Auditory verbal hallucinations of epileptic origin

Complex auditory hallucinations are often characterized by hearing voices and are then called auditory verbal hallucinations (AVHs). While AVHs have been extensively investigated in psychiatric patients suffering from schizophrenia, reports from neurological patients are rare and, in most cases, incomplete. Here, we characterize AVHs in 9 patients suffering from pharmacoresistant epilepsy by analyzing the phenomenology of AVHs and patients' neuropsychological and lesion profiles. From a cohort of 352 consecutively examined patients with epilepsy, 9 patients suffering AVHs were identified and studied by means of a semistructured interview, neuropsychological tests, and multimodal imaging, relying on a combination of functional and structural neuroimaging data and surface and intracranial EEG. We found that AVHs in patients with epilepsy were associated with prevalent language deficits and damage to posterior language areas and basal language areas in the left temporal cortex. Auditory verbal hallucinations, most of the times, consisted in hearing a single voice of the same gender and language as the patient and had specific spatial features, being, most of the times, perceived in the external space, contralateral to the lesion. We argue that the consistent location of AVHs in the contralesional external space, the prominence of associated language deficits, and the prevalence of lesions to the posterior temporal language areas characterize AVHs of neurological origin, distinguishing them from those of psychiatric origin.     

Auditory verbal hallucinations in schizophrenia as aberrant lateralized speech perception: evidence from dichotic listening

We report evidence that auditory verbal hallucinations (AVH) in schizophrenia patients are perceptual distortions lateralized to the left hemisphere. We used a dichotic listening task with repeated presentations of consonant-vowel syllables, a different syllable in the right and left ear. This task produces more correct reports for the right ear syllable in healthy individuals, indicative of left hemisphere speech processing focus. If AVHs are lateralized to the left hemisphere language receptive areas, then this should interfere with correct right ear reports in the dichotic task, which would result in significant negative correlations with severity of AVHs. We correlated the right and left ear correct reports with the PANSS hallucination symptom, and a randomly selected negative symptom, in addition to the sum total of the positive and negative symptoms, in 160 patients with schizophrenia. The results confirmed the predictions with significant negative correlations for the right ear scores with the PANSS hallucination item, and for the sum total of positive symptoms, while all other correlations were close to zero. The results are unambiguous evidence for AVHs as aberrant speech perceptions originating in the left hemisphere.     

Auditory verbal hallucinations and cognitive functioning in healthy individuals

Auditory verbal hallucinations (AVH) are a characteristic symptom in schizophrenia, and also occur in the general, non-clinical population. In schizophrenia patients, several specific cognitive deficits, such as in speech processing, working memory, source memory, attention, inhibition, episodic memory and self-monitoring have been associated with auditory verbal hallucinations. Such associations are interesting, as they may identify specific cognitive traits that constitute a predisposition for AVH. However, it is difficult to disentangle a specific relation with AVH in patients with schizophrenia, as so many other factors can affect the performance on cognitive tests. Examining the cognitive profile of healthy individuals experiencing AVH may reveal a more direct association between AVH and aberrant cognitive functioning in a specific domain. For the current study, performance in executive functioning, memory (both short- and long-term), processing speed, spatial ability, lexical access, abstract reasoning, language and intelligence performance was compared between 101 healthy individuals with AVH and 101 healthy controls, matched for gender, age, handedness and education. Although performance of both groups was within the normal range, not clinically impaired, significant differences between the groups were found in the verbal domain as well as in executive functioning. Performance on all other cognitive domains was similar in both groups. The predisposition to experience AVH is associated with lower performance in executive functioning and aberrant language performance. This association might be related to difficulties in the inhibition of irrelevant verbal information.     

Auditory hallucinations and subvocal speech in schizophrenic patients

Fourteen of 18 hallucinating schizophrenic patients reported that the voices they heard went away when they undertook a maneuver that precluded subvocalization. The same applied to 18 of 21 normal subjects who hallucinated under the influence of hypnotic suggestion. Control maneuvers had no such effect. The authors suggest that auditory hallucinations may be projections of schizophrenic patients' verbal thoughts, subvocalized due to deficient cerebral cortical inhibition.     

