Reality of auditory verbal hallucinations

Abstract

Distortion of the sense of reality, actualized in delusions and hallucinations, is the key feature of psychosis but the underlying neuronal correlates remain largely unknown. We studied 11 highly functioning subjects with schizophrenia or schizoaffective disorder while they rated the reality of auditory verbal hallucinations (AVH) during functional magnetic resonance imaging (fMRI). The subjective reality of AVH correlated strongly and specifically with the hallucination-related activation strength of the inferior frontal gyri (IFG), including the Broca's language region. Furthermore, how real the hallucination that subjects experienced was depended on the hallucination-related coupling between the IFG, the ventral striatum, the auditory cortex, the right posterior temporal lobe, and the cingulate cortex. Our findings suggest that the subjective reality of AVH is related to motor mechanisms of speech comprehension, with contributions from sensory and salience-detection-related brain regions as well as circuitries related to self-monitoring and the experience of agency.

Figure 1

During fMRI scanning, the subjects signalled the beginning and end of multiple AVHs and rated the SRH and loudness of AVHs by pressing two buttons. (A) Schematic example of a part of a session; time runs from left to right. Contrast images for hallucination versus non-hallucination periods (B) were correlated with the SRH over subjects (C). We then compared the coupling of the so-found neuronal correlates of the SRH between hallucination versus non-hallucination periods (D). Finally, we correlated the hallucination-related coupling with the SRH (E).

Figure 2

Correlation between AVH-related brain activation and the SRH. Brodman areas 44 and 45 (the Broca's region and its right homologue) are marked according to cytoarchitectonical maps by Eickhoff et al. (2005). Right: the colour scale for statistical significance.

Figure 3

Positive correlations between hallucination-related coupling (in parameter estimates) and the SRH. The coupling refers to the difference with the left IFG (x, y, z = –52, 20, 8) during hallucinations versus non-hallucination periods. The stronger the SRH, the stronger the coupling of the IFG with the right ventral striatum (A), the middle right anterior cingulate cortex (B), the right posterior temporal lobe (C), the auditory cortex (D), and the left nucleus accumbens (E). (F) The colour scale for statistical significance.

Figure 4

Negative correlation between the AVH-related coupling (in parameter estimates) of the left IFG and the SRH. The stronger the SRH, the weaker the coupling of the IFG with the posterior and rostral anterior cingulate cortex.