Selective speech perception alterations in schizophrenic patients reporting hallucinated "voices"

OBJECTIVE: The authors tested a model of hallucinated "voices" based on a neural network computer simulation of disordered speech perception. METHOD: Twenty-four patients with schizophrenia spectrum disorders who reported hallucinated voices were compared with 21 patients with schizophrenia spectrum disorders who did not report voices and 26 normal subjects. Narrative speech perception was assessed through use of a masked speech tracking task with three levels of superimposed phonetic noise. A sentence repetition task was used to assess grammar-dependent verbal working memory, and an auditory continuous performance task was used to assess nonlanguage attention. RESULTS: Masked speech tracking task and sentence repetition performance by hallucinating patients was impaired relative to both nonhallucinating patients and normal subjects. Although both hallucinating and nonhallucinating patients demonstrated auditory attention impairments when compared to normal subjects, the two patient groups did not differ with respect to these variables. CONCLUSIONS: Results support the hypothesis that hallucinated voices in schizophrenia arise from disrupted speech perception and verbal working memory systems rather than from nonlanguage cognitive or attentional deficits.     

An fMRI study of auditory hallucinations in patients with epilepsy

Purpose : The aim of the study was to investigate behavioral and brain activation in nonpsychotic hallucinating individuals. Auditory hallucinations are reported by patients with epilepsy, although less frequent than visual hallucinations are. If behavioral and neuronal activation patterns in hallucinating patients with epilepsy are found to be similar to what has been found in hallucinating patients with schizophrenia, this would support a unique neuronal representation for auditory hallucinations cutting across diagnostic groups. Methods : We report behavioral and functional magnetic resonance imaging (fMRI) data from six epilepsy patients experiencing auditory hallucinations compared with six healthy control subjects. The participants had to report which of two simultaneously presented simple speech sounds they perceived on each trial, using a dichotic stimulus presentation mode. Results : The results showed that the patients failed to show an expected right ear advantage on the task, and they also showed significantly reduced activation in temporal, frontal, and cingulate cortex areas. Discussion : The results are discussed in relation to a view that neuropsychological and functional neuroimaging indices of auditory hallucinations may be orthogonal to diagnostic category and not unique to patients with schizophrenia.     

Increased susceptibility to auditory conditioning in hallucinating schizophrenic patients: a preliminary investigation

Auditory hallucinations have been elicited in the laboratory after repeated pairings of a tone (unconditioned stimulus) with a light (conditioned stimulus), until the presentation of the light alone resulted in subjects hearing the tone. This auditory sensory-conditioning phenomenon was first reported in normal subjects over a half-century ago. But the model remains, to date, untested in actively hallucinating patients. If sensory-conditioning mechanisms actually mediate the occurrence of clinical hallucinations, one would expect that hallucinating patients would more readily acquire and be more resistant to extinguish a conditioned hallucination than nonhallucinating psychotic patients. The present study examined the susceptibility of 15 hallucinating and 15 nonhallucinating acute schizophrenic inpatients to acquire and maintain a sensory-conditioned hallucination response. Consistent with the auditory sensory-conditioning model, evidence suggests that hallucinating patients acquire and maintain sensory-conditioned hallucinations more quickly than their nonhallucinating counterparts. Results are discussed in terms of hallucinators' susceptibility to sensory conditioning and suggestibility as important factors underlying hallucinatory behavior. The findings are interpreted with respect to the behavioral mechanisms underlying psychotic symptom formation.     

The psycholinguistics of auditory hallucinations

Abstract

The purpose of this study was to investigate psycholinguistic behaviour, as language processing, verbal reasoning and discourse production, in hallucinating and non-hallucinating subjects suffering from psychotic disorders. Nineteen hallucinating and 13 non-hallucinating subjects were assessed on a battery of tests of psycholinguistic functioning with complementary measures of abstraction and discourse cohesion. The experimental groups were matched with healthy controls by age, gender and education. Only a discourse score differentiated the patient groups. No tests of receptive or executive psycholinguistic functioning or abstraction distinguished the patient groups with hallucinating or non-hallucinating behaviour, thus disorders of linguistic processing in these domains are not specific to patients with auditory hallucinations. The patient groups did differ from their healthy controls on tests that required abstract processing and reasoning. There is also some evidence that both patient groups had difficulty with lexical retrieval or word generation, and with memory and comprehension. The conclusions support a concept of dysfunction of the executive system that facilitates linguistic processing in psychotic disorders. They also support further investigation of a comprehension deficit in psychosis and the use of discourse analysis as a diagnostic tool in this heterogeneous disease.     

Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging

BACKGROUND: Perceptions of speech in the absence of an auditory stimulus (auditory verbal hallucinations) are a cardinal feature of schizophrenia. Functional neuroimaging provides a powerful means of measuring neural activity during auditory hallucinations, but the results from previous studies have been inconsistent. This may reflect the acquisition of small numbers of images in each subject and the confounding effects of patients actively signaling when hallucinations occur. METHODS: We examined 6 patients with schizophrenia who were experiencing frequent auditory hallucinations, using a novel functional magnetic resonance imaging method that permitted the measurement of spontaneous neural activity without requiring subjects to signal when hallucinations occurred. Approximately 50 individual scans were acquired at unpredictable intervals in each subject while they were intermittently hallucinating. Immediately after each scan, subjects reported whether they had been hallucinating at that instant. Neural activity when patients were and were not experiencing hallucinations was compared in each subject and the group as a whole. RESULTS: Auditory hallucinations were associated with activation in the inferior frontal/insular, anterior cingulate, and temporal cortex bilaterally (with greater responses on the right), the right thalamus and inferior colliculus, and the left hippocampus and parahippocampal cortex (P<.0001). CONCLUSIONS: Auditory hallucinations may be mediated by a distributed network of cortical and subcortical areas. Previous neuroimaging studies of auditory hallucinations may have identified different components of this network.     

Abnormal brain response during the auditory emotional processing in schizophrenic patients with chronic auditory hallucinations

OBJECTIVE: Few neuroimaging studies have been conducted regarding clinical associations between auditory hallucinations (AHs) and affective disturbances in patients with schizophrenia. This study aimed to elucidate the neurobiological basis of emotional disturbances in schizophrenic patients with persisting AHs. METHODS: Using functional magnetic resonance imaging (fMRI), the cortical responsiveness during the processing of laughing and crying sounds was measured and compared between 14 hallucinating schizophrenic patients, 14 nonhallucinating schizophrenic patients and 28 normal controls. RESULTS: The hallucinating patients showed differential neural activities in various areas including the amygdala, the hippocampus, the cingulate, the prefrontal cortex, and the parietal cortex, compared with the nonhallucinating patients and the normal controls. In particular, compared with the nonhallucinators, the hallucinators revealed reduced activation in the left amygdala and the bilateral hippocampus during the processing of crying sounds. CONCLUSION: Our findings suggest that the persistence of AHs in schizophrenia may induce functional disturbances of the emotion-related interconnected neural networks, including reduced responsiveness in the amygdala and hippocampus to negative stimuli.     

The role of brief instructions and suggestibility in the elicitation of auditory and visual hallucinations in normal and psychiatric subjects

The present study is an investigation of the elicitation of auditory and visual hallucinations by brief instructions and the relationship of the report of hallucinatory-type experiences to standard measures of suggestibility. Two experiments were carried out. The first used normal subjects predisposed or not predisposed to hallucinate, as assessed by the Launay-Slade Hallucination Scale (LSHS-A). The second used hallucinating and nonhallucinating psychiatric patients. The high LSHS-A scorers and the hallucinating psychiatric patients were significantly more likely to hear suggested sounds than were their respective controls. High LSHS-A scorers were also significantly more likely to see suggested objects than were their respective controls, although this finding was not replicated in the psychiatric subjects. No significant differences on measures of suggestibility were found between the groups, although in the psychiatric group Barber Test Suggestion and Subjective Involvement scores correlated positively with LSHS-A scores.     

Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study

A [H(2)(15)O] PET correlation analysis technique was employed to correlate brain activations associated with self-reports of auditory hallucinations in hallucinating patients (n=8) and perception of transient, random human speech in non-hallucinating (n=7) patients and normal control subjects (n=8). Perception of externally generated human speech amongst the non-hallucinating and normal control participants was associated with a consistent pattern of extensive bilateral auditory cortex activation (Brodmann areas 40/41/42/22). Hallucinating participants demonstrated a network of cortical activations including bilateral auditory cortex, left limbic regions, right medial frontal and right prefrontal regions. The observed pattern of activation is consistent with models of auditory hallucinations as mis-remembered episodic memories of speech.     

