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Meta-analytic evidence for the plurality of mechanisms in transdiagnostic structural MRI studies of hallucination status

View ORCID ProfileColleen Rollins, Jane R Garrison, Jon S Simons, James B Rowe, Claire O’Callaghan, Graham Murray, John Suckling
doi: https://doi.org/10.1101/413609
Colleen Rollins
1Department of Psychiatry, University of Cambridge, Cambridge, UK (Colleen Rollins BSc, Jane R Garrison PhD, Claire O’Callaghan PhD, Graham Murray MD, Professor John Suckling PhD)
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  • ORCID record for Colleen Rollins
  • For correspondence: cper2@cam.ac.uk
Jane R Garrison
1Department of Psychiatry, University of Cambridge, Cambridge, UK (Colleen Rollins BSc, Jane R Garrison PhD, Claire O’Callaghan PhD, Graham Murray MD, Professor John Suckling PhD)
2Department of Psychology and Behavioural & Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK (Jane R Garrison PhD, Jon S Simons PhD)
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Jon S Simons
2Department of Psychology and Behavioural & Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK (Jane R Garrison PhD, Jon S Simons PhD)
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James B Rowe
3Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK (Professor James B Rowe MD)
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Claire O’Callaghan
1Department of Psychiatry, University of Cambridge, Cambridge, UK (Colleen Rollins BSc, Jane R Garrison PhD, Claire O’Callaghan PhD, Graham Murray MD, Professor John Suckling PhD)
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Graham Murray
1Department of Psychiatry, University of Cambridge, Cambridge, UK (Colleen Rollins BSc, Jane R Garrison PhD, Claire O’Callaghan PhD, Graham Murray MD, Professor John Suckling PhD)
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John Suckling
1Department of Psychiatry, University of Cambridge, Cambridge, UK (Colleen Rollins BSc, Jane R Garrison PhD, Claire O’Callaghan PhD, Graham Murray MD, Professor John Suckling PhD)
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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 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 meta-analyses were formally confirmed and a jackknife sensitivity analysis established the reproducibility of results across nearly all study combinations. For other 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.

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.

Evidence before this study There is increasing recognition that hallucinations occur beyond the archetype of schizophrenia, presenting in other psychiatric disorders, neurological and neurodegenerative conditions, and among the general population. Not only are hallucinations a transdiagnostic phenomenon, but also the experience of hallucinating is phenomenologically diverse, varying in modality, content, frequency, and affect. It has been suggested that no one type of hallucination is pathognomic to any one disorder, but rather that hallucinations may exist on a continuum. However, limited research has been done to directly compare the underlying neuroanatomy of hallucinations between different disorders. With this aim, we conducted a meta-analysis and systematic review of structural MRI studies comparing individuals who experience hallucinations with those who do not, to investigate the brain morphology related to the transdiagnostic presentation of hallucinations. We searched PubMed and Web of Science with no start date limit, up to May 2018 using the keyword combination (hallucinat*) AND (MRI OR magnetic resonance imaging OR morphology OR voxel?based OR morphometr* OR neural correlate OR structur*). We included only studies with a within-group no-hallucination control to tease out structural changes specific to hallucinations from effects of the broader pathology. Neuroimaging meta-analyses were conducted on studies performing whole-brain voxelwise gray matter differences, while studies assessing other structural correlates were qualitatively synthesized.

Added value of this study This is the first meta-analysis to illustrate the brain structural correlates of hallucination occurrence derived from T1-weighted MRI, and to do so in a comparative manner across clinical groups. We identified two distinct gray matter substrates for hallucination presence in psychiatric compared to neurodegenerative diseases, which we hypothesise constitute at least two distinct mechanisms. In addition, we qualitatively assessed other structural neuroimaging studies over a variety of morphometric indices. We therefore provide a complete characterization of current knowledge of the brain morphology associated with hallucinations across clinical status and modality.

Implications of all the available evidence Our findings show at least two structural substrates that link to the hallucinatory experience. This informs theoretical work on hallucinations which have to date been limited in generating unifying direction-specific predictions of brain structure and function. Understanding the plurality of anatomical signatures of hallucinations may also inform treatment strategies. We predict that other disorders in which patients experience hallucinations can be categorised by our approach based on the broader phenotype; for example, hallucinations in personality disorder may be of the psychiatric type, and similarly for early onset hallucinations in the general population, whilst later onset will be neurodegenerative. Moreover, by differentiating the mechanisms of hallucinations we recommend the contextualising of research by the appropriate phenotype.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 11, 2018.
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Meta-analytic evidence for the plurality of mechanisms in transdiagnostic structural MRI studies of hallucination status
Colleen Rollins, Jane R Garrison, Jon S Simons, James B Rowe, Claire O’Callaghan, Graham Murray, John Suckling
bioRxiv 413609; doi: https://doi.org/10.1101/413609
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Meta-analytic evidence for the plurality of mechanisms in transdiagnostic structural MRI studies of hallucination status
Colleen Rollins, Jane R Garrison, Jon S Simons, James B Rowe, Claire O’Callaghan, Graham Murray, John Suckling
bioRxiv 413609; doi: https://doi.org/10.1101/413609

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