Auditory verbal hallucinations and the interhemispheric auditory pathway in chronic schizophrenia

Objectives. The interhemispheric auditory pathway has been shown to play a crucial role in the processing of acoustic stimuli, and alterations of structural and functional connectivity between bilateral auditory areas are likely relevant to the pathogenesis of auditory verbal hallucinations (AVHs). The aim of this study was to examine this pathway in patients with chronic schizophrenia regarding their lifetime history of AVHs. Methods. DTI scans were acquired from 33 healthy controls (HC), 24 schizophrenia patients with a history of AVHs (LT-AVH) and nine schizophrenia patients without any lifetime hallucinations (N-LT-AVH). The interhemispheric auditory fibre bundles were extracted using streamline tractography. Subsequently, diffusivity indices, namely Fractional Anisotropy (FA), Trace, Mode, Axial and Radial diffusivity, were calculated. Results. FA was decreased over the entire pathway in LT-AVH compared with N-LT-AVH. Moreover, LT-AVH displayed decreased FA and Mode as well as increased radial diffusivity in the midsagittal section of the fibre tract. Conclusions. These findings indicate complex microstructural changes in the interhemispheric auditory pathway of schizophrenia patients with a history of AVHs. Alterations appear to be absent in patients who have never hallucinated.     

Auditory verbal hallucinations: imaging,analysis, and intervention

In this article, we will link neuroimaging, data analysis, and intervention methods in an important psychiatric condition: auditory verbal hallucinations (AVH). The clinical and phenomenological background as well as neurophysiological findings will be covered and discussed with respect to noninvasive brain stimulation. Additionally, methods of noninvasive brain stimulation will be presented as ways to intervene with AVH. Finally, preliminary conclusions and possible future perspectives will be proposed.

     

Auditory verbal hallucinations in schizophrenia correlate with P50 gating

ObjectiveWhile auditory verbal hallucinations (AVHs) are a common symptom of schizophrenia, the underlying mechanisms behind these perceptual anomalies and their effects on auditory processing are not fully understood. Patients suffering from schizophrenia have been shown to exhibit impaired sensory gating of acoustic stimuli, evidenced by a failure to inhibit the auditory P50 scalp recorded middle latency evoked potential response to the second of two paired auditory “clicks” (S1–S2).MethodsBecause abnormal activation of auditory pathways is associated with a general AVH trait of schizophrenia patients, this study correlated the hallucinatory trait subscale of the Psychotic Symptoms Ratings Scale (PSYRATS) scores of 16 actively hallucinating patients with their P50 responses to S1 and S2 as well as sensory gating indices. P50 gating in patients was also compared to twenty one healthy controls.ResultsControl S1 amplitudes were significantly greater than those of patients. There was a negative correlation between PSYRATS scores and gating difference score as well as with S1 amplitude, and a positive correlation with gating ratio, indicating the global trait of hallucinating schizophrenia patients may be associated with deficiencies in the processing of auditory stimuli. No significant correlation was found when the same analysis was applied to a state-dependent hallucination ratings scale.SignificanceResults suggest the relationship between auditory hallucinations and auditory processing dysfunction measured by P50 response is more trait than state dependent in schizophrenia.     

Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations

Several studies report that patients with schizophrenia who experience auditory verbal hallucinations (AVH) tend to misidentify their own speech as that of somebody else. We tested the hypothesis that this tendency is associated with poor functional integration within the network of regions that mediate the evaluation of speech. Using functional magnetic resonance imaging, we measured brain responses from 11 schizophrenics with AVH, 10 schizophrenics without AVH, and 10 healthy controls. Stimuli comprised prerecorded words, which varied for their source (self, alien) and acoustic quality (undistorted, distorted). Participants had to indicate whether each word was spoken in their own or another person's voice via a button press. Using dynamic causal modeling, we estimated the impact of one region over another ("effective connectivity") and how this was modulated by source and distortion. In controls and in patients without AVH, the connectivity between left superior temporal and anterior cingulate cortex was significantly greater for alien- than for self-generated speech; in contrast, the reverse trend was found in schizophrenic patients with AVH. In conclusion, when patients with AVH appraise their own speech we find impaired functional integration between left superior temporal and anterior cingulate cortex. Although this finding is based on external rather than internal speech, the same mechanism may contribute to the faulty appraisal of inner speech that putatively underlies AVH.     

Auditory hallucinations and schizophrenia

Forty-five patients with auditory hallucinations were studied. Sixty per cent proved to be excellent hypnotic subjects with multiple personalities. These latter patients received 11 different diagnoses by clinicians, predominantly those related to schizophrenia or an affective illness. Because patients with multiple personalities frequently have hallucinations, delusions, paranoid ideas and bizarre behaviors, they may be misdiagnosed as some form of schizophrenia.     

