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

Colleen P E Rollins, Jane R Garrison, Jon S Simons, James B Rowe, Claire O'Callaghan, Graham K Murray, John Suckling, Colleen P E Rollins, Jane R Garrison, Jon S Simons, James B Rowe, Claire O'Callaghan, Graham K Murray, John Suckling

Abstract

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.

Keywords: Hallucination; Meta-analysis; Neurodegenerative; Psychiatric; Structural MRI; Systematic review; Transdiagnostic.

Conflict of interest statement

Ms. Rollins reports a scholarship from Gates Cambridge during the conduct of the study. Professor Rowe reports grants from Wellcome Trust during the conduct of the study, grants from NIHR, McDonnell Foundation, PSP Association, Parkinsons UK, Medical Research Council, Evelyn Trust, and AZ-Medimmune, personal fees from Asceneuron, and other from Guarantors of Brain outside the submitted work. Professor Suckling, Dr. Murray, Dr. Garrison, Dr. Simons, and Dr. O'Callaghan have nothing to disclose.

Figures

Fig. 1
Fig. 1
Landscape of theoretical models of hallucinations. The major cognitive, psychological, and neurobiological theories for auditory and visual hallucinations are depicted. Separate theories have been proposed to underlie auditory versus visual hallucinations, although they share many common themes. Different theories within each modality category are not mutually exclusive and may overlap in their predictions. Dotted lines delineate proposals of divisions between, extensions to, or limitations of current theories. Key references: Inner speech model ; Intrusive memory hypothesis ; Resting state hypothesis ; Abnormal salience monitoring hypothesis ; Expectation-perception model ; Reality monitoring deficit theory, Dream imagery intrusion theory, Activation input modulation theory , ; Disinhibition hypothesis ; Perception and attention deficit model ; Top-down bottom-up models , ; Excitatory-inhibitory imbalance ; Predictive processing accounts , ; proposal of divide between self-monitoring accounts and spontaneous activity accounts for auditory verbal hallucinations (AVH) ; proposal of subtypes for AVH ; proposal for differential contribution of pharmacological subsystems to different types of AVH ; commentary on need to address interaction between and hierarchy of different modalities of hallucinations .
Fig. 2
Fig. 2
PRISMA flowchart for identification and selection of studies. Some studies performed analyses of multiple structural features and are therefore represented more than once. Abbreviations: H: population with hallucinations; NH: population without hallucination; VBM: voxel-based morphometry.
Fig. 3
Fig. 3
Meta-analysis results for individuals with hallucinations compared to those without hallucinations in psychiatric (A) and in neurodegenerative disorders (B). A. For psychiatric disorders, the meta-analysis revealed gray matter decreases in the left insula, right inferior frontal gyrus (pars triangularis)/frontal pole, left anterior cingulate gyrus/paracingulate gyrus, left middle temporal gyrus, and gray matter increases in the bilateral fusiform gyrus in patients with hallucinations relative to those without. B. For neurodegenerative disorders, the meta-analysis revealed decreases in the left lingual gyrus/intracalcarine cortex, left fusiform gyrus, right supramarginal gyrus, left parahippocampal gyrus, right thalamus, and right lateral occipital cortex. C. Formal comparison between meta-analyses revealed reduced GM in the left insula and left anterior cingulate/paracingulate gyrus for individuals with psychiatric relative to neurodegenerative hallucinations, and greater GM in the right lingual gyrus, IFG, and supramarginal gyrus, left thalamus, fusiform gyrus, inferior occipital gyrus, parahippocamapal and hippocampal gyri, and bilateral SFG. Abbreviations: STG: superior temporal gyrus; MTG: middle temporal gyrus; IFG: inferior frontal gyrus; PHG: parahippocampal gyrus; ICC: intracalcarine cortex; SFG: superior frontal gyrus.

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Source: PubMed

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