Reconciling competing mechanisms posited to underlie auditory verbal hallucinations

Perception is not the passive registration of incoming sensory data. Rather, it involves some analysis by synthesis, based on past experiences and context. One adaptive consequence of this arrangement is imagination—the ability to richly simulate sensory experiences, interrogate and manipulate those simulations, in service of action and decision making. In this paper, we will discuss one possible cost of this adaptation, namely hallucinations—perceptions without sensory stimulation, which characterize serious mental illnesses like schizophrenia, but which also occur in neurological illnesses, and—crucially for the present piece—are common also in the non-treatment-seeking population. We will draw upon a framework for imagination that distinguishes voluntary from non-voluntary experiences and explore the extent to which the varieties and features of hallucinations map onto this distinction, with a focus on auditory-verbal hallucinations (AVHs)—colloquially, hearing voices. We will propose that sense of agency for the act of imagining is key to meaningfully dissecting different forms and features of AVHs, and we will outline the neural, cognitive and phenomenological sequelae of this sense. We will conclude that a compelling unifying framework for action, perception and belief—predictive processing—can incorporate observations regarding sense of agency, imagination and hallucination.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Imagine that: elevated sensory strength of mental imagery in individuals with Parkinson's disease and visual hallucinations

Visual hallucinations occur when our conscious experience does not accurately reflect external reality. However, these dissociations also regularly occur when we imagine the world around us in the absence of visual stimulation. We used two novel behavioural paradigms to objectively measure visual hallucinations and voluntary mental imagery in 19 individuals with Parkinson''s disease (ten with visual hallucinations; nine without) and ten healthy, age-matched controls. We then used this behavioural overlap to interrogate the connectivity both within and between the major attentional control networks using resting-state functional magnetic resonance imaging. Patients with visual hallucinations had elevated mental imagery strength compared with patients without hallucinations and controls. Specifically, the sensory strength of imagery predicted the frequency of visual hallucinations. Together, hallucinations and mental imagery predicted multiple abnormalities in functional connectivity both within and between the attentional control networks, as measured with resting-state functional magnetic resonance imaging. However, the two phenomena were also dissociable at the neural level, with both mental imagery and visual misperceptions associated with specific abnormalities in attentional network connectivity. Our results provide the first evidence of both the shared and unique neural correlates of these two similar, yet distinct phenomena.     

Attention driven phantom vision: measuring the sensory strength of attentional templates and their relation to visual mental imagery and aphantasia

When we search for an object in an array or anticipate attending to a future object, we create an ‘attentional template'' of the object. The definitions of attentional templates and visual imagery share many similarities as well as many of the same neural characteristics. However, the phenomenology of these attentional templates and their neural similarities to visual imagery and perception are rarely, if ever discussed. Here, we investigate the relationship between these two forms of non-retinal phantom vision through the use of the binocular rivalry technique, which allows us to measure the sensory strength of attentional templates in the absence of concurrent perceptual stimuli. We find that attentional templates correlate with both feature-based attention and visual imagery. Attentional templates, like imagery, were significantly disrupted by the presence of irrelevant visual stimuli, while feature-based attention was not. We also found that a special population who lack the ability to visualize (aphantasia), showed evidence of feature-based attention when measured using the binocular rivalry paradigm, but not attentional templates. Taken together, these data suggest functional similarities between attentional templates and visual imagery, advancing the theory of visual imagery as a general simulation tool used across cognition.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Hallucinations on demand: the utility of experimentally induced phenomena in hallucination research

Despite the desire to delve deeper into hallucinations of all types, methodological obstacles have frustrated development of more rigorous quantitative experimental techniques, thereby hampering research progress. Here, we discuss these obstacles and, with reference to visual phenomena, argue that experimentally induced phenomena (e.g. hallucinations induced by flickering light and classical conditioning) can bring hallucinations within reach of more objective behavioural and neural measurement. Expanding the scope of hallucination research raises questions about which phenomena qualify as hallucinations, and how to identify phenomena suitable for use as laboratory models of hallucination. Due to the ambiguity inherent in current hallucination definitions, we suggest that the utility of phenomena for use as laboratory hallucination models should be represented on a continuous spectrum, where suitability varies with the degree to which external sensory information constrains conscious experience. We suggest that existing strategies that group pathological hallucinations into meaningful subtypes based on hallucination characteristics (including phenomenology, disorder and neural activity) can guide extrapolation from hallucination models to other hallucinatory phenomena. Using a spectrum of phenomena to guide scientific hallucination research should help unite the historically separate fields of psychophysics, cognitive neuroscience and clinical research to better understand and treat hallucinations, and inform models of consciousness.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Fluctuating Minds: Spontaneous Psychophysical Variability during Mind-Wandering