Strategies of disattention and auditory hallucinations in schizophrenics

Disattentional strategies used by schizophrenics to attenuate auditory stimulation from the environment were proposed as extraordinary conditions of attention which facilitate the misperception of lexical thought as a voice and create an auditory hallucination. Two strategies were studied. The switching strategy involved concentration upon an external visual display to prevent a clearly audible list of words from registering. The holding strategy required mentally repeating a word in the list so as to ignore the words that followed. Process (N = 32) and reactive (N = 32) schizophrenics, 46 of whom had a history of auditory hallucinations, served as subjects. Effectiveness of the two disattentional strategies was tested by subsequent inability of the schizophrenic to recognize words from the taped list. Process schizophrenics with auditory hallucinations were able to use switching effectively but not holding. In contrast, reactive schizophrenics suffering auditory hallucinations successfully used holding but not switching. Both effects were confirmed relative to hallucinating controls given standard memory instructions. Strategy effects were not apparent in nonhallucinating schizophrenics. These results suggest that different disattentional strategies may have been practiced by hallucinating schizophrenics in keeping with their premorbid status and style of attention deployment. A proposal functionally relating disattention to the genesis of auditory hallucinations was suggested.     

Emotional prosodic processing in auditory hallucinations

Deficits in emotional prosodic processing, the expression of emotions in voice, have been widely reported in patients with schizophrenia, not only in comprehending emotional prosody but also expressing it. Given that prosodic cues are important in memory for voice and speaker identity, Cutting has proposed that prosodic deficits may contribute to the misattribution that appears to occur in auditory hallucinations in psychosis. The present study compared hallucinating patients with schizophrenia, non-hallucinating patients and normal controls on an emotional prosodic processing task. It was hypothesised that hallucinators would demonstrate greater deficits in emotional prosodic processing than non-hallucinators and normal controls. Participants were 67 patients with a diagnosis of schizophrenia or schizoaffective disorder (hallucinating = 38, non-hallucinating = 29) and 31 normal controls. The prosodic processing task used in this study comprised a series of semantically neutral sentences expressed in happy, sad and neutral voices which were rated on a 7-point Likert scale from sad (− 3) through neutral (0) to happy (+ 3). Significant deficits in the prosodic processing tasks were found in hallucinating patients compared to non-hallucinating patients and normal controls. No significant differences were observed between non-hallucinating patients and normal controls. In the present study, patients experiencing auditory hallucinations were not as successful in recognising and using prosodic cues as the non-hallucinating patients. These results are consistent with Cutting's hypothesis, that prosodic dysfunction may mediate the misattribution of auditory hallucinations.     

Reversibility of abnormal auditory findings in cerebral hemisphere lesions

Three cases are presented to illustrate the reversibility of abnormal central auditory function in patients with cerebral hemisphere lesions. In 1 patient, abnormal scores with dichotic simultaneous-binaural and competing sentence discrimination tests in the ear contralateral to the affected hemisphere returned to normal after evacuation of an intracerebral hematoma of the right temporal lobe. In the other 2 cases, abnormal dichotic speech discrimination test scores in the left ear improved for a period of time after decompression and subtotal removal of astrocytomas deep in the parietal lobe of the right hemisphere. Eventually, central auditory test findings became abnormal again in these 2 cases which was consistent with the deteriorating condition of the patients. Findings in these 3 cases indicate that distorted and dichotic speech discrimination tests yield information which may be useful in monitoring the course of patients with reversible as well as progressive lesions of the brain.     

Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia.

BACKGROUND: Previous studies have reported significant correlations, indicating an emerging relationship, between severity of auditory hallucinations and reduced size of temporal lobe cortical regions implicated in language processing. The present study used high-resolution magnetic resonance imaging (MRI) scanning, along with assessment of functional lateralization via a dichotic listening task (DLT), to extend these findings. METHODS: Thirty patients with schizophrenia and a history of auditory hallucinations participated in the study. All were completely right-handed. Eleven subjects were currently hallucinating at the time of the study. Volumetric T1-weighted MRI scans were obtained and regions of interest were manually traced using the BRAINS package (Andreasen et al 1993). Whole brain, bilateral temporal lobe, and anterior superior temporal gyrus volumes were calculated. Subjects completed a binaural consonant-vowel DLT. RESULTS: Increased severity of hallucinatory experience was significantly associated with smaller left anterior superior temporal gyrus volumes. Current hallucinators demonstrated a reduction in right ear advantage on the DLT. CONCLUSIONS: The results suggest that auditory hallucinations are subserved by a trait-like dysfunction in language-related neural networks, of which the superior temporal cortex forms one component. The findings are also consistent with theories proposing abnormal lateralization in the etiology of auditory hallucinations.     

Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations

CONTEXT: A forward model of intended thoughts and actions prepares sensory cortex for sensations that are a consequence of those actions. Imprecision of the corollary discharge in schizophrenia may contribute to the misperception of inner experiences and thoughts as "voices" or auditory hallucinations. OBJECTIVES: To assess the precision of the forward model in schizophrenia using the N100 component of the auditory event-related potential to speech that is altered or unaltered, in real time, as it is being spoken. To assess the relationship between auditory hallucinations and the imprecision of the corollary discharge. DESIGN: Prospective case-control study. SETTING: Community mental health centers and Palo Alto Veterans Affairs Health Care System, Palo Alto, Calif. PARTICIPANTS: Twenty patients with schizophrenia and 17 sex- and age-matched healthy control subjects. MAIN OUTCOME MEASURES: N100 responses to auditory feedback, which was altered by pitch-shifting the self-voice, substituting an alien voice, or pitch-shifting the alien voice. On each trial, subjects judged whether feedback was "self," "other," or "unsure." Clinical ratings were used to assess severity of auditory hallucinations in patients. RESULTS: In controls, N100 to unaltered self-voice feedback was dampened relative to N100 to altered self-voice or alien auditory feedback. This pattern was not seen in hallucinating patients. This imprecision correlated with the severity of hallucinations and with the percentage of misattribution errors. CONCLUSION: These data support a connection between auditory verbal hallucinations and the imprecision of the corollary discharge heralding the sensory consequences of thoughts and actions.     

Left-Dominant Temporal-Frontal Hypercoupling in Schizophrenia Patients With Hallucinations During Speech Perception

Background:

Task-based functional neuroimaging studies of schizophrenia have not yet replicated the increased coordinated hyperactivity in speech-related brain regions that is reported with symptom-capture and resting-state studies of hallucinations. This may be due to suboptimal selection of cognitive tasks.

Methods:

In the current study, we used a task that allowed experimental manipulation of control over verbal material and compared brain activity between 23 schizophrenia patients (10 hallucinators, 13 nonhallucinators), 22 psychiatric (bipolar), and 27 healthy controls. Two conditions were presented, one involving inner verbal thought (in which control over verbal material was required) and another involving speech perception (SP; in which control verbal material was not required).

Results:

A functional connectivity analysis resulted in a left-dominant temporal-frontal network that included speech-related auditory and motor regions and showed hypercoupling in past-week hallucinating schizophrenia patients (relative to nonhallucinating patients) during SP only.

Conclusions:

These findings replicate our previous work showing generalized speech-related functional network hypercoupling in schizophrenia during inner verbal thought and SP, but extend them by suggesting that hypercoupling is related to past-week hallucination severity scores during SP only, when control over verbal material is not required. This result opens the possibility that practicing control over inner verbal thought processes may decrease the likelihood or severity of hallucinations.Key words: schizophrenia, inner speech, speech perception, functional magnetic resonance imaging, functional connectivity     

Comparison of auditory deficits associated with neglect and auditory cortex lesions

In contrast to lesions of the visual and somatosensory cortex, lesions of the auditory cortex are not associated with self-evident contralesional deficits. Only when two or more stimuli are presented simultaneously to the left and right, contralesional extinction has been observed after unilateral lesions of the auditory cortex. Because auditory extinction is also considered a sign of neglect, clinical separation of auditory neglect from deficits caused by lesions of the auditory cortex is challenging. Here, we directly compared a number of tests previously used for either auditory-cortex lesions or neglect in 29 controls and 27 patients suffering from unilateral auditory-cortex lesions, neglect, or both. The results showed that a dichotic-speech test revealed similar amounts of extinction for both auditory cortex lesions and neglect. Similar results were obtained for words lateralized by inter-aural time differences. Consistent extinction after auditory cortex lesions was also observed in a dichotic detection task. Neglect patients showed more general problems with target detection but no consistent extinction in the dichotic detection task. In contrast, auditory lateralization perception was biased toward the right in neglect but showed considerably less disruption by auditory cortex lesions. Lateralization of auditory-evoked magnetic fields in auditory cortex was highly correlated with extinction in the dichotic target-detection task. Moreover, activity in the right primary auditory cortex was somewhat reduced in neglect patients. The results confirm that auditory extinction is observed with lesions of the auditory cortex and auditory neglect. A distinction can nevertheless be made with dichotic target-detection tasks, auditory-lateralization perception, and magnetoencephalography.     

