Locating voices in space: A perceptual model for auditory hallucinations?

Introduction. Auditory hallucinations are often perceived as being located in external auditory space (“outside the head”), like real auditory perceptions, but in the absence of a speaker or other external stimulus. Method. A selective literature review of the spatial phenomenology of auditory hallucinations and the cognitive neuroscience of locating real voices in external space was undertaken. An auditory-perceptual model of external auditory hallucinations was developed in healthy right-handed subjects using functional magnetic resonance imaging and the presentation of speech in virtual acoustic space. Results. Karl Jaspers inextricably linked “reality” and “externality” of auditory hallucinations. Although these two properties do not always occur simultaneously in hallucinating patients, the issue of “externality” is important from both a clinical and neuroscientific perspective. In an auditory-perceptual model of auditory hallucinations, association cortex in the left planum temporale is critically involved in the perception of real voices as located in external space. Right-sided voice stimuli are associated with greater neural response in the dominant (left) auditory cortex than left-sided stimuli. Subjects are better at identifying the spatial location of voices presented on the right than on the left. Conclusion. The auditory-perceptual model described helps identify candidate brain systems likely to be involved in the pathogenesis of auditory hallucinations in schizophrenia, and is distinct from other models, which use concepts of “internal monitoring” and “inner speech”. Its application, in the cognitive neuroscientific investigation of the phenomenology of auditory hallucinations, may shed further light on the mechanisms underlying this distressing experience.     

The cognitive neuropsychiatry of auditory verbal hallucinations: An overview

Introduction. The cognitive neuropsychiatric approach to auditory verbal hallucinations (AVHs) attempts to explain the phenomena in cognitive or information-processing terms and ultimately their brain bases. Methods. A narrative review of the literature and an overview of this special issue of Cognitive Neuropsychiatry. Results. First, an operational definition of AVHs is offered. Next, clues to etiology are derived from a detailed consideration of the clinical phenomenology of “voices”, their form and content. Functional and structural neuroimaging studies suggest the importance of left-side language areas in the generation/perception of AVHs. Conclusions. Existing cognitive neuropsychiatric models provide a useful framework for the understanding of AVHs. However, data need to be applied more specifically to these models so that they may be refined.     

Neural correlates of inner speech and auditory verbal hallucinations: a critical review and theoretical integration

The neuroimaging and neurophysiological literature on inner speech in healthy participants and those who experience auditory verbal hallucinations (AVHs) is reviewed. AVH-hearers in remission and controls do not differ neurologically on tasks involving low levels of verbal self-monitoring (VSM), such as reciting sentences in inner speech. In contrast, on tasks involving high levels of VSM, such as auditory verbal imagery, AVH-hearers in remission show less activation in areas including the middle and superior temporal gyri. This pattern of findings leads to a conundrum, given that mentation involving low levels of VSM is typically held to form the raw material for AVHs. We address this by noting that existing neuroimaging and neurophysiological studies have been based on unexamined assumptions about the form and developmental significance of inner speech. We set out a Vygotskian approach to AVHs which can account for why they are generally experienced as the voice of another person, with specific acoustic properties, and a tendency to take the form of commands. On this approach, which we argue is consistent with the neural correlates evidence, AVHs result from abnormalities in the transition between condensed and expanded dialogic inner speech. Further potential empirical tests of this model are discussed.     

Auditory hallucinations and the P3a: Attention-switching to speech in schizophrenia

BackgroundIn line with emerging research strategies focusing on specific symptoms rather than global syndromes in psychiatric disorders, we examined the functional neural correlates of auditory verbal hallucinations (AHs) in schizophrenia. Recent neuroimaging and behavioural evidence suggest altered early cognitive processes may be seen in patients with AH as a result of limited processing resources.MethodsThe P3a subcomponent of the P300, an event-related potential (ERP) index of early attention switching, was assessed in 12 hallucinating patients (HP), 12 non-hallucinating patients (NP) and 12 healthy controls (HC) within a passive two-tone auditory oddball paradigm using vowel phonemes. P3a amplitudes and latencies were measured in response to across-phoneme changes. Following P3a acquisition, patients indicated the duration, intensity and clarity of their auditory hallucinations during recording.ResultsHallucinating patients exhibited smaller P3a amplitudes than non-hallucinating patients and healthy controls. In HPs, P3a amplitude was negatively correlated with AH trait scores.SignificanceThese findings suggest that AHs are associated with impaired processing of speech as evidenced by altered P3a amplitudes to vowel phonemes. This finding may be due to limited cognitive resources available for incoming external stimuli due to a usurping of finite resources by AHs. The P3a may be a useful non-invasive tool for probing relationships between hallucinatory and neural states within schizophrenia and the manner in which auditory processing is altered in these afflicted patients.     

