Real-Time Functional Magnetic Resonance Imaging Neurofeedback for the Relief of Distressing Auditory-Verbal Hallucinations: Methodological and Empirical Advances.

Auditory-verbal hallucinations (AVH) are often associated with high levels of distress and disability in individuals with schizophrenia-spectrum disorders. In around 30% of individuals with distressing AVH and diagnosed with schizophrenia, traditional antipsychotic drugs have little or no effect. Thus, it is important to develop mechanistic models of AVH to inform new treatments. Recently a small number of studies have begun to explore the use of real-time functional magnetic resonance imaging neurofeedback (rtfMRI-NF) for the treatment of AVH in individuals with schizophrenia. rtfMRI-NF protocols have been developed to provide feedback about brain activation in real time to enable participants to progressively achieve voluntary control over their brain activity. We offer a conceptual review of the background and general features of neurofeedback procedures before summarizing and evaluating existing mechanistic models of AVH to identify feasible neural targets for the application of rtfMRI-NF as a potential treatment. We consider methodological issues, including the choice of localizers and practicalities in logistics when setting up neurofeedback procedures in a clinical setting. We discuss clinical considerations relating to the use of rtfMRI-NF for AVH in individuals distressed by their experiences and put forward a number of questions and recommendations about best practice. Lastly, we conclude by offering suggestions for new avenues for neurofeedback methodology and mechanistic targets in relation to the research and treatment of AVH.

Reading characters in voices: Ratings of personality characteristics from voices predict proneness to auditory verbal hallucinations.

People rapidly make first impressions of others, often based on very little information-minimal exposure to faces or voices is sufficient for humans to make up their mind about personality of others. While there has been considerable research on voice personality perception, much less is known about its relevance to hallucination-proneness, despite auditory hallucinations being frequently perceived as personified social agents. The present paper reports two studies investigating the relation between voice personality perception and hallucination-proneness in non-clinical samples. A voice personality perception task was created, in which participants rated short voice recordings on four personality characteristics, relating to dimensions of the voice's perceived Valence and Dominance. Hierarchical regression was used to assess contributions of Valence and Dominance voice personality ratings to hallucination-proneness scores, controlling for paranoia-proneness and vividness of mental imagery. Results from Study 1 suggested that high ratings of voices as dominant might be related to high hallucination-proneness; however, this relation seemed to be dependent on reported levels of paranoid thinking. In Study 2, we show that hallucination-proneness was associated with high ratings of voice dominance, and this was independent of paranoia and imagery abilities scores, both of which were found to be significant predictors of hallucination-proneness. Results from Study 2 suggest an interaction between gender of participants and the gender of the voice actor, where only ratings of own gender voices on Dominance characteristics are related to hallucination-proneness scores. These results are important for understanding the perception of characterful features of voices and its significance for psychopathology.

Musical hallucinations, musical imagery, and earworms: A new phenomenological survey.

Musical hallucinations (MH) account for a significant proportion of auditory hallucinations, but there is a relative lack of research into their phenomenology. In contrast, much research has focused on other forms of internally generated musical experience, such as earworms (involuntary and repetitive inner music), showing that they can vary in perceived control, repetitiveness, and in their effect on mood. We conducted a large online survey (N = 270), including 44 participants with MH, asking participants to rate imagery, earworms, or MH on several variables. MH were reported as occurring less frequently, with less controllability, less lyrical content, and lower familiarity, than other forms of inner music. MH were also less likely to be reported by participants with higher levels of musical expertise. The findings are outlined in relation to other forms of hallucinatory experience and inner music, and their implications for psychological models of hallucinations discussed.

Distinct processing of ambiguous speech in people with non-clinical auditory verbal hallucinations.

Auditory verbal hallucinations (hearing voices) are typically associated with psychosis, but a minority of the general population also experience them frequently and without distress. Such 'non-clinical' experiences offer a rare and unique opportunity to study hallucinations apart from confounding clinical factors, thus allowing for the identification of symptom-specific mechanisms. Recent theories propose that hallucinations result from an imbalance of prior expectation and sensory information, but whether such an imbalance also influences auditory-perceptual processes remains unknown. We examine for the first time the cortical processing of ambiguous speech in people without psychosis who regularly hear voices. Twelve non-clinical voice-hearers and 17 matched controls completed a functional magnetic resonance imaging scan while passively listening to degraded speech ('sine-wave' speech), that was either potentially intelligible or unintelligible. Voice-hearers reported recognizing the presence of speech in the stimuli before controls, and before being explicitly informed of its intelligibility. Across both groups, intelligible sine-wave speech engaged a typical left-lateralized speech processing network. Notably, however, voice-hearers showed stronger intelligibility responses than controls in the dorsal anterior cingulate cortex and in the superior frontal gyrus. This suggests an enhanced involvement of attention and sensorimotor processes, selectively when speech was potentially intelligible. Altogether, these behavioural and neural findings indicate that people with hallucinatory experiences show distinct responses to meaningful auditory stimuli. A greater weighting towards prior knowledge and expectation might cause non-veridical auditory sensations in these individuals, but it might also spontaneously facilitate perceptual processing where such knowledge is required. This has implications for the understanding of hallucinations in clinical and non-clinical populations, and is consistent with current 'predictive processing' theories of psychosis.

The effect of auditory verbal imagery on signal detection in hallucination-prone individuals.