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

A range of psychological theories have been proposed to account for the experience of auditory hallucinations in patients with psychosis. Influential amongst these theories are those implicating the defective monitoring of inner speech. Furthermore, self-monitoring and inner speech models have been the most studied using functional imaging. The aim of this article is to review the behavioural and neuroimaging evidence for the impaired monitoring of inner speech in patients who experience auditory verbal hallucinations. A comprehensive literature search was conducted for research investigating inner speech and cognitive self-monitoring models of auditory hallucinations in patients with schizophrenia. The evidence is critically discussed and directions for future investigations are suggested.     

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

A range of psychological theories have been proposed to account for the experience of auditory hallucinations in patients with psychosis. Influential amongst these theories are those implicating the defective monitoring of inner speech. Furthermore, self-monitoring and inner speech models have been the most studied using functional imaging. The aim of this article is to review the behavioural and neuroimaging evidence for the impaired monitoring of inner speech in patients who experience auditory verbal hallucinations. A comprehensive literature search was conducted for research investigating inner speech and cognitive self-monitoring models of auditory hallucinations in patients with schizophrenia. The evidence is critically discussed and directions for future investigations are suggested.     

Investigation of the neural substrates of voice recognition in Chinese schizophrenic patients with auditory verbal hallucinations: an event-related functional MRI study

Objective: Auditory hallucinations (AVHs), like real auditory perceptions, are often perceived as familiar voices. Given that neural correlates of AVHs involve the auditory cortex, it is likely that those brain regions responsible for recognition of voice identity are invoked during AVHs. Method: Schizophrenic patients with (n = 13) and without (n = 13) auditory hallucinations, and 13 healthy subjects performed a voice recognition task during functional magnetic resonance imaging at 1.5 T. In the task using prerecorded vocal stimuli, they classified voice as familiar and unfamiliar. Results: Under the familiar minus unfamiliar contrasts, cerebral activation pattern is different in the three groups and patients with auditory hallucinations showed less activation in the right temporal lobe than controls. Conclusion: Voice recognition was impaired in patients with AVHs. Our results support that auditory association cortices play a role in the perception of AVHs.     

Auditory/Verbal hallucinations, speech perception neurocircuitry, and the social deafferentation hypothesis.

Auditory/verbal hallucinations (AVHs) are comprised of spoken conversational speech seeming to arise from specific, nonself speakers. One hertz repetitive transcranial magnetic stimulation (rTMS) reduces excitability in the brain region stimulated. Studies utilizing 1-Hz rTMS delivered to the left temporoparietal cortex, a brain area critical to speech perception, have demonstrated statistically significant improvements in AVHs relative to sham simulation. A novel mechanism of AVHs is proposed whereby dramatic pre-psychotic social withdrawal prompts neuroplastic reorganization by the "social brain" to produce spurious social meaning via hallucinations of conversational speech. Preliminary evidence supporting this hypothesis includes a very high rate of social withdrawal emerging prior to the onset of frank psychosis in patients who develop schizophrenia and AVHs. Moreover, reduced AVHs elicited by temporoparietal 1-Hz rTMS are likely to reflect enhanced long-term depression. Some evidence suggests a loss of long-term depression following experimentally-induced deafferentation. Finally, abnormal cortico-cortical coupling is associated with AVHs and also is a common outcome of deafferentation. Auditory/verbal hallucinations (AVHs) of spoken speech or "voices" are reported by 60-80% of persons with schizophrenia at various times during the course of illness. AVHs are associated with high levels of distress, functional disability, and can lead to violent acts. Among patients with AVHs, these symptoms remain poorly or incompletely responsive to currently available treatments in approximately 25% of cases. For patients with AVHs who do respond to antipsychotic drugs, there is a very high likelihood that these experiences will recur in subsequent episodes. A more precise characterization of underlying pathophysiology may lead to more efficacious treatments.     

