 100 ms interval from which the TPLV was calculated. The right panels show the time courses of the mean number of significant connections across subjects within each group (error bar: standard error). In both groups, the most apparent old/new difference in the TPLVs occurred during the 250–550 ms interval, when the old words elicited higher TPLVs than the new words (*: p<0.05, ***: p<0.005).

Fig 4. The network small-worldness (S) of the theta-band phase locking value (TPLV) maps as a function of degree (K).

(a) The schizotypal trait and (b) control groups. Blue solid line: new word. Red dotted line: old word. Shaded area: standard error. Based on the dual-process model of recognition memory, we focused on networks during the two temporal intervals related to ‘familiarity’ and ‘recollection’ processing (i.e., the 250–550 and 550–750 ms intervals, respectively). Within each group, the S values for the old and new words were statistically compared at each K from 3 to 7. During the 250–550 ms period, both groups did not reveal that any S was significantly higher for the old words than for the new words at several degrees (Ks; between 3 and 5) only in the control group (▼: p<0.05 by paired-sample t-test). The optimal K was defined as 3.3, which showed the largest difference between the two types of words. However, the schizotypal trait group did not show a significant old/new effect in S at any K during the 550–750 ms period.