Language, gesture, and the developing brain

Do language abilities develop in isolation? Are they mediated by a unique neural substrate, a “mental organ” devoted exclusively to language? Or is language built upon more general abilities, shared with other cognitive domains, and mediated by common neural systems? Here, we review results suggesting that language and gesture are “close family”, then turn to evidence that raises questions about how real those “family resemblances” are, summarizing dissociations from our developmental studies of several different child populations. We then examine both these veins of evidence in light of some new findings from the adult neuroimaging literature and suggest a possible reinterpretation of these dissociations as well as new directions for research with both children and adults. © 2002 Wiley Periodicals, Inc. Dev Psychobiol 40: 293–310, 2002. DOI 10.1002/dev.10034     

Impaired verbal self-monitoring in psychosis: effects of state, trait and diagnosis

BACKGROUND: Cognitive models propose that auditory verbal hallucinations arise through defective self-monitoring and external attribution of inner speech. We used a paradigm that engages verbal self-monitoring to examine how deficits in this process are related to symptoms and diagnosis in patients with psychosis. METHOD: We tested 45 patients with schizophrenia. Fifteen had current auditory hallucinations, 15 had a history of (but no current) auditory hallucinations, and 15 had delusions but neither current nor previous hallucinations. We also tested 10 patients with affective psychosis and current auditory hallucinations, and 20 healthy volunteers. Participants read single adjectives aloud while the source and the pitch of the on-line auditory verbal feedback was manipulated, then immediately identified the source of the speech they heard ('self'/'other'/'unsure'). RESULTS: When reading aloud with distorted feedback of their own voice, patients with schizophrenia who had auditory hallucinations were more likely than controls to misidentify its source as 'other'. Patients with delusions but no current hallucinations displayed a similar deficit, although there was a trend for this to be less marked. Patients with a history of hallucinations did not differ from controls. Patients with hallucinations in the context of an affective disorder made more unsure responses rather than misattributions. CONCLUSIONS: Difficulty with source monitoring was related to the acute psychotic state rather than a predisposition to hallucinations, and was evident in patients with affective psychosis as well as schizophrenia. External misattribution of source may reflect an impairment in verbal self-monitoring and/or the appraisal of ambiguous sensory material.     

Internal versus external auditory hallucinations in schizophrenia: symptom and course correlates

Introduction. The auditory hallucinations associated with schizophrenia are phenomenologically diverse. “External” hallucinations classically have been considered to reflect more severe psychopathology than “internal” hallucinations, but empirical support has been equivocal.

Methods. We examined associations of “internal” versus “external” hallucinations with (1) other characteristics of the hallucinations, (2) severity of other symptoms and (3) course of illness variables, in a sample of 97 stable outpatients with schizophrenia or schizoaffective disorder who experienced auditory hallucinations.

Results. Patients with internal hallucinations did not differ from those with external hallucinations on severity of other symptoms. However, they reported their hallucinations to be more emotionally negative, distressing and long-lasting, less controllable and less likely to remit over time. They also were more likely to experience voices commenting, conversing or commanding. However, they also were more likely to have insight into the self-generated nature of their voices. Patients with internal hallucinations were not older, but had a later age of illness onset.

Conclusions. Differences in characteristics of auditory hallucinations are associated with differences in other characteristics of the disorder, and hence may be relevant to identifying subgroups of patients that are more homogeneous with respect to their underlying disease processes.     

THE EFFECT OF GSR CONFIRMED PERCEPTION OF BISENSORY INPUT ON IMMEDIATE VERBAL MEMORY

Following adaptation, Ss learned visually presented paired associate (PA) word lists, while “distracting” verbal material was read aloud to them. Skin resistance was recorded. Ss who received auditory “interference” containing words present in the PA task made fewer errors than controls. An objective scoring method showed that GSR peaks following the onset of relevant words in the “interference” were more frequent than those following control words, confirming Ss' verbal reports of perception of and attention to relevant stimuli. The improved learning could not be accounted for by changes in the tonic level of skin resistance, but seemed to be a direct result of the bimodal input.     