Auditory hallucinations and functional imaging

Auditory verbal hallucinations are a common symptom of schizophrenia. In general, hallucinations can affect all sensory modalities and occur in many neuropsychiatric disorders. They also serve the psychology of perception as the classic example of sensory experience in the absence of adequate external stimuli. Functional imaging studies showed the auditory cortex, the limbic system and language areas, both motor and sensory, to be active during auditory hallucinations. The psychological and neurophysiological models of hallucination can be integrated if we consider that patients with schizophrenia might ascribe internal monologues or dialogues to external sources. The activity of language areas during hallucinations would conform to such a model while the activity in auditory cortex might explain why auditory hallucinations are often so vivid and real for the patients suffering from them. Moreover, the activation of the limbic system might correspond to the emotional aspects of the content of the voices and the accompanying arousal. While the neurophysiological models of hallucination are thus already rather refined, the attempt at suppressing auditory cortex activity with repetitive transcranial magnetic stimulation in order to alleviate treatment-resistant acoustic hallucinations, which is based on the functional imaging findings, still needs further study. Treatment schemes that are based on the psychological theories are more varied and have shown more consistent and long lasting effects but also suffer from the difficulty in measuring hallucinations quantitatively. Future research with functional and structural imaging should go beyond correlating brain activity and symptoms and also address the functional and structural connectivity patterns in the brain that enable hallucinations.     

Reading speech from still and moving faces: the neural substrates of visible speech

Speech is perceived both by ear and by eye. Unlike heard speech, some seen speech gestures can be captured in stilled image sequences. Previous studies have shown that in hearing people, natural time-varying silent seen speech can access the auditory cortex (left superior temporal regions). Using functional magnetic resonance imaging (fMRI), the present study explored the extent to which this circuitry was activated when seen speech was deprived of its time-varying characteristics. In the scanner, hearing participants were instructed to look for a prespecified visible speech target sequence ("voo" or "ahv") among other monosyllables. In one condition, the image sequence comprised a series of stilled key frames showing apical gestures (e.g., separate frames for "v" and "oo" [from the target] or "ee" and "m" [i.e., from nontarget syllables]). In the other condition, natural speech movement of the same overall segment duration was seen. In contrast to a baseline condition in which the letter "V" was superimposed on a resting face, stilled speech face images generated activation in posterior cortical regions associated with the perception of biological movement, despite the lack of apparent movement in the speech image sequence. Activation was also detected in traditional speech-processing regions including the left inferior frontal (Broca's) area, left superior temporal sulcus (STS), and left supramarginal gyrus (the dorsal aspect of Wernicke's area). Stilled speech sequences also generated activation in the ventral premotor cortex and anterior inferior parietal sulcus bilaterally. Moving faces generated significantly greater cortical activation than stilled face sequences, and in similar regions. However, a number of differences between stilled and moving speech were also observed. In the visual cortex, stilled faces generated relatively more activation in primary visual regions (V1/V2), while visual movement areas (V5/MT+) were activated to a greater extent by moving faces. Cortical regions activated more by naturally moving speaking faces included the auditory cortex (Brodmann's Areas 41/42; lateral parts of Heschl's gyrus) and the left STS and inferior frontal gyrus. Seen speech with normal time-varying characteristics appears to have preferential access to "purely" auditory processing regions specialized for language, possibly via acquired dynamic audiovisual integration mechanisms in STS. When seen speech lacks natural time-varying characteristics, access to speech-processing systems in the left temporal lobe may be achieved predominantly via action-based speech representations, realized in the ventral premotor cortex.     

Neurophysiological studies of auditory verbal hallucinations

We discuss 3 neurophysiological approaches to study auditory verbal hallucinations (AVH). First, we describe "state" (or symptom capture) studies where periods with and without hallucinations are compared "within" a patient. These studies take 2 forms: passive studies, where brain activity during these states is compared, and probe studies, where brain responses to sounds during these states are compared. EEG (electroencephalography) and MEG (magnetoencephalography) data point to frontal and temporal lobe activity, the latter resulting in competition with external sounds for auditory resources. Second, we discuss "trait" studies where EEG and MEG responses to sounds are recorded from patients who hallucinate and those who do not. They suggest a tendency to hallucinate is associated with competition for auditory processing resources. Third, we discuss studies addressing possible mechanisms of AVH, including spontaneous neural activity, abnormal self-monitoring, and dysfunctional interregional communication. While most studies show differences in EEG and MEG responses between patients and controls, far fewer show symptom relationships. We conclude that efforts to understand the pathophysiology of AVH using EEG and MEG have been hindered by poor anatomical resolution of the EEG and MEG measures, poor assessment of symptoms, poor understanding of the phenomenon, poor models of the phenomenon, decoupling of the symptoms from the neurophysiology due to medications and comorbidites, and the possibility that the schizophrenia diagnosis breeds truer than the symptoms it comprises. These problems are common to studies of other psychiatric symptoms and should be considered when attempting to understand the basic neural mechanisms responsible for them.