Mind-wandering is the occasional distraction we experience while performing a cognitive task. It arises without any external precedent, varies over time, and interferes with the processing of sensory information. Here, we asked whether the transition from the on-task state to mind-wandering is a gradual process or an abrupt event. We developed a new experimental approach, based on the continuous, online assessment of individual psychophysical performance. Probe questions were asked whenever response times (RTs) exceeded 2 standard deviations from the participant’s average RT. Results showed that mind-wandering reports were generally preceded by slower RTs, as compared to trials preceding on-task reports. Mind-wandering episodes could be reliably predicted from the response time difference between the last and the second-to-last trials. Thus, mind-wandering reports follow an abrupt increase in behavioral variability, lasting between 2.5 and 10 seconds.     

How deep is the rift between conscious states in sleep and wakefulness? Spontaneous experience over the sleep–wake cycle

Whether we are awake or asleep is believed to mark a sharp divide between the types of conscious states we undergo in either behavioural state. Consciousness in sleep is often equated with dreaming and thought to be characteristically different from waking consciousness. Conversely, recent research shows that we spend a substantial amount of our waking lives mind wandering, or lost in spontaneous thoughts. Dreaming has been described as intensified mind wandering, suggesting that there is a continuum of spontaneous experience that reaches from waking into sleep. This challenges how we conceive of the behavioural states of sleep and wakefulness in relation to conscious states. I propose a conceptual framework that distinguishes different subtypes of spontaneous thoughts and experiences independently of their occurrence in sleep or waking. I apply this framework to selected findings from dream and mind-wandering research. I argue that to assess the relationship between spontaneous thoughts and experiences and the behavioural states of sleep and wakefulness, we need to look beyond dreams to consider kinds of sleep-related experience that qualify as dreamless. I conclude that if we consider the entire range of spontaneous thoughts and experiences, there appears to be variation in subtypes both within as well as across behavioural states. Whether we are sleeping or waking does not appear to strongly constrain which subtypes of spontaneous thoughts and experiences we undergo in those states. This challenges the conventional and coarse-grained distinction between sleep and waking and their putative relation to conscious states.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Offline perception: an introduction

Experiences that are self-generated and independent of sensory stimulations permeate our whole life. This theme issue examines their similarities and differences, systematizes the literature from an integrative perspective, critically discusses state-of-the-art empirical findings and proposes new theoretical approaches. The aim of the theme issue is to foster interaction between the different disciplines and research directions involved and to explore the prospects of a unificatory account of offline perception in general.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

The Hallucinations of Widowhood

227 widows and 66 widowers were interviewed to determine the extent to which they had hallucinatory experiences of their dead spouse. The people interviewed formed 80·7% of all widowed people resident within a defined area, in mid-Wales, and 94·2% of those suitable, through the absence of incapacitating illness, for interview.Almost half the people interviewed had hallucinations or illusions of the dead spouse. The proportion of men and women who had these experiences was similar. The hallucinations often lasted many years but were most common during the first 10 years of widowhood. Social isolation did not affect the incidence of hallucination, nor was it related to the incidence of known depressive illness. There was no variation within cultural groups and there was no variation with place of residence, whether this was within town, country, or village, or within England and Wales.Young people were less likely to be hallucinated than those widowed after the age of 40. The incidence of hallucination increased with length of marriage and was particularly associated with a happy marriage and parenthood. Members of the “professional and managerial” group were particularly likely to be hallucinated, while widows of “non-manual and sales workers” were the ones least likely to be hallucinated. The incidence was greater with hysteroid than obsessoid people. It was unusual for the hallucinations to have been disclosed, even to close friends or relatives.These hallucinations are considered to be normal and helpful accompaniments of widowhood.     

End-of-life decision-making in Canada: the report by the Royal Society of Canada expert panel on end-of-life decision-making

This report on end-of-life decision-making in Canada was produced by an international expert panel and commissioned by the Royal Society of Canada. It consists of five chapters. Chapter 1 reviews what is known about end-of-life care and opinions about assisted dying in Canada. Chapter 2 reviews the legal status quo in Canada with regard to various forms of assisted death. Chapter 3 reviews ethical issues pertaining to assisted death. The analysis is grounded in core values central to Canada's constitutional order. Chapter 4 reviews the experiences had in a number of jurisdictions that have decriminalized or recently reviewed assisted dying in some shape or form. Chapter 5 provides recommendations with regard to the provision of palliative care in Canada, as well as recommendations for reform with respect to the various forms of assisted death covered in this document.     