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

OBJECTIVE: This study investigated the functional neuroanatomy of inner speech and auditory verbal imagery in schizophrenic patients predisposed to auditory hallucinations. METHOD: Eight patients with schizophrenia with a history of prominent auditory hallucinations and six comparison subjects underwent functional magnetic resonance imaging while generating inner speech or imagining external speech. RESULTS: Patients showed no differences while generating inner speech but experienced a relatively attenuated response in the posterior cerebellar cortex, hippocampi, and lenticular nuclei bilaterally and the right thalamus, middle and superior temporal cortex, and left nucleus accumbens during auditory verbal imagery. CONCLUSIONS: Patients with schizophrenia who were prone to auditory hallucinations show attenuated activation when processing inner speech in areas implicated in verbal self-monitoring.     

Exploration of the auditory system in humans: From click to speech auditory brainstem responses

There is a growing and unprecedented interest in the objective evaluation of the subcortical processes that are involved in speech perception, with potential clinical applications in speech and language impairments. Here, we review the studies illustrating the development of electrophysiological methods for assessing speech encoding in the human brainstem: from the pioneer recordings of click-evoked auditory brainstem responses (ABR), via studies of frequency-following responses (FFR) to the most recent measurements of speech ABR (SABR) or ABR in response to speech sounds. Recent research on SABR has provided new insights in the understanding of subcortical auditory processing mechanisms. The SABR test is an objective and non-invasive tool for assessing individual capacity of speech encoding in the brainstem. SABR characteristics are potentially useful both as a diagnosis tool of speech encoding deficits and as an assessment tool of the efficacy of rehabilitation programs in patients with learning and/or auditory processing disorders.     

Deficient auditory interhemispheric transfer in patients with PAX6 mutations

PAX6 mutations are associated with absence/hypoplasia of the anterior commissure and reduction in the callosal area in humans. Both of these structures contain auditory interhemispheric fibers. The aim of this study was to characterize central auditory function in patients with a PAX6 mutation. We conducted central auditory tests (dichotic speech, pattern, and gaps in noise tests) on eight subjects with a PAX6 mutation and eight age- and sex-matched controls. Brain magnetic resonance imaging showed absent/hypoplastic anterior commissure in six and a hypoplastic corpus callosum in three PAX6 subjects. The control group gave normal central auditory tests results. All the PAX6 subjects gave abnormal results in at least two tests that require interhemispheric transfer, and all but one gave normal results in a test not requiring interhemispheric transfer. The left ear scores in the dichotic speech tests was significantly lower in the PAX6 than in the control group. These results are consistent with deficient auditory interhemispheric transfer in patients with a PAX6 mutation, which may be attributable to structural and/or functional abnormalities of the anterior commisure and corpus callosum, although the exact contribution of these two formations to our findings remains unclear. Our unique findings broaden the possible functions of PAX6 to include neurodevelopmental roles in higher order auditory processing.     

Are auditory-verbal hallucinations associated with auditory affective processing deficits?

We investigated whether the presence of auditory-verbal hallucinations (AVH) was associated with impaired auditory affect perception. Controls, schizophrenia patients with a history of AVH (AVH) or with no history of AVH (NAVH) completed four perceptual auditory affect tasks. The tasks used either non-verbal/non-semantic or verbal/semantic stimuli. AVH patients showed significant impairments on a non-verbal task requiring the recognition of environmental sounds, this was particularly so for the affective stimuli and not the neutral valance stimuli. Thus, confirming auditory affect deficits in AVH patients. AVH patients also showed reduced right ear performance on a dichotic listening task. Conversely, both patient groups showed impairments on auditory affect tasks that used verbal/semantic stimuli; as these tasks require proficient semantic processing we speculated that significant semantic impairments in schizophrenia masked the additional auditory affect deficits present in the AVH group. The overall results support the notion that patients with AVH have increased liability for auditory affect perception deficits.