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

Molecular Psychiatry

Volumn 19, Issue 2, 2014, Pages 184-191

  Amad, A ^a,b,c   Cachia, A ^d,e,f   Gorwood, P ^d   Pins, D ^b,g   Delmaire, C ^a,b,c   Rolland, B ^a,b,c   Mondino, M ^h   Thomas, P ^a,b,c   Jardri, R ^a,b,c  

^a UNIV LILLE   (France)

^b Amiens University Medical Center and Jules Verne University of Picardy   (France)

^c LILLE UNIVERSITY HOSPITAL   (France)

^d INSERM   (France)

^e Alliance for Higher Education and research Sorbonne Paris Cité   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g CNRS   (France)

^h UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AUDITORY HALLUCINATION; CLINICAL ARTICLE; CLINICAL STUDY; COMPARATIVE STUDY; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; DSM-IV-TR; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPAL COMPLEX; HIPPOCAMPUS; HUMAN; MALE; MEDICAL HISTORY; NEUROLOGIC EXAMINATION; NUCLEAR MAGNETIC RESONANCE IMAGING; POSITIVE AND NEGATIVE SYNDROME SCALE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; STRUCTURAL MAGNETIC RESONANCE IMAGING; VISUAL HALLUCINATION; YOUNG ADULT;

ADULT; ANTIPSYCHOTIC AGENTS; AUDITORY PERCEPTION; BRAIN; BRAIN MAPPING; CAUDATE NUCLEUS; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; HALLUCINATIONS; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE FIBERS, MYELINATED; NEURAL PATHWAYS; PREFRONTAL CORTEX; REST; SCHIZOPHRENIA; THALAMUS; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 84893681653     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2012.181     Document Type: Article

References (75)

1. Andreasen NC, Flaum M. Schizophrenia: the characteristic symptoms. Schizophr Bull 1991; 17: 27-49.
2. Cummings JL, Miller BL. Visual hallucinations: clinical occurrence and use in differential diagnosis. West J Med 1987; 146: 46.
3. Bracha HS, Wolkowitz OM, Lohr JB, Karson CN, Bigelow LB. High prevalence of visual hallucinations in research subjects with chronic schizophrenia. Am J Psychiatry 1989; 146: 526-528.
4. Braun CMJ, Dumont M, Duval J, Hamel-He'bert I, Godbout L. Brain modules of hallucination: an analysis of multiple patients with brain lesions. J Psychiatry Neurosci 2003; 28: 432.
5. Allen P, Larøi F, McGuire PK, Aleman A. The hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev 2008; 32: 175-191.
6. Jardri R, Pouchet A, Pins D, Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am J Psychiatry 2011; 168: 73-81.
7. Ryan L, Nadel L, Keil K, Putnam K, Schnyer D, Trouard T et al. Hippocampal complex and retrieval of recent and very remote autobiographical memories: evidence from functional magnetic resonance imaging in neurologically intact people. Hippocampus 2001; 11: 707-714.
8. Buckholtz JW, Meyer-Lindenberg A. Psychopathology and the human connectome: toward a transdiagnostic model of risk for mental illness. Neuron 2012; 74: 990-1004.
9. ffytche DH. The hodology of hallucinations. Cortex 2008; 44: 1067-1083.
10. Friston KJ. The disconnection hypothesis. Schizophr Res 1998; 30: 115-125.
11. Stephan KE, Baldeweg T, Friston KJ. Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry 2006; 59: 929-