A working memory related mechanism of auditory hallucinations

Abstract

Cognitive mechanisms underlying auditory hallucinations (AH) in schizophrenia have been related to working memory (WM), although the formative mechanism is unknown. The phonological loop refers to subvocal rehearsals of information held online for supporting WM. As WM deficiency is frequent in schizophrenia, we hypothesized that AH and WM deficit share a common dysfunction in phonological loop operation, especially when it is taxed by ambiguous auditory and verbal associations. We developed an active phonological priming (APP) paradigm in which participants generated arbitrary verbal associations to pseudowords with ambiguous meaning. They were later asked to rate their familiarity to each pseudoword, a task that required subvocal evaluation of ambiguous auditory-verbal information. Factor and mediation analyses were used to test the hypothesis that WM, AH, and APP induced phonological bias toward perceiving ambiguous contents as familiar may share a common underlying mechanism. In 32 patients with schizophrenia (SZ) and 20 healthy controls (HC), SZ rated ambiguous pseudowords as significantly more familiar compared with HC (p = .006), indicating a proneness to APP-induced bias. This increased subjective bias to perceive ambiguous contents as familiar after APP significantly correlated with AH severity (p = .001) and mediated the relationship between WM and AH. Factor analysis demonstrated a common latent factor among WM, AH, and the bias induced by active priming to ambiguous contents. A heightened phonological loop priming to ambiguous contents appears to be mechanistically linked to WM deficits and AH in schizophrenia. These findings emphasize the importance of jointly addressing WM deficits and AH in clinical practice and research. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Fig. 1.

An illustration of the study paradigm with actual examples from participants. Top two rows: participants listened and immediately responded with an audible verbal association to a pseudo-randomized set of 100 words and 100 pseudo-words; these stimuli were then repeated and participants were asked to rate their familiarity to the words and the pseudo-words (1=not familiar; 2=somewhat familiar; 3=very familiar). Bottom two rows: participants engaged in a passive control task by listening to another set of pseudo-randomized 100 words and 100 pseudo-words without making any verbal responses; these stimuli were then repeated and participants were again asked to rate their familiarity to the words and the pseudo-words.

Fig. 2.

Average familiarity scores from recognition rating on both real words (A and B) and pseudo-words (C and D) after passive listening (control) and active phonological priming tasks. d is Cohen’s effect size for paired sample comparison.

Fig. 3.

Relationships between auditory hallucinations and average familiarity scores after passive listening (A and B) and active phonological priming (C and D) tasks in SZ. E: Verbal working memory (WM) correlations with average familiarity scores (recognition rating). Poorer WM was significantly associated with reporting stronger recognition of pseudo-words as familiar after active phonological priming (APP) in HC (r=−0.51, p=0.022) and SZ (r=−0.46, p=0.009), but not in any of the three control conditions. Y-axis plots the correlation coefficient r values between WM and average familiarity score during recognition rating (y-axis is flipped from negative to positive). F: Scatter plots between working memory and average familiarity scores after active phonological priming to pseudo-words in patients and controls. G: Mediation analysis. All values are t values. The total effect of WM on AH was significant (path C, t=−2.38). However, the direct effect of WM on AH was not significant when controlling for the mediator (path C’, t=−1.02), suggesting the effect of WM on AH was largely mediated by the familiarity level to pseudo-words after active phonological priming. * Statistically significant.