Arts-based methods for hallucination research.

INTRODUCTION: Neurocognitive models of hallucinations posit theories of misattribution and deficits in the monitoring of mental or perceptual phenomena but cannot yet account for the subjective experience of hallucinations across individuals and diagnostic categories. Arts-based research methods (ABRM) have potential for advancing research, as art depicts experiences which cognitive neuropsychiatry seeks to explain. METHODS: To examine how incorporating ABRM may advance hallucination research and theories, we explore data on the lived experiences of hallucinations in psychiatric and neurological populations. We present a multiple case study of two empirical ABRM studies, which used participant-generated artwork and artist collaborations alongside interviews. RESULTS: ABRM combined with interviews illustrated that hallucinations were infused with sensory features, characterised by embodiment, and situated within lived circumstances. These findings advance neurocognitive models of hallucinations by nuancing their multimodal nature, illustrating their embodied feelings, and exploring their content and themes. The process of generating artworks aided in disclosing difficult to discuss hallucinations, promoted participant self-reflection, and clarified multimodal details that may have been misconstrued through interview alone. ABRM were relevant and acceptable for participants and researchers. CONCLUSION: ABRM may contribute to the development of neurocognitive models of hallucinations by making hallucination experiences more visible, tangible, and accessible.

Evidence in cortical folding patterns for prenatal predispositions to hallucinations in schizophrenia.

All perception is a construction of the brain from sensory input. Our first perceptions begin during gestation, making fetal brain development fundamental to how we experience a diverse world. Hallucinations are percepts without origin in physical reality that occur in health and disease. Despite longstanding research on the brain structures supporting hallucinations and on perinatal contributions to the pathophysiology of schizophrenia, what links these two distinct lines of research remains unclear. Sulcal patterns derived from structural magnetic resonance (MR) images can provide a proxy in adulthood for early brain development. We studied two independent datasets of patients with schizophrenia who underwent clinical assessment and 3T MR imaging from the United Kingdom and Shanghai, China (n = 181 combined) and 63 healthy controls from Shanghai. Participants were stratified into those with (n = 79 UK; n = 22 Shanghai) and without (n = 43 UK; n = 37 Shanghai) hallucinations from the PANSS P3 scores for hallucinatory behaviour. We quantified the length, depth, and asymmetry indices of the paracingulate and superior temporal sulci (PCS, STS), which have previously been associated with hallucinations in schizophrenia, and constructed cortical folding covariance matrices organized by large-scale functional networks. In both ethnic groups, we demonstrated a significantly shorter left PCS in patients with hallucinations compared to those without, and to healthy controls. Reduced PCS length and STS depth corresponded to focal deviations in their geometry and to significantly increased covariance within and between areas of the salience and auditory networks. The discovery of neurodevelopmental alterations contributing to hallucinations establishes testable models for these enigmatic, sometimes highly distressing, perceptions and provides mechanistic insight into the pathological consequences of prenatal origins.

Paracingulate Sulcus Length Is Shorter in Voice-Hearers Regardless of Need for Care.

Hallucinations-while often considered an indication of mental illness-are commonly experienced by those without a need for clinical care. These nonclinical voice-hearers offer an opportunity to investigate hallucinations in the absence of confounds inherent to the clinical state. Recent work demonstrates an association between auditory verbal hallucinations (AVH) and structural variability in paracingulate sulcus (PCS) of medial prefrontal cortex in a clinical population. However, before PCS length may be considered a biomarker for clinical hallucination risk, it is necessary to investigate PCS structure in a nonclinical population of voice-hearers with AVH phenomenology similar to those of their clinical counterparts. In the current study, PCS length was measured from T1-weighted structural MRI scans of four groups of participants: (1) voice-hearers with a psychotic disorder (n = 15); (2) voice-hearers without a psychotic disorder (n = 15); (3) nonvoice-hearers with a psychotic disorder (n = 14); and (4) nonvoice-hearers without a psychotic disorder (n = 15). There was a main effect of AVH status-but not psychosis-on right PCS length, with no interaction of AVH and psychosis. Participants with AVH exhibited reduced right PCS length compared to participants without AVH (mean reduction = 8.8 mm, P < 0.05). While past studies have demonstrated decreased PCS length in clinical voice-hearers, ours is the first demonstration that shorter right PCS extends to nonclinical voice-hearers. Our findings support the hypothesis that differences in PCS length are related to the propensity to hear voices and not to illness, consistent with a continuum model of voice-hearing.

Meta-analytic Evidence for the Plurality of Mechanisms in Transdiagnostic Structural MRI Studies of Hallucination Status.