Auditory hallucinations and the P3a: Attention-switching to speech in schizophrenia

Background

In line with emerging research strategies focusing on specific symptoms rather than global syndromes in psychiatric disorders, we examined the functional neural correlates of auditory verbal hallucinations (AHs) in schizophrenia. Recent neuroimaging and behavioural evidence suggest altered early cognitive processes may be seen in patients with AH as a result of limited processing resources.

Methods

The P3a subcomponent of the P300, an event-related potential (ERP) index of early attention switching, was assessed in 12 hallucinating patients (HP), 12 non-hallucinating patients (NP) and 12 healthy controls (HC) within a passive two-tone auditory oddball paradigm using vowel phonemes. P3a amplitudes and latencies were measured in response to across-phoneme changes. Following P3a acquisition, patients indicated the duration, intensity and clarity of their auditory hallucinations during recording.

Results

Hallucinating patients exhibited smaller P3a amplitudes than non-hallucinating patients and healthy controls. In HPs, P3a amplitude was negatively correlated with AH trait scores.

Significance

These findings suggest that AHs are associated with impaired processing of speech as evidenced by altered P3a amplitudes to vowel phonemes. This finding may be due to limited cognitive resources available for incoming external stimuli due to a usurping of finite resources by AHs. The P3a may be a useful non-invasive tool for probing relationships between hallucinatory and neural states within schizophrenia and the manner in which auditory processing is altered in these afflicted patients.     

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

Introduction. The application of neurocognitive models to study schizophrenia has been influential in understanding the nature of this complex and heterogeneous disorder. However, a comprehensive and empirically validated account of auditory hallucinations remains elusive. The aim of this review was to critically assess the current evidence for specific neurocognitive deficits associated with auditory verbal hallucinations (AVHs) in schizophrenia. Methods. A systematic literature search was conducted of research involving three influential cognitive models of auditory hallucinations: those implicating dysfunction in auditory imagery, verbal self-monitoring, and episodic memory. Results. The findings of the review suggested that AVHs have been associated with impaired verbal self-monitoring, impaired memory for self-generated speech, heightened influence of top-down processing on perception, and an externalising response bias. Conclusions. On the basis of the findings of the review a multidimensional model of AVHs is proposed incorporating the identified cognitive deficits and biases.     

Is auditory imagery defective in patients with auditory hallucinations?

BACKGROUND: A variant of the 'inner speech' theory of auditory verbal hallucinations in schizophrenia suggests that there is an abnormality of the relationship between the 'inner voice' and 'inner ear', such that hallucinators are unable to distinguish inner 'imagined' speech from real external speech, and so misrecognize inner speech as alien. METHODS: Five experiments were carried out comparing 12 schizophrenic patients who were highly prone to hallucinate, with seven patients who were not, on a series of auditory imagery tasks that are differentially dependent on inner voice/inner ear partnership for successful performance: parsing meaningful letter/number strings; the verbal transformation effect; phoneme judgements; pitch judgements, and homophony and rhyme judgements. RESULTS: Contrary to our hypothesis, there was no evidence that the group with the propensity to hallucinate were impaired on tasks requiring normal inner ear/inner voice partnership. CONCLUSIONS: Together with previous work indicating no impairment of the phonological loop in patients who hallucinate, these results suggest that inner speech and auditory verbal hallucinations are not connected in a simplistic or direct way. Indeed, a reappraisal of psychological models of hallucinations in general may be warranted.     

Cortical potential imaging of episodic memory encoding

Previous findings suggest that episodic memory encoding is subserved by different brain structures that interplay and transform experience into memories. The present study aims to identify topographic location of the underlying neural generators, and correlate their activities with the subsequent memory effect, using electrophysiological neuroimaging of the event-related potentials (ERPs) recorded from 11 healthy subjects participating in word encoding tasks. Cortical potentials were imaged noninvasively from scalp ERPs. Different levels of brain activation were found in the left inferior prefrontal, left temporal and left parietal lobes with different latencies after onset of event. It is concluded that these regions work jointly across both spatial and temporal domains to promote verbal memory formation.     

