Abstract
Auditory hallucinations, the perception of a sound without a corresponding source, are common in people with hearing impairment. Two forms can be distinguished: simple (i.e., tinnitus) and complex hallucinations (speech and music). Little is known about the precise mechanisms underlying these types of hallucinations. Here we tested the assumption that spontaneous activity in the auditory pathways, following deafferentation, underlies these hallucinations and is related to their phenomenology. By extracting (fractional) Amplitude of Low Frequency Fluctuation [(f)ALFF] scores from resting state fMRI of 18 hearing impaired patients with complex hallucinations (voices or music), 18 hearing impaired patients with simple hallucinations (tinnitus or murmuring), and 20 controls with normal hearing, we investigated differences in spontaneous brain activity between these groups. Spontaneous activity in the anterior and posterior cingulate cortex of hearing-impaired groups was significantly higher than in the controls. The group with complex hallucinations showed elevated activity in the bilateral temporal cortex including Wernicke's area, while spontaneous activity of the group with simple hallucinations was mainly located in the cerebellum. These results suggest a decrease in error monitoring in both hearing-impaired groups. Spontaneous activity of language-related areas only in complex hallucinations suggests that the manifestation of the spontaneous activity represents the phenomenology of the hallucination. The link between cerebellar activity and simple hallucinations, such as tinnitus, is new and may have consequences for treatment.
Highlights
The occurrence of auditory hallucinations (AH), the perception of an auditory stimulus in the absence of a corresponding source, is not limited to psychiatric disease (Sommer, Kleijer, & Hugdahl, 2018) Several small-scale studies have suggested a link between hallucinations and deafness (Cole, Dowson, Dendukuri, & Belzile, 2002; Teunisse & Rikkert, 2012)
Our results show that hearing-impaired individuals with any form of hallucinations show increased spontaneous activity in areas known to be involved in hallucinations, such as the anterior cingulate cortex (ACC) and the parahippocampal gyrus as well as in the posterior cingulate cortex, (PCC; as indicated by fALFF scores), areas known for higher order cognitive processes, such as attention, salience and memory
While the two patient groups did not differ in their amplitude of low frequency fluctuation (ALFF) scores, fALFF scores revealed that patients with complex hallucinations showed more spontaneous activity in areas related to language comprehension, whereas in the group with simple hallucinations activity was found predominately in the cerebellum
Summary
The occurrence of auditory hallucinations (AH), the perception of an auditory stimulus in the absence of a corresponding source, is not limited to psychiatric disease (Sommer, Kleijer, & Hugdahl, 2018) Several small-scale studies have suggested a link between hallucinations and deafness (Cole, Dowson, Dendukuri, & Belzile, 2002; Teunisse & Rikkert, 2012) In line with these observations, a recent cross-sectional study including over 1000 subjects reported that between 12% and 24% of patients with hearing loss experience AH, with higher prevalence in more severe hearing impairment (Linszen et al, 2019). Treatment options for both complex and simple hallucinations associated with hearing loss are scarce (Coebergh et al, 2015), unless hearing impairment can be repaired (Colon-Rivera & Oldham, 2014)
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