BACKGROUND: Hallucinations are transmodal and transdiagnostic phenomena, occurring across sensory modalities and presenting in psychiatric, neurodegenerative, neurological, and non-clinical populations. Despite their cross-category occurrence, little empirical work has directly compared between-group neural correlates of hallucinations. METHODS: We performed whole-brain voxelwise meta-analyses of hallucination status across diagnoses using anisotropic effect-size seed-based d mapping (AES-SDM), and conducted a comprehensive systematic review in PubMed and Web of Science until May 2018 on other structural correlates of hallucinations, including cortical thickness and gyrification. FINDINGS: 3214 abstracts were identified. Patients with psychiatric disorders and hallucinations (eight studies) exhibited reduced gray matter (GM) in the left insula, right inferior frontal gyrus, left anterior cingulate/paracingulate gyrus, left middle temporal gyrus, and increased in the bilateral fusiform gyrus, while patients with neurodegenerative disorders with hallucinations (eight studies) showed GM decreases in the left lingual gyrus, right supramarginal gyrus/parietal operculum, left parahippocampal gyrus, left fusiform gyrus, right thalamus, and right lateral occipital gyrus. Group differences between psychiatric and neurodegenerative hallucination meta-analyses were formally confirmed using Monte Carlo randomizations to determine statistical significance, and a jackknife sensitivity analysis established the reproducibility of results across nearly all study combinations. For other structural measures (28 studies), the most consistent findings associated with hallucination status were reduced cortical thickness in temporal gyri in schizophrenia and altered hippocampal volume in Parkinson's disease and dementia. Additionally, increased severity of hallucinations in schizophrenia correlated with GM reductions within the left superior temporal gyrus, right middle temporal gyrus, bilateral supramarginal and angular gyri. INTERPRETATION: Distinct patterns of neuroanatomical alteration characterize hallucination status in patients with psychiatric and neurodegenerative diseases, suggesting a plurality of anatomical signatures. This approach has implications for treatment, theoretical frameworks, and generates refutable predictions for hallucinations in other diseases and their occurrence within the general population. FUNDING: None.

Paracingulate Sulcus Morphology and Hallucinations in Clinical and Nonclinical Groups.

Hallucinations are a characteristic symptom of psychotic mental health conditions that are also experienced by many individuals without a clinical diagnosis. Hallucinations in schizophrenia have been linked to differences in the length of the paracingulate sulcus (PCS), a structure in the medial prefrontal cortex which has previously been associated with the ability to differentiate perceived and imagined information. We investigated whether this putative morphological basis for hallucinations extends to individuals without a clinical diagnosis, by examining whether nonclinical individuals with hallucinations have shorter PCS than nonclinical individuals without hallucinations. Structural MRI scans were examined from 3 demographically matched groups of individuals: 50 patients with psychotic diagnoses who experienced auditory verbal hallucinations (AVHs), 50 nonclinical individuals with AVHs, and 50 healthy control subjects with no life-time history of hallucinations. Results were verified using automated data-driven gyrification analyses. Patients with hallucinations had shorter PCS than both healthy controls and nonclinical individuals with hallucinations, with no difference between nonclinical individuals with hallucinations and healthy controls. These findings suggest that the association of shorter PCS length with hallucinations is specific to patients with a psychotic disorder. This presents challenges for full-continuum models of psychosis and suggests possible differences in the mechanisms underlying hallucinations in clinical and nonclinical groups.

Brain Mechanisms of Reality Monitoring.

Reality monitoring processes are necessary for discriminating between internally generated information and information that originated in the outside world. They help us to identify our thoughts, feelings, and imaginations, and to distinguish them from events we may have experienced or have been told about by someone else. Reality monitoring errors range from confusions between real and imagined experiences, that are byproducts of normal cognition, to symptoms of mental illness such as hallucinations. Recent advances support an emerging neurocognitive characterization of reality monitoring that provides insights into its underlying operating principles and neural mechanisms, the differing ways in which impairment may occur in health and disease, and the potential for rehabilitation strategies to be devised that might help those who experience clinically significant reality monitoring disruption.

Reality monitoring impairment in schizophrenia reflects specific prefrontal cortex dysfunction.