Development of a Data Management Tool for Investigating Multivariate Space and Free Will Experiences in Virtual Reality

Virtual reality (VR) has become mature enough to be successfully used in clinical applications such as exposure therapy, pain distraction, and neuropsychological assessment. However, we now need to go beyond the outcome data from this research and conduct the detailed scientific investigations required to better understand what factors influence why VR works (or doesn’t) in these types of clinical applications. This knowledge is required to guide the development of VR applications in the key areas of education, training, and rehabilitation and to further evolve existing VR approaches. One of the primary assets obtained with the use of VR is the ability to simulate the complexity of real world environments, within which human performance can be tested and trained. But this asset comes with a price in terms of the capture, quantification and analysis of large, multivariate and concurrent data sources that reflect the naturalistic behavioral interaction that is afforded in a virtual world. As well, while achieving realism has been a main goal in making convincing VR environments, just what constitutes realism and how much is needed is still an open question situated firmly in the research domain. Just as in real “reality,” such factors in virtual reality are complex and multivariate, and the understanding of this complexity presents exceptional challenges to the VR researcher. For certain research questions, good behavioral science often requires consistent delivery of stimuli within tightly controlled lab-based experimental conditions. However, for other important research questions we do not want to constrain naturalistic behavior and limit VR’s ability to replicate real world conditions, simply because it is easier to study human performance with traditional lab-based methodologies. By doing so we may compromise the very qualities that comprise VR’s unique capacity to mimic the experiences and challenges that exist in everyday life. What is really needed to address scientific questions that require natural exploration of a simulated environment are more usable and robust tools to instrument, organize, and visualize the complex data generated by measurements of participant behaviors within a virtual world. This paper briefly describes the rationale and methodology of an initial study in an ongoing research program that aims to investigate human performance within a virtual environment where unconstrained “free will” exploratory behavior is essential to research questions that involve the relationships between physiology, emotion, and memory. After a discussion of the research protocol and the types of data that were collected, we describe a novel tool that was borne from our need to more efficiently capture, manage, and explore the complex data that was generated in this research. An example of a research participant’s annotated display from this data management and visualization tool is then presented. It is our view that this tool provides the capacity to better visualize and understand the complex data relationships that may arise in VR research that investigates naturalistic free will behavior and its impact on other human performance variables.     

Subclinical Elevation of Plasma C-Reactive Protein and Illusions/Hallucinations in Subjects with Parkinson’s Disease: Case–control Study

Background

Though infections are associated with psychotic symptoms, whether or not subclinical inflammation is associated with hallucinations is not known in Parkinson’s disease (PD).

Purpose

To investigate the association of illusions/hallucinations and plasma CRP levels in PD patients without symptomatic infections.

Methods

PD patients not diagnosed as having infections were assessed for illusions and hallucinations using the Parkinson Psychosis Questionnaire (PPQ). It comprises four-domain questions: PPQ-A for sleep problems, PPQ-B for hallucinations/illusions, PPQ-C for delusions, and PPQ-D for disorientation. Assigning patients with ≥1 points in the PPQ-B score to be cases and others as controls, the association of hallucinations/illusions and clinical features (age, sex, duration of PD, Unified Parkinson’s Disease Rating Scale part 3 (UPDRS-3), Mini-Mental State Examination (MMSE) score, sleep disturbance (PPQ-A score) as well as daily doses of L-Dopa, dopamine agonists, amantadine, and selegiline) were analyzed using a case–control design.

Results

A total of 111 patients were examined and plasma CRP levels were <0.1–6.0 mg/L. Hallucinations or illusions were detected in 28 (25.2%). There were significant differences in age, UPDRS-3 score, MMSE score, PPQ-A, daily doses of L-Dopa and dopamine agonists and plasma CRP levels between cases and controls. A multivariate logistic regression model revealed that UPDRS-3 scores and plasma CRP levels were significantly associated with hallucinations/illusions with an adjusted odds ratio of 1.96 (95% confidence interval (CI) 1.20–3.20) per 10 points and 1.57 (95% confidence interval 1.13–2.16) per two-fold, respectively. Dividing patients into thirds by CRP levels (≤0.2, 0.3–0.6, ≥0.7 mg/L), the prevalence of hallucinations/illusions was 13.2%, 21.6%, and 41.7%, in the bottom-, middle-, and top-thirds, respectively (for trend p = 0.012).

Conclusions

Subclinical elevation of plasma CRP levels was associated with hallucinations or illusions after adjustment for motor disability, suggesting that subclinical elevations of CRP levels might be an independent risk for hallucinations/illusions.     

