Auditory hallucinations activate language and verbal short-term memory, but not auditory, brain regions

Paola Fuentes-Claramonte,María Ángeles García-León,Raymond Salvador,María Llanos Torres,Josep Munuera,Peter J Mckenna,Salvador Sarró,Edith Pomarol-Clotet,Amalia Guerrero-Pedraza,Josep Tristany,Joan Soler-Vidal,Aniol Santo-Angles,Pilar Salgado-Pineda,Wolfram Hinzen,Nuria Ramiro

doi:10.1038/s41598-021-98269-1

Abstract

Auditory verbal hallucinations (AVH, ‘hearing voices’) are an important symptom of schizophrenia but their biological basis is not well understood. One longstanding approach proposes that they are perceptual in nature, specifically that they reflect spontaneous abnormal neuronal activity in the auditory cortex, perhaps with additional ‘top down’ cognitive influences. Functional imaging studies employing the symptom capture technique—where activity when patients experience AVH is compared to times when they do not—have had mixed findings as to whether the auditory cortex is activated. Here, using a novel variant of the symptom capture technique, we show that the experience of AVH does not induce auditory cortex activation, even while real speech does, something that effectively rules out all theories that propose a perceptual component to AVH. Instead, we find that the experience of AVH activates language regions and/or regions that are engaged during verbal short-term memory.

Highlights

Auditory verbal hallucinations (AVH, ‘hearing voices’) are an important symptom of schizophrenia but their biological basis is not well understood
Theoretical approaches to AVH include so-called ‘cognitive’ models, which argue that they are a manifestation of non-perceptual processes, for example inner speech that fails to be labeled as internally g enerated[3], or memories whose vividness and/or intrusiveness leads them to be misinterpreted as perceptions[4,5]
We further explored the AVH + patients’ responses to hallucinated and real speech using time series plots of activation in anatomically-defined regions of interest (ROIs) in regions where activation was found in the two conditions

Summary

Results

Activations in response to AVH and real auditory stimuli. Findings using whole brain, voxel-based analyses, with an initial threshold of z = 3.1 (p < 0.001) and cluster-corrected for multiple comparisons at p < 0.05, are shown in Fig. 2 (for full details of the data analysis see “Methods”; MNI coordinates for all clusters are given in Supplementary Table S2). Activation levels for both real speech and AVH were similar in the two regions generally accepted as comprising Broca’s area, the left inferior frontal gyrus, pars opercularis and pars triangularis, and in its homologue on the right. This was the case for the anterior and posterior portions of the supramarginal gyrus, which on the left overlap with Wernicke’s area[16]. As in the original analysis, we found a small cluster of activation in the extreme posterior superior temporal gyrus, in this case only in the right hemisphere, roughly overlapping with Wernicke’s area right homologue

Discussion

F Precentral

Methods