Evidence for functional abnormality in the right auditory cortex during musical hallucinations

doi:10.1016/S0140-6736(99)05213-7

The Lancet

Volume 354, Issue 9191, 13 November 1999, Pages 1703-1704

https://doi.org/10.1016/S0140-6736(99)05213-7 Get rights and content

Summary

Right auditory cortex dysfunction during musical hallucinations occurred in an 88–year-old woman, who was otherwise cognitively intact. We assessed this phenomenon with a combination of neuromagnetic and cerebral blood-flow measurements.

References (5)

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DA Silbersweig et al.
A functional neuroanatomy of hallucinations in schizophrenia.
Nature
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Cited by (57)

Altered effective brain network topology in tinnitus: An EEG source connectivity analysis
2021, Biomedical Signal Processing and Control
Citation Excerpt :
Regarding our Granger causality analysis, we identified abnormally increased causal flow from the IFGtriang to the PHG in the beta2 frequency range, and from the IFGtriang to the PHG and TPOmid in the beta3 band in tinnitus group compared to the controls. MEG and SPECT studies have revealed increased blood flow of the inferior frontal gyrus during musical hallucination [70]. Neuroimaging evidence suggests that tinnitus and musical hallucination reveal similar central cortex activity, with an increase in theta-gamma response during EEG measurement.
Tinnitus is defined as the auditory phantom perception in the absence of any objective external sound source. In this paper, we used the resting-state electroencephalography (EEG) data to reconstruct the neural sources based on the unit-noise-gain linearly constrained minimum-variance (LCMV) beamformer and applied the effective connectivity analysis on the reconstructed sources to examine the directional neuronal interactions between brain regions in tinnitus patients compared to the healthy controls. We found significantly disrupted patterns of effective connectivity in several brain areas including the frontal, temporal, and occipital cortices as well as the caudate nucleus. Particularly, significant aberrant causal couplings were observed in the orbitofrontal cortex, inferior frontal gyrus_triangular, and parahippocampal region that could potentially illustrate the auditory information retrieval, perception, and evaluation of the phantom sound in the brain of tinnitus patients. Furthermore, topological alterations of the brain network were investigated using graph theoretical analysis. Our findings demonstrated significantly decreased both global integration and segregation of the brain network in tinnitus patients accompanied by the topological shift of tinnitus network to a more random structure in the high-frequency bands. These findings were consistent with the hypothesis of the brain network deviation from small-worldness topology accompanied by reduced global integration in brain-related disorders.
A brain basis for musical hallucinations
2014, Cortex
Citation Excerpt :
Although a number of case studies involving MH have been reported in the literature (for reviews see Evers, 2006; Evers & Ellger, 2004), there are only a few studies that have investigated the brain bases for MH. In order to determine how the states of a hallucinating brain differ from that of a normal brain, these studies have either compared brain activities in the same subject but in two different sessions (Griffiths, 2000; Kasai, Asada, Yumoto, Takeya, & Matsuda, 1999; Shoyama et al., 2010) often separated by several days, or compared brain activity across different population of subjects, with and without hallucinations (Shinosaki et al., 2003; Vanneste, Song, & De Ridder, 2013). A wide range of cortical and sub-cortical areas, which are inconsistent across studies, have been implicated in MH.
The physiological basis for musical hallucinations (MH) is not understood. One obstacle to understanding has been the lack of a method to manipulate the intensity of hallucination during the course of experiment. Residual inhibition, transient suppression of a phantom percept after the offset of a masking stimulus, has been used in the study of tinnitus. We report here a human subject whose MH were residually inhibited by short periods of music. Magnetoencephalography (MEG) allowed us to examine variation in the underlying oscillatory brain activity in different states. Source-space analysis capable of single-subject inference defined left-lateralised power increases, associated with stronger hallucinations, in the gamma band in left anterior superior temporal gyrus, and in the beta band in motor cortex and posteromedial cortex. The data indicate that these areas form a crucial network in the generation of MH, and are consistent with a model in which MH are generated by persistent reciprocal communication in a predictive coding hierarchy.
Tinnitus and musical hallucinosis: The same but more
2013, NeuroImage
Citation Excerpt :
Furthermore, we found increased activity for the patients with a complex auditory phantom within the right inferior frontal area and right superior temporal pole in contrast to patients with a simple auditory phantom. This is in line with previous records of MEG and SPECT that showed increase of blood flow in the right superior temporal gyrus and right inferior frontal gyrus during musical hallucination (Kasai et al., 1999). In addition, Halpern and Zatorre observed activation in the right inferior frontal area during a musical imagery task and assumed that it reflected the involvement of these regions in the retrieval of familiar musical information (Halpern and Zatorre, 1999).
