Functional Magnetic Resonance Imaging of Inner Speech in Schizophrenia

doi:10.1016/j.biopsych.2009.09.007

Biological Psychiatry

Volume 67, Issue 3, 1 February 2010, Pages 232-237

https://doi.org/10.1016/j.biopsych.2009.09.007 Get rights and content

Background

Auditory verbal hallucinations in schizophrenia have been linked to defective monitoring of one's own verbal thoughts. Previous studies have shown that patients with auditory verbal hallucinations show attenuated activation of brain regions involved with auditory processing during the monitoring of inner speech. However, there are no functional magnetic resonance imaging studies explicitly comparing the perception of external speech with internal speech in the same patients with schizophrenia. The present study investigated the functional neuroanatomy of inner and external speech in both patients with schizophrenia and healthy control subjects.

Methods

Fifteen patients with schizophrenia and 12 healthy control subjects were studied using functional magnetic resonance imaging while listening to sentences or imagining sentences.

Results

Significant interactions between group (control subjects vs. patients) and task (listening vs. inner speech) were seen for the left superior temporal gyrus, as well as regions within the cingulate gyrus.

Conclusions

Attenuated deactivation of the left superior temporal gyrus in schizophrenia patients during the processing of inner speech may reflect deficits in the forward models subserving self-monitoring.

Section snippets

Subjects

Fifteen male patients with a DSM-IV diagnosis of schizophrenia and right-handed, as assessed with the Annett Handedness Inventory (20), participated in the study. Patients were recruited through consultant and key worker recommendations and had all experienced prominent auditory hallucinations during exacerbations of their illness. Fourteen subjects were outpatients and one subject was an inpatient. All patients were receiving regular doses of antipsychotic medication. Mean age of the patients

Behavioral Data

The mean response time to complete the inner speech task was 2.62 seconds (SD = 1.59) for control subjects and 2.28 seconds (SD = .85) for patients. This difference was not statistically significant [t(22) = .64, p = .53]. On postscan debriefing, all subjects reported that they had been able to perform the tasks and thus data from all subjects were included in the analyses.

Imaging Data: Inner Speech Versus Listening

The main effect of inner speech was associated with greater activation in the left inferior frontal gyrus and anterior

Discussion

The main finding was a significant interaction between group and task for the left superior temporal cortex. During the listening trials, the anticipated activation of the left superior temporal cortex was evident in control subjects and in schizophrenia patients, suggesting that listening to spoken sentences is not impaired in schizophrenia patients. Control subjects showed greater decrease in activation during inner speech compared with listening than patients. This provides evidence for

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Auditory verbal hallucinations (AVH) ― experienced as voice hearing independent of a corresponding external sound source ― are a cardinal symptom of psychosis. Approximately 6-13% of healthy individuals also experience voice hearing. Despite numerous attempts to explain the neurofunctional mechanisms underlying AVH, they remain notoriously unexplained. However, evidence relates AVH to mechanistic changes in the forward model. This review synthesizes behavioral and neuroimaging studies exploring the central role of cerebellar circuitry in the forward model, with a particular focus on non-verbal and verbal auditory feedback. It confirms that erratic prediction of sensory consequences in voice and sound production is linked to impaired cerebellar function, which initiates AVH and affects higher-level cognitive functions. We propose new research directions linking the forward model to voice and sound feedback processing. We consider this review as a starting point for mapping mechanisms of the forward model to neurocognitive mechanisms underlying AVH.
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Archival ReportFunctional Magnetic Resonance Imaging of Inner Speech in Schizophrenia

Background

Methods

Results

Conclusions

Section snippets

Subjects

Behavioral Data

Imaging Data: Inner Speech Versus Listening

Discussion

Conscious Cogn

Neuron

Lancet

Magn Reson Imaging

Neuroimage

Neuroimage

Int J Psychophysiol

Biol Psychiatry

Lancet

Cortical responsiveness during inner speech in schizophrenia: An event-related potential study

Am J Psychiatry

Evidence for sensory prediction deficits in schizophrenia

Am J Psychiatry

Functional MRI of verbal self-monitoring in schizophrenia: Performance and illness-specific effects

Schizophr Bull

Inner speech models of auditory verbal hallucinations: Evidence from behavioural and neuroimaging studies

Int Rev Psychiatry

An internal model for sensorimotor integration

Science

Compelling imagery, unanticipated speech and deceptive memory: Neurocognitive models of auditory verbal hallucinations in schizophrenia

Cogn Neuropsychiatry

Efference copy and corollary discharge: Implications for thinking and its disorders

Schizophr Bull

Regional brain activity in schizophrenic patients during the performance of a verbal fluency task

Br J Psychiatry

Functional anatomy of verbal fluency in people with schizophrenia and those at genetic riskFocal dysfunction and distributed disconnectivity reappraised

Br J Psychiatry

No evidence for left superior temporal dysfunction in asymptomatic schizophrenia and bipolar disorderPET study of verbal fluency

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Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging

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Engagement of brain areas implicated in processing inner speech in people with auditory hallucinations

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Auditory verbal hallucinations predominantly activate the right inferior frontal area

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Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations

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Acoustic noise and functional magnetic resonance imaging: Current strategies and future prospects

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Archival Report
Functional Magnetic Resonance Imaging of Inner Speech in Schizophrenia