The sensory ecology of adaptive landscapes

In complex environments, behavioural plasticity depends on the ability of an animal to integrate numerous sensory stimuli. The multidimensionality of factors interacting to shape plastic behaviour means it is difficult for both organisms and researchers to predict what constitutes an adaptive response to a given set of conditions. Although researchers may be able to map the fitness pay-offs of different behavioural strategies in changing environments, there is no guarantee that the study species will be able to perceive these pay-offs. We thus risk a disconnect between our own predictions about adaptive behaviour and what is behaviourally achievable given the umwelt of the animal being studied. This may lead to erroneous conclusions about maladaptive behaviour in circumstances when the behaviour exhibited is the most adaptive possible given sensory limitations. With advances in the computational resources available to behavioural ecologists, we can now measure vast numbers of interactions among behaviours and environments to create adaptive behavioural surfaces. These surfaces have massive heuristic, predictive and analytical potential in understanding adaptive animal behaviour, but researchers using them are destined to fail if they ignore the sensory ecology of the species they study. Here, we advocate the continued use of these approaches while directly linking them to perceptual space to ensure that the topology of the generated adaptive landscape matches the perceptual reality of the animal it intends to study. Doing so will allow predictive models of animal behaviour to reflect the reality faced by the agents on adaptive surfaces, vastly improving our ability to determine what constitutes an adaptive response for the animal in question.     

Unconscious mental imagery

Historically, mental imagery has been defined as an experiential state—as something necessarily conscious. But most behavioural or neuroimaging experiments on mental imagery—including the most famous ones—do not actually take the conscious experience of the subject into consideration. Further, recent research highlights that there are very few behavioural or neural differences between conscious and unconscious mental imagery. I argue that treating mental imagery as not necessarily conscious (as potentially unconscious) would bring much needed explanatory unification to mental imagery research. It would also help us to reassess some of the recent aphantasia findings inasmuch as at least some subjects with aphantasia would be best described as having unconscious mental imagery.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.     

Pupil Dilation Dynamics Track Attention to High-Level Information

It has long been thought that the eyes index the inner workings of the mind. Consistent with this intuition, empirical research has demonstrated that pupils dilate as a consequence of attentional effort. Recently, Smallwood et al. (2011) demonstrated that pupil dilations not only provide an index of overall attentional effort, but are time-locked to stimulus changes during attention (but not during mind-wandering). This finding suggests that pupil dilations afford a dynamic readout of conscious information processing. However, because stimulus onsets in their study involved shifts in luminance as well as information, they could not determine whether this coupling of stimulus and pupillary dynamics reflected attention to low-level (luminance) or high-level (information) changes. Here, we replicated the methodology and findings of Smallwood et al. (2011) while controlling for luminance changes. When presented with isoluminant digit sequences, participants'' pupillary dilations were synchronized with stimulus onsets when attending, but not when mind-wandering. This replicates Smallwood et al. (2011) and clarifies their finding by demonstrating that stimulus-pupil coupling reflects online cognitive processing beyond sensory gain.     

Sleep Paralysis and the Structure of Waking-Nightmare Hallucinations

Sleep paralysis (SP) entails a period of paralysis upon waking or falling asleep and is often accompanied by terrifying hallucinations. These hallucinations constitute a waking nightmare (w-nightmare) REM experience and are the original referents of the term nightmare. W-nightmare hallucinations are described by a three-factor structure involving experiences consistent with 1) threatening intruders, 2) physical assaults, and 3) vestibular-motor (V-M) bodily sensations. The present study assesses the reliability of this structure and some of the underlying measurement assumptions using several large samples of w-nightmare experients. Causal modeling further elucidated the potential causal relations among the three types of hallucinations. The first two factors appear to be strongly thematically and sequentially linked by an underlying theme of threat and assault. The third factor is relatively autonomous but appears to be sometimes recruited into the threat and assault themes. A theoretical model is proposed that combines REM mechanisms, a threat activated vigilance system (TAVS), and a bodily-self neuromatrix (BSN), as generators and organizers of w-nightmare hallucinatory experiences. More generally, it is argued that these mechanisms underwrite two fundamental domains of conscious experience: the experience of an agent-inhabited world and that of a spatial-kinetic bodily self.     

