Enhanced cortical effects of auditory stimulation and auditory attention in healthy individuals prone to auditory hallucinations during partial wakefulness.

People who experience auditory hallucinations while falling asleep (hypnagogic) or waking up (hypnopompic) show heightened brain sensitivity to sounds. In a behavioral study, 26 hallucinators reported greater subjective sensitivity to environmental sounds than 74 controls. Two fMRI experiments with 12 hallucinators and 12 matched controls found that hallucinators had greater speech-evoked brain activation in the left supramarginal gyrus. When directing attention to sound, they showed stronger activation in the anterior cingulate gyrus. These findings suggest that a tendency toward hallucinations involves increased auditory and polysensory cortex sensitivity, possibly due to enhanced attentional bias from the anterior cingulate gyrus, supporting the idea that top-down modulation of auditory cortex responses is key to generating auditory hallucinations.

Study at a glance

Abstract

Investigating auditory hallucinations that occur in health may help elucidate brain mechanisms which lead to the pathological experience of auditory hallucinations in neuropsychiatric disorders such as schizophrenia. In this study, we investigated healthy individuals who reported auditory hallucinations whilst falling asleep (hypnagogic hallucinations; HG) and waking up (hypnopompic hallucinations; HP). In an initial behavioural study, we found that subjects with a history of auditory HG/HP hallucinations (n = 26) reported significantly greater subjective sensitivity to environmental sounds than non-hallucinator controls (n = 74). Then, two fMRI experiments were performed. The first examined speech-evoked brain activation in 12 subjects with a history of auditory HG/HP hallucinations and 12 non-hallucinator controls matched for age, gender and IQ. The second fMRI experiment, in the same subjects, probed how brain activation was modulated by auditory attention using a bimodal selective attention paradigm. In the first experiment, the hallucinator group demonstrated significantly greater speech-evoked activation in the left supramarginal gyrus than the control group. In the second experiment, directing attention towards the auditory (vs. visual) modality induced significantly greater activation of the anterior cingulate gyrus in the hallucinator group than in the control group. These results suggest that hallucination proneness is associated with increased sensitivity of auditory and polysensory association cortex to auditory stimulation, an effect which might arise due to enhanced attentional bias from the anterior cingulate gyrus. Our data support the overarching hypothesis that top-down modulation of auditory cortical response characteristics may be a key mechanistic step in the generation of auditory hallucinations.