Reality monitoring impairment is often reported in schizophrenia but the neural basis of this deficit is poorly understood. Difficulties with reality monitoring could be attributable to the same pattern of neural dysfunction as other cognitive deficits that characterize schizophrenia, or might instead represent a separable and dissociable impairment. This question was addressed through direct comparison of behavioral performance and neural activity associated with reality monitoring and working memory in patients with schizophrenia and matched healthy controls. Participants performed a word-pair reality monitoring task and a Sternberg working memory task while undergoing fMRI scanning. Distinct behavioral deficits were observed in the patients during performance of each task, which were associated with separable task- and region-specific dysfunction in the medial anterior prefrontal cortex for reality monitoring and dorsolateral prefrontal cortex for working memory. The results suggest that reality monitoring impairment is a distinct neurocognitive deficit in schizophrenia. The findings are consistent with the presence of a range of dissociable cognitive deficits in schizophrenia which may be associated with variable functional and structural dysconnectivity in underlying processing networks.

Testing continuum models of psychosis: No reduction in source monitoring ability in healthy individuals prone to auditory hallucinations.

People with schizophrenia who hallucinate show impairments in reality monitoring (the ability to distinguish internally generated information from information obtained from external sources) compared to non-hallucinating patients and healthy individuals. While this may be explained at least in part by an increased externalizing bias, it remains unclear whether this impairment is specific to reality monitoring, or whether it also reflects a general deficit in the monitoring of self-generated information (internal source monitoring). Much interest has focused recently on continuum models of psychosis which argue that hallucination-proneness is distributed in clinical and non-clinical groups, but few studies have directly investigated reality monitoring and internal source monitoring abilities in healthy individuals with a proneness to hallucinations. Two experiments are presented here: the first (N = 47, with participants selected for hallucination-proneness from a larger sample of 677 adults) found no evidence of an impairment or externalizing bias on a reality monitoring task in hallucination-prone individuals; the second (N = 124) found no evidence of atypical performance on an internal source monitoring task in hallucination-prone individuals. The significance of these findings is reviewed in light of the clinical evidence and the implications for models of hallucination generation discussed.

Monitoring what is real: The effects of modality and action on accuracy and type of reality monitoring error.

Reality monitoring refers to processes involved in distinguishing internally generated information from information presented in the external world, an activity thought to be based, in part, on assessment of activated features such as the amount and type of cognitive operations and perceptual content. Impairment in reality monitoring has been implicated in symptoms of mental illness and associated more widely with the occurrence of anomalous perceptions as well as false memories and beliefs. In the present experiment, the cognitive mechanisms of reality monitoring were probed in healthy individuals using a task that investigated the effects of stimulus modality (auditory vs visual) and the type of action undertaken during encoding (thought vs speech) on subsequent source memory. There was reduced source accuracy for auditory stimuli compared with visual, and when encoding was accompanied by thought as opposed to speech, and a greater rate of externalization than internalization errors that was stable across factors. Interpreted within the source monitoring framework (Johnson, Hashtroudi, & Lindsay, 1993), the results are consistent with the greater prevalence of clinically observed auditory than visual reality discrimination failures. The significance of these findings is discussed in light of theories of hallucinations, delusions and confabulation.

The neural mechanisms of hallucinations: A quantitative meta-analysis of neuroimaging studies.

Activation likelihood estimation meta-analysis of functional neuroimaging data was used to investigate the neural mechanisms underlying auditory-verbal and visual hallucinations (AVHs and VHs). Consistent activation across studies during AVHs, but not VHs, in Wernicke's and Broca's areas is consistent with involvement of speech and language processes in the experience of hearing voices when none are present. Similarly, greater activity in auditory cortex during AVHs and in visual cortex during VHs supports models proposing over-stimulation of sensory cortices in the generation of these perceptual anomalies. Activation across studies in the medial temporal lobe highlights a role for memory intrusions in the provision of content for AVHs, whereas insula activation may relate to the involvement of awareness and self-representation. Finally, activation in the paracingulate region of medial prefrontal cortex during AVHs is consistent with models implicating reality monitoring impairment in the misattribution of self-generated information as externally perceived. In the light of the results, the need for unified theoretical frameworks that account for the full range of hallucinatory experiences is discussed.

Paracingulate sulcus morphology is associated with hallucinations in the human brain.

Hallucinations are common in psychiatric disorders, and are also experienced by many individuals who are not mentally ill. Here, in 153 participants, we investigate brain structural markers that predict the occurrence of hallucinations by comparing patients with schizophrenia who have experienced hallucinations against patients who have not, matched on a number of demographic and clinical variables. Using both newly validated visual classification techniques and automated, data-driven methods, hallucinations were associated with specific brain morphology differences in the paracingulate sulcus, a fold in the medial prefrontal cortex, with a 1 cm reduction in sulcal length increasing the likelihood of hallucinations by 19.9%, regardless of the sensory modality in which they were experienced. The findings suggest a specific morphological basis for a pervasive feature of typical and atypical human experience.