The "paradoxical" engagement of the primary auditory cortex in patients with auditory verbal hallucinations: a meta-analysis of functional neuroimaging studies

Abstract

The existing literature on neuroimaging studies of auditory verbal hallucinations (AVHs) in patients with schizophrenia contains an apparent "paradox" in that the same areas in the auditory cortex seem to be both activated and deactivated in relation to AVHs, depending on whether an external auditory stimulus is present or not. We performed meta-analyses of neuroimaging studies examining patients with schizophrenia during the processing of auditory stimuli and in individuals experiencing hallucinations in the absence of auditory stimuli to examine whether the auditory cortex shows the paradoxical decrease/increase pattern across studies. Databases PubMed and ISI Web of Knowledge were queried with the combination of the keywords "auditory verbal hallucinations", "auditory hallucinations", "fMRI", "PET", "imaging", yielding 11 studies involving comparison between schizophrenia and control group during external auditory stimulation, and 12 studies of hallucinating subjects experiencing AVHs and resting in the absence of auditory stimulation. The data were analyzed using Activation Likelihood Estimation method. The results showed overlapping increased activation in the absence of an external stimulus, and decreased activation in the presence of an external auditory stimulus in the left primary auditory cortex and in the right rostral prefrontal cortex, confirming the "paradoxical" brain activation in relation to AVHs. It is suggested that the "paradox" may be caused by an attentional bias towards internally generated information and failure of down- and up-regulation of the default mode and auditory processing networks, respectively, with the consequence that the spontaneous activation in the absence of an external stimulus shuts down the perceptual apparatus for further processing.