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The multimodal connectivity of the hippocampal complex in auditory and visual hallucinations

Molecular Psychiatry volume 19, pages 184–191 (2014)Cite this article

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Abstract

Hallucinations constitute one of the most representative and disabling symptoms of schizophrenia. Several Magnetic Resonance Imaging (MRI) findings support the hypothesis that distinct patterns of connectivity, particularly within networks involving the hippocampal complex (HC), could be associated with different hallucinatory modalities. The aim of this study was to investigate HC connectivity as a function of the hallucinatory modality, that is, auditory or visual. Two carefully selected subgroups of schizophrenia patients with only auditory hallucinations (AH) or with audio-visual hallucinations (A+VH) were compared using the following three complementary multimodal MRI methods: resting state functional MRI, diffusion MRI and structural MRI were used to analyze seed-based Functional Connectivity (sb-FC), Tract-Based Spatial Statistics (TBSS) and shape analysis, respectively. Sb-FC was significantly higher between the HC, the medial prefrontal cortex (mPFC) and the caudate nuclei in A+VH patients compared with the AH group. Conversely, AH patients exhibited a higher sb-FC between the HC and the thalamus in comparison with the A+VH group. In the A+VH group, TBSS showed specific higher white matter connectivity in the pathways connecting the HC with visual areas, such as the forceps major and the inferior-fronto-occipital fasciculus than in the AH group. Finally, shape analysis showed localized hippocampal hypertrophy in the A+VH group. Functional results support the fronto-limbic dysconnectivity hypothesis of schizophrenia, while specific structural findings indicate that plastic changes are associated with hallucinations. Together, these results suggest that there are distinct connectivity patterns in patients with schizophrenia that depend on the sensory-modality, with specific involvement of the HC in visual hallucinations.

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Acknowledgements

This study was supported by the GDR CNRS - 3557 ‘Institut de Recherche en Psychiatrie’, as well as by grants from the ERANET-NEURON program (AUSZ_EUCan), the Program Hospitalier de Recherche Clinique (PHRC Multimodhal), the Pierre Houriez foundation (hosted by the Fondation de France), the Pierre Deniker foundation and the NRJ foundation. M Mondino held a doctoral fellowship from la Région Rhône-Alpes (France).

Author contributions

All the authors designed the study; AA, PT, DP, RJ recruited the participants; CD, DP, RJ acquired the MRI data; AA, AC, RJ performed the analyses. All the authors contributed to the manuscript writing.

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Authors and Affiliations

  1. Univ Lille Nord de France, CHRU de Lille, Lille, France

    A Amad, C Delmaire, B Rolland, P Thomas & R Jardri

  2. Laboratoire de Neurosciences Fonctionnelles et Pathologies (LNFP), Université Droit & Santé Lille (UDSL), Lille, France

    A Amad, D Pins, C Delmaire, B Rolland, P Thomas & R Jardri

  3. Psychiatry and Pediatric Psychiatry Department, University Medical Centre of Lille (CHULille), Lille, France

    A Amad, B Rolland, P Thomas & R Jardri

  4. INSERM U894, Centre de Psychiatrie & Neurosciences (Paris-Descartes University), Paris, France

    A Cachia & P Gorwood

  5. CNRS U3521, Laboratoire de Psychologie du développement et de l'Éducation de l'Enfant, Paris, France

    A Cachia

  6. Université Paris Descartes, Sorbonne Paris Cité, Paris, France

    A Cachia

  7. Centre National de la Recherche Scientifique (CNRS), Paris, France

    D Pins

  8. Neuroradiology Department, University Medical Centre of Lille (CHULille), Lille, France

    C Delmaire

  9. Équipe d’Accueil 4615, Université Claude Bernard Lyon 1 (UCBL),

    M Mondino

  10. Centre Hospitalier le Vinatier, Bron, France

    M Mondino

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  1. A Amad
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Amad, A., Cachia, A., Gorwood, P. et al. The multimodal connectivity of the hippocampal complex in auditory and visual hallucinations. Mol Psychiatry 19, 184–191 (2014). https://doi.org/10.1038/mp.2012.181

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