Cognitive models have suggested that auditory hallucinations occur when internal mental events, such as inner speech or auditory verbal imagery (AVI), are misattributed to an external source. This has been supported by numerous studies indicating that individuals who experience hallucinations tend to perform in a biased manner on tasks that require them to distinguish self-generated from non-self-generated perceptions. However, these tasks have typically been of limited relevance to inner speech models of hallucinations, because they have not manipulated the AVI that participants used during the task. Here, a new paradigm was employed to investigate the interaction between imagery and perception, in which a healthy, non-clinical sample of participants were instructed to use AVI whilst completing an auditory signal detection task. It was hypothesized that AVI-usage would cause participants to perform in a biased manner, therefore falsely detecting more voices in bursts of noise. In Experiment 1, when cued to generate AVI, highly hallucination-prone participants showed a lower response bias than when performing a standard signal detection task, being more willing to report the presence of a voice in the noise. Participants not prone to hallucinations performed no differently between the two conditions. In Experiment 2, participants were not specifically instructed to use AVI, but retrospectively reported how often they engaged in AVI during the task. Highly hallucination-prone participants who retrospectively reported using imagery showed a lower response bias than did participants with lower proneness who also reported using AVI. Results are discussed in relation to prominent inner speech models of hallucinations.

Hearing voices in the resting brain: A review of intrinsic functional connectivity research on auditory verbal hallucinations.

Resting state networks (RSNs) are thought to reflect the intrinsic functional connectivity of brain regions. Alterations to RSNs have been proposed to underpin various kinds of psychopathology, including the occurrence of auditory verbal hallucinations (AVH). This review outlines the main hypotheses linking AVH and the resting state, and assesses the evidence for alterations to intrinsic connectivity provided by studies of resting fMRI in AVH. The influence of hallucinations during data acquisition, medication confounds, and movement are also considered. Despite a large variety of analytic methods and designs being deployed, it is possible to conclude that resting connectivity in the left temporal lobe in general and left superior temporal gyrus in particular are disrupted in AVH. There is also preliminary evidence of atypical connectivity in the default mode network and its interaction with other RSNs. Recommendations for future research include the adoption of a common analysis protocol to allow for more overlapping datasets and replication of intrinsic functional connectivity alterations.

The role of the superior temporal lobe in auditory false perceptions: a transcranial direct current stimulation study.

Neuroimaging has shown that a network of cortical areas, which includes the superior temporal gyrus, is active during auditory verbal hallucinations (AVHs). In the present study, healthy, non-hallucinating participants (N=30) completed an auditory signal detection task, in which participants were required to detect a voice in short bursts of white noise, with the variable of interest being the rate of false auditory verbal perceptions. This paradigm was coupled with transcranial direct current stimulation, a noninvasive brain stimulation technique, to test the involvement of the left posterior superior temporal gyrus in the creation of auditory false perceptions. The results showed that increasing the levels of excitability in this region led to a higher rate of 'false alarm' responses than when levels of excitability were decreased, with false alarm responses under a sham stimulation condition lying at a mid-point between anodal and cathodal stimulation conditions. There were also corresponding changes in signal detection parameters. These results are discussed in terms of prominent cognitive neuroscientific theories of AVHs, and potential future directions for research are outlined.

The impact of negative affect on reality discrimination.

BACKGROUND AND OBJECTIVES: People who experience auditory hallucinations tend to show weak reality discrimination skills, so that they misattribute internal, self-generated events to an external, non-self source. We examined whether inducing negative affect in healthy young adults would increase their tendency to make external misattributions on a reality discrimination task. METHODS: Participants (N = 54) received one of three mood inductions (one positive, two negative) and then performed an auditory signal detection task to assess reality discrimination. RESULTS: Participants who received either of the two negative inductions made more false alarms, but not more hits, than participants who received the neutral induction, indicating that negative affect makes participants more likely to misattribute internal, self-generated events to an external, non-self source. LIMITATIONS: These findings are drawn from an analogue sample, and research that examines whether negative affect also impairs reality discrimination in patients who experience auditory hallucinations is required. CONCLUSIONS: These findings show that negative affect disrupts reality discrimination and suggest one way in which negative affect may lead to hallucinatory experiences.

Auditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option.

Auditory verbal hallucinations (AVHs) are the experience of hearing voices in the absence of any speaker, often associated with a schizophrenia diagnosis. Prominent cognitive models of AVHs suggest they may be the result of inner speech being misattributed to an external or non-self source, due to atypical self- or reality monitoring. These arguments are supported by studies showing that people experiencing AVHs often show an externalising bias during monitoring tasks, and neuroimaging evidence which implicates superior temporal brain regions, both during AVHs and during tasks that measure verbal self-monitoring performance. Recently, efficacy of noninvasive neurostimulation techniques as a treatment option for AVHs has been tested. Meta-analyses show a moderate effect size in reduction of AVH frequency, but there has been little attempt to explain the therapeutic effect of neurostimulation in relation to existing cognitive models. This article reviews inner speech models of AVHs, and argues that a possible explanation for reduction in frequency following treatment may be modulation of activity in the brain regions involving the monitoring of inner speech.

Mind-mindedness and theory of mind: mediating roles of language and perspectival symbolic play.

Relations among indices of maternal mind-mindedness (appropriate and nonattuned mind-related comments) and children's: (a) internal state vocabulary and perspectival symbolic play at 26 months (N = 206), and (b) theory of mind (ToM) at 51 months (n = 161) were investigated. Appropriate comments were positively associated with ToM, but were unrelated to internal state language and perspectival symbolic play. Nonattuned comments were negatively correlated with internal state language and perspectival symbolic play, but were unrelated to ToM. Path analyses indicated that the best fit model assumed: (a) indirect links between nonattuned comments and ToM via children's perspectival symbolic play, (b) a direct link between appropriate comments and ToM, and (c) an indirect link between appropriate comments and ToM via children's concurrent receptive verbal ability.

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.