Successful Community Midwives in Pakistan: An Asset-Based Approach

In response to the low levels of skilled birth attendance in rural Pakistan, the government introduced a new cadre of community midwives (CMWs) in 2006. Assessments to-date have found that these CMWs have yet to emerge as significant providers for a number of sociocultural, geographic and financial reasons. However, a small number of CMWs have managed to establish functional practices in the private sector in conservative, infrastructure-challenged rural contexts. With an objective to highlight “what are the successful CMWs doing right given their context?” this paper adopts an asset-based approach to explore the experiences of the Pakistani CMWs who have managed to overcome the barriers and practice. We drew upon ethnographic data that was collected as part of a larger mixed methods study conducted in 2011–2012 in districts Jhelum and Layyah, Pakistan. Thirty eight CMWs, 45 other health care providers, 20 policymakers, 78 women, 35 husbands and 23 older women were interviewed. CMW clinics and practices were observed. Our data showed that only eight 8 out of 38 CMWs sampled were active providers. Poverty as a push factor to work and intrinsic individual-level characteristics that enabled the CMWs to respond successfully to the demands of the midwifery profession in the private sector emerged as the two key themes. Household poverty pushed the CMWs to work in this perceived low-status occupation. Their families supported them since they became the breadwinners. The successful CMWs also had an intrinsic sense of what was required to establish a private practice; they exhibited professionalism, had strong business sense and provided respectful maternity care. The study provides insight into how the program might improve its functioning by adapting its recruitment criteria to ensure selection of right candidates.     

Sensory Perception: Lessons from Synesthesia: Using Synesthesia to Inform the Understanding of Sensory Perception

Synesthesia, the conscious, idiosyncratic, repeatable, and involuntary sensation of one sensory modality in response to another, is a condition that has puzzled both researchers and philosophers for centuries. Much time has been spent proving the condition’s existence as well as investigating its etiology, but what can be learned from synesthesia remains a poorly discussed topic. Here, synaesthesia is presented as a possible answer rather than a question to the current gaps in our understanding of sensory perception. By first appreciating the similarities between normal sensory perception and synesthesia, one can use what is known about synaesthesia, from behavioral and imaging studies, to inform our understanding of “normal” sensory perception. In particular, in considering synesthesia, one can better understand how and where the different sensory modalities interact in the brain, how different sensory modalities can interact without confusion ― the binding problem ― as well as how sensory perception develops.     

John Woolman's Light in the Night: An Analysis

This is an analysis of a religious experience in the night recorded in the journal of John Woolman, a colonial Quaker. As a basis for analysis, I try to clarify the data of Woolman's experience without presuppositions about causes, states of consciousness, three-dimensional space, or meaning. I then study the phenomena in the light of what we know about perception, dreaming, hallucinatory geometric forms, light, and other people's comparable experiences. Because different modalities of his experience appear to be in different states at the same time, I examine each part of his experience separately. There is discussion of the relationship of dreams to visions and hallucinations, the concept of discrete states of consciousness, and the distinction between simulation and authentic experience while dreaming. The article is both an analysis of a religious experience recorded in 1757 and a discussion of methods of analysis.     

Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network

Sensory deprivation has long been known to cause hallucinations or “phantom” sensations, the most common of which is tinnitus induced by hearing loss, affecting 10–20% of the population. An observable hearing loss, causing auditory sensory deprivation over a band of frequencies, is present in over 90% of people with tinnitus. Existing plasticity-based computational models for tinnitus are usually driven by homeostatic mechanisms, modeled to fit phenomenological findings. Here, we use an objective-driven learning algorithm to model an early auditory processing neuronal network, e.g., in the dorsal cochlear nucleus. The learning algorithm maximizes the network’s output entropy by learning the feed-forward and recurrent interactions in the model. We show that the connectivity patterns and responses learned by the model display several hallmarks of early auditory neuronal networks. We further demonstrate that attenuation of peripheral inputs drives the recurrent network towards its critical point and transition into a tinnitus-like state. In this state, the network activity resembles responses to genuine inputs even in the absence of external stimulation, namely, it “hallucinates” auditory responses. These findings demonstrate how objective-driven plasticity mechanisms that normally act to optimize the network’s input representation can also elicit pathologies such as tinnitus as a result of sensory deprivation.     

Hallucination,imagery, dreaming: reassembling stimulus-independent perceptions based on Edmund Parish's classic misperception framework

Within the broad field of human perception lies the category of stimulus-independent perceptions, which draws together experiences such as hallucinations, mental imagery and dreams. Traditional divisions between medical and psychological sciences have contributed to these experiences being investigated separately. This review aims to examine their similarities and differences at the levels of phenomenology and underlying brain function and thus reassemble them within a common framework. Using Edmund Parish''s historical work as a guiding tool and the latest research findings in the cognitive, clinical and computational sciences, we consider how different perspectives may be reconciled and help generate novel hypotheses for future research.This article is part of the theme issue ‘Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation’.