While tinnitus can be interpreted as a simple or elementary form of auditory phantom perception, musical hallucinosis is a more complex auditory phantom phenomenon not only limited to sound perception, but also containing semantic and musical content. It most often occurs in association with hearing loss. To elucidate the relation between simple and complex auditory phantom percepts a source localized electroencephalography (EEG) study is performed. The analyses showed in both simple and complex auditory phantoms an increase in theta–gamma activity and coupling within the auditory cortex that could be associated with the thalamocortical dysrhythmia model. Furthermore increased beta activity within the dorsal anterior cingulate cortex and anterior insula is demonstrated, that might be related to auditory awareness, salience and its attribution to an external sound source. The difference between simple and complex auditory phantoms relies on differential alpha band activity within the auditory cortex and on beta activity in the dorsal anterior cingulate cortex and (para)hippocampal area. This could be related to memory based load dependency, while suppression within the primary visual cortex might be due the presence of a continuous auditory cortex activation inducing an inhibitory signal to the visual system. Complex auditory phantoms further activate the right inferior frontal area (right sided Broca homolog) and right superior temporal pole that might be associated with the musical content. In summary, this study showed for the first time that simple and complex auditory phantoms might share a common neural substrate but differ as complex auditory phantoms are associated with activation in brain areas related to music and language processing.
Prevalence of musical hallucinations in patients referred for audiometric testing
2012, American Journal of Geriatric Psychiatry
To assess the prevalence of musical hallucinations in patients referred for audiometric testing and to analyze associations with age, sex, degree of hearing loss, asymmetrical hearing loss, and tinnitus.
Patients referred for audiometric testing underwent a semi-structured interview on tinnitus and musical hallucinations.
Out of 194 patients, most of whom had mild to moderate hearing loss, seven (3.6%) had musical hallucinations. Significant associations were found with female sex and predominant left-sided hearing impairment, but not with age, severity of hearing loss, or tinnitus.
This study offers no evidence that age is a risk factor. Musical hallucinations seem to be prevalent in women with predominant left-sided hearing impairment.
Shared mechanisms in perception and imagery of auditory accents
2011, Clinical Neurophysiology
Citation Excerpt :
Compared to the visual and motor domains, the number of studies focussing on the relationship between auditory perception and imagery is relatively small. Support for shared mechanisms in auditory perception and imagery comes from behavioral (e.g. Farah and Smith, 1983; Halpern et al., 2004) as well as clinical angles (e.g. Kasai et al., 1999; Shinosaki et al., 2003). Zatorre et al. (1996) reported evidence from a positron emission tomography (PET) study for activation of parts of the auditory cortex during perception as well as during imagination of music.
An auditory rhythm can be perceived as a sequence of accented (loud) and non-accented (soft) beats or it can be imagined. Subjective rhythmization refers to the induction of accenting patterns during the presentation of identical auditory pulses at an isochronous rate. It can be an automatic process, but it can also be voluntarily controlled. We investigated whether imagined accents can be decoded from brain signals on a single-trial basis, and if there is information shared between perception and imagery in the contrast of accents and non-accents.
Ten subjects perceived and imagined three different metric patterns (two-, three-, and four-beat) superimposed on a steady metronome while electroencephalography (EEG) measurements were made. Shared information between perception and imagery EEG is investigated by means of principal component analysis and by means of single-trial classification.
Classification of accented from non-accented beats was possible with an average accuracy of 70% for perception and 61% for imagery data. Cross-condition classification yielded significant performance above chance level for a classifier trained on perception and tested on imagery data (up to 66%), and vice versa (up to 60%).
Results show that detection of imagined accents is possible and reveal similarity in brain signatures relevant to distinction of accents from non-accents in perception and imagery.
Our results support the idea of shared mechanisms in perception and imagery for auditory processing. This is relevant for a number of clinical settings, most notably by elucidating the basic mechanisms of rhythmic auditory cuing paradigms, e.g. as used in motor rehabilitation or therapy for Parkinson’s disease. As a novel Brain–Computer Interface (BCI) paradigm, our results imply a reduction of the necessary BCI training in healthy subjects and in patients.
Ictal hallucination and hemispheric specialization: Findings from 217 cases with a unilateral epileptic focus
2009, Biological Psychology
Epileptic populations are generally considered inappropriate to investigate hemispheric specialization. However, (1) because hallucination occurs in the early stage of the ictus during which activation is observed in and around the focus, the former could be a direct result of the latter (hypothesis 1), and (2) the type of psychological content of ictal hallucination could depend on which hemisphere is ictally activated (hypothesis 2). It was predicted that, on the basis of quantitative analysis of previously published singles case reports, unilateral ictal hallucinations should occur in the visual field, ear or hemibody contralateral to the side of the ictal focus (test of hypothesis 1). It was also predicted that verbal ictal auditory hallucinations should result more often from left hemisphere foci, and non-verbal auditory ictal hallucinations from right hemisphere foci (test of hypothesis 2). Previously published cases (N = 217) of ictal hallucination from a unilateral epileptic focus were reviewed and analyzed with multivariate statistics. Both predictions were strongly supported.

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Research LettersEvidence for functional abnormality in the right auditory cortex during musical hallucinations

Summary

Musical hallucinations: a review of synthesis.

Neuropsych Neuropsychol Behav Neurol

A functional neuroanatomy of hallucinations in schizophrenia.

Nature

Research Letters
Evidence for functional abnormality in the right auditory cortex during musical hallucinations