The Brain’s Voices: Comparing Nonclinical Auditory Hallucinations and Imagery

Abstract

Although auditory verbal hallucinations are often thought to denote mental illness, the majority of voice hearers do not satisfy the criteria for a psychiatric disorder. Here, we report the first functional imaging study of such nonclinical hallucinations in 7 healthy voice hearers comparing them with auditory imagery. The human voice area in the superior temporal sulcus was activated during both hallucinations and imagery. Other brain areas supporting both hallucinations and imagery included fronto temporal language areas in the left hemisphere and their contralateral homologues and the supplementary motor area (SMA). Hallucinations are critically distinguished from imagery by lack of voluntary control. We expected this difference to be reflected in the relative timing of prefrontal and sensory areas. Activity of the SMA indeed preceded that of auditory areas during imagery, whereas during hallucinations, the 2 processes occurred instantaneously. Voluntary control was thus represented in the relative timing of prefrontal and sensory activation, whereas the sense of reality of the sensory experience may be a product of the voice area activation. Our results reveal mechanisms of the generation of sensory experience in the absence of external stimulation and suggest new approaches to the investigation of the neurobiology of psychopathology.

Auditory Hallucinations Elicit Similar Brain Activation in Psychotic and Nonpsychotic Individuals

“…[11][12][13][14] Thus far, only one study investigated brain activation during AVH in nonclinical individuals. 15 This study included seven nonclinical individuals with AVH and 7 control subjects. The main difference between this study and the current study is that the current study compared AVH between psychotic and nonpsychotic individuals, while Linden and colleagues 15 compared brain activation during AVH in nonclinical individuals with brain activation during imagery in a control group.…”

“…15 This study included seven nonclinical individuals with AVH and 7 control subjects. The main difference between this study and the current study is that the current study compared AVH between psychotic and nonpsychotic individuals, while Linden and colleagues 15 compared brain activation during AVH in nonclinical individuals with brain activation during imagery in a control group. As Linden and colleagues 15 reported activation of frontotemporal language areas, in the left hemisphere and their contralateral homologues and the supplementary motor area during AVH, as well as during verbal imagery, these results are for the most part in concordance with the present study.…”

“…[11][12][13][14] Thus far, only one study visualized AVH-related brain activation in nonpsychotic subjects, revealing activation in bilateral frontal and temporoparietal areas as well as motor areas. 15 However, this study included only 7 subjects and did not compare AVH-related brain activation in their group of nonpsychotic subjects to that of psychotic patients. The aim of the present study was to identify commonalities and/or differences in brain activation during AVH between psychotic and nonpsychotic individuals with AVH in samples that are large enough to enable group-wise analysis.…”

Cognition and Brain Function in Schizotypy: A Selective Review

“…81 Mental imagery is also related to hallucinations but with a key difference in the perceived locus of agency. 82 Enhanced subjective vividness of mental imagery has been reported in individuals with schizophrenia and elevated schizotypal traits in visual 83 and auditory 84 modalities. However, the link between vivid imagery experiences and hallucinations is weak or unclear.…”

Similarities in face and voice cerebral processing

“…TVAs show greater response to voices -whether they contain speech or not -than to other categories of nonvocal sounds from the environment or to acoustical control stimuli such as scrambled voices and amplitude-modulated noise. They are organized bilaterally in several clusters along the superior temporal gyrus and superior temporal sulcus of the temporal lobe (Belin et al, 2000;Belin, Zatorre, & Ahad, 2002;Linden, Thornton, Kuswanto, Johnston, & Jackson, 2011;Von Kriegstein & Giraud, 2004). A recent large analysis of cerebral voice sensitivity in several hundred participants (Pernet et al, 2015) demonstrates that TVAs are the most salient part of a "vocal brain", a bilateral, distributed network of cortical and subcortical regions showing significant voice-sensitivity including in particular inferior prefrontal areas and the amygdala.…”