Articulatory rehearsal in verbal working memory: a possible neurocognitive endophenotype that differentiates between schizophrenia and schizoaffective disorder

Recent fMRI studies have identified brain systems underlying different components of working memory in healthy individuals. The aim of this study was to compare the functional integrity of these neural networks in terms of behavioural performance in patients with schizophrenia, schizoaffective disorder and healthy controls. In order to detect specific working memory deficits based on dysfunctions of underlying brain circuits we used the same verbal and visuospatial Sternberg item-recognition tasks as in previous neuroimaging studies. Clinical and performance data from matched groups consisting of 14 subjects each were statistically analyzed. Schizophrenic patients exhibited pronounced impairments of both verbal and visuospatial working memory, whereas verbal working memory performance was preserved in schizoaffective patients. The findings provide first evidence that dysfunction of a brain system subserving articulatory rehearsal could represent a biological marker which differentiates between schizophrenia and schizoaffective disorder.     

Functional neuroimaging of grammatical class: Ambiguous and unambiguous nouns and verbs

Neuropsychological and neuroimaging studies of grammatical-class differences suggest that nouns and verbs may be associated with different brain regions. The current functional magnetic resonance imaging (fMRI) study focused on auditory grammaticality judgements of two-word stimuli consisting of noun/verb ambiguous and unambiguous nouns and verbs preceded by either “the” or “to”. The fMRI results showed effects of class ambiguity in the left inferior frontal gyrus, possibly due to greater selection demands, and effects of grammaticality (“yes” vs. “no” response) in left superior temporal gyrus, consistent with greater activation for trials with greater conflict. In addition, posterior left temporal lobe regions showed increased activity on unambiguous trials for verbs than for nouns, consistent with prior imaging studies. Thus, in a task specifically focused on the grammatical (rather than semantic) aspects of words and that used morphologically simple nouns and verbs controlled for imageability, verbs preferentially activated posterior temporal but not frontal lobe regions. However, for ambiguous trials in this same region, nouns showed greater activation than verbs, suggesting that these effects can be modulated by class ambiguity.     

Contributions of emotional prosody comprehension deficits to the formation of auditory verbal hallucinations in schizophrenia

Deficits in emotional processing have been widely described in schizophrenia. Associations of positive symptoms with poor emotional prosody comprehension (EPC) have been reported at the phenomenological, behavioral, and neural levels. This review focuses on the relation between emotional processing deficits and auditory verbal hallucinations (AVH). We explore the possibility that the relation between AVH and EPC in schizophrenia might be mediated by the disruption of a common mechanism intrinsic to auditory processing, and that, moreover, prosodic feature processing deficits play a pivotal role in the formation of AVH. The review concludes with proposing a mechanism by which AVH are constituted and showing how different aspects of our neuropsychological model can explain the constellation of subjective experiences which occur in relation to AVH.     

Auditory hallucinations and PTSD in ex-POWS

Literature has suggested that auditory hallucinations might be prevalent in the general population and could be linked to the experience of trauma. This prospective study examines the prevalence of auditory hallucinations in trauma survivors and its association with posttraumatic stress disorder (PTSD) symptoms, over time. Former prisoners of war (ex-POWs) from the 1973 Yom Kippur War (n = 99) with and without PTSD and comparable veterans (n = 103) were assessed twice, in 1991 (T1) and 2003 (T2) in regard to auditory hallucinations and PTSD symptoms. Findings indicated that ex-POWs who suffered from PTSD reported higher levels of auditory hallucinations at T2 as well as increased hallucinations over time, compared to ex-POWs without PTSD and combatants who did not endure captivity. The relation between PTSD and auditory hallucinations was unidirectional, so that the PTSD overall score at T1 predicted an increase in auditory hallucinations between T1 and T2, but not vice versa. Assessing the role of PTSD clusters in predicting hallucinations revealed that intrusion symptoms had a unique contribution, compared to avoidance and hyperarousal symptoms. The findings suggest that auditory hallucinations might be a consequence of the posttraumatic reaction among veterans.     

Is there evidence for neural compensation in attention deficit hyperactivity disorder? A review of the functional neuroimaging literature

This article reviews evidence for the presence of a compensatory, alternative, neural system and its possible link to associated processing strategies in children and adults with attention deficit hyperactivity disorder (ADHD). The article presents findings on a region by region basis that suggests ADHD should be characterized not only by neural hypo-activity, as it is commonly thought but neural hyperactivity as well, in regions of the brain that may relate to compensatory brain and behavioral functioning. In this context studies from the functional neuroimaging literature are reviewed. We hypothesize that impaired prefrontal (PFC) and anterior cingulate (ACC) cortex function in ADHD reduces the ability to optimally recruit subsidiary brain regions and strategies to perform cognitive tasks. The authors conclude that healthy individuals can recruit brain regions using visual, spatial or verbal rehearsal for tasks as needed. In contrast, individuals with ADHD may be less able to engage higher order executive systems to flexibly recruit brain regions to match given task demands. This may result in greater reliance on neuroanatomy that is associated with visual, spatial, and motoric processing rather than verbal strategies. The authors speculate that this impaired flexibility in recruiting brain regions and associated strategies limits adaptation to new cognitive demands as they present and may require more effortful processing.     

A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis

Whether we feel sympathy for another, listen to our heartbeat, experience pain or negotiate, the insular cortex is thought to integrate perceptions, emotions, thoughts, and plans into one subjective image of “our world”. The insula has hence been ascribed an integrative role, linking information from diverse functional systems. Nevertheless, various anatomical and functional studies in humans and non-human primates also indicate a functional differentiation of this region. In order to investigate this functional differentiation as well as the mechanisms of the functional integration in the insula, we performed activation-likelihood-estimation (ALE) meta-analyses of 1,768 functional neuroimaging experiments. The analysis revealed four functionally distinct regions on the human insula, which map to the social-emotional, the sensorimotor, the olfacto-gustatory, and the cognitive network of the brain. Sensorimotor tasks activated the mid-posterior and social-emotional tasks the anterior-ventral insula. In the central insula activation by olfacto-gustatory stimuli was found, and cognitive tasks elicited activation in the anterior-dorsal region. A conjunction analysis across these domains revealed that aside from basic somatosensory and motor processes all tested functions overlapped on the anterior-dorsal insula. This overlap might constitute a correlate for a functional integration between different functional systems and thus reflect a link between them necessary to integrate different qualities into a coherent experience of the world and setting the context for thoughts and actions.     

Verbal self-monitoring and auditory verbal hallucinations in patients with schizophrenia

BACKGROUND: Contemporary cognitive models of auditory verbal hallucinations propose that they arise through defective self-monitoring. We used a paradigm that engages verbal self-monitoring to investigate this theory in patients with schizophrenia. METHODS: Ten patients with auditory verbal hallucinations and delusions (hallucinators), eight patients with delusions but no hallucinations (non-hallucinators), and 20 non-psychiatric control subjects were tested. Participants read single adjectives aloud, under the following randomized conditions: reading aloud; reading aloud with acoustic distortion of their own voice; reading aloud with alien feedback (someone else's voice); and reading aloud with distorted alien feedback. Immediately after articulating each word, participants identified the source of the speech they heard ('self'/'other'/'unsure'), via a button press. Response choice and reaction time were recorded. RESULTS: When reading aloud with distorted feedback of their own voice, patients in both groups made more errors than controls; they either misidentified its source or were unsure. Hallucinators were particularly prone to misattributing their distorted voice to someone else, and were more likely to make errors when the words presented were derogatory. Both patient groups made faster decisions than controls about the source of distorted or alien speech, but faster responses were only associated with errors in the former condition. CONCLUSIONS: Impaired verbal self-monitoring was evident in both hallucinators and non-hallucinators. As both groups had delusions, the results suggest an association between delusions and impaired judgements about ambiguous sensory stimuli. The specific tendency of hallucinators to misattribute their distorted voice to someone else may reflect impaired awareness of internally generated verbal material.     

Visual hallucinations in schizophrenia: confusion between imagination and perception

OBJECTIVE: An association between hallucinations and reality-monitoring deficit has been repeatedly observed in patients with schizophrenia. Most data concern auditory/verbal hallucinations. The aim of this study was to investigate the association between visual hallucinations and a specific type of reality-monitoring deficit, namely confusion between imagined and perceived pictures. METHOD: Forty-one patients with schizophrenia and 43 healthy control participants completed a reality-monitoring task. Thirty-two items were presented either as written words or as pictures. After the presentation phase, participants had to recognize the target words and pictures among distractors, and then remember their mode of presentation. RESULTS: All groups of participants recognized the pictures better than the words, except the patients with visual hallucinations, who presented the opposite pattern. The participants with visual hallucinations made more misattributions to pictures than did the others, and higher ratings of visual hallucinations were correlated with increased tendency to remember words as pictures. No association with auditory hallucinations was revealed. CONCLUSIONS: Our data suggest that visual hallucinations are associated with confusion between visual mental images and perception.