The role of the primary auditory cortex in the neural mechanism of auditory verbal hallucinations

Abstract

Auditory verbal hallucinations (AVHs) are a subjective experience of "hearing voices" in the absence of corresponding physical stimulation in the environment. The most remarkable feature of AVHs is their perceptual quality, that is, the experience is subjectively often as vivid as hearing an actual voice, as opposed to mental imagery or auditory memories. This has lead to propositions that dysregulation of the primary auditory cortex (PAC) is a crucial component of the neural mechanism of AVHs. One possible mechanism by which the PAC could give rise to the experience of hallucinations is aberrant patterns of neuronal activity whereby the PAC is overly sensitive to activation arising from internal processing, while being less responsive to external stimulation. In this paper, we review recent research relevant to the role of the PAC in the generation of AVHs. We present new data from a functional magnetic resonance imaging (fMRI) study, examining the responsivity of the left and right PAC to parametrical modulation of the intensity of auditory verbal stimulation, and corresponding attentional top-down control in non-clinical participants with AVHs, and non-clinical participants with no AVHs. Non-clinical hallucinators showed reduced activation to speech sounds but intact attentional modulation in the right PAC. Additionally, we present data from a group of schizophrenia patients with AVHs, who do not show attentional modulation of left or right PAC. The context-appropriate modulation of the PAC may be a protective factor in non-clinical hallucinations.

Keywords: auditory attention; auditory verbal hallucinations; non-clinical; primary auditory cortex; schizophrenia.

Figure 1

Schematic illustration of the primary auditory cortex (PAC) on a brain template. The PAC occupies most of the Heschl's gyrus (red), which extends mediolaterally within the Sylvian fissure. PAC is surrounded by auditory association areas on the superior temporal gyrus (blue).

Figure 2

Attention by IID interaction in the primary auditory cortex (PAC) projected on a brain template. Two axial slices are presented, at z-coordinate −1 and −7 (position of slice presented with red horizontal lines on inset in the right corner). Results from NCH (red) and control group (green) are plotted separately for illustrative purposes. Line graphs on the left side show changes in parameter estimates (arbitrary units) in the left and right PAC (peak voxel) to change in interaural intensity difference (IID) and attention (FR, forced-right; FL, forced-left), pooled across groups. Vertical lines represent 95% confidence intervals.

Figure 3

Main effect of group across all levels of attention and IID in the right PAC projected on a brain template. Scatterplot shows the individual subjects' mean parameter estimate at peak voxel, demonstrating that the reduction of activation was consistent within NCH group. Lines represent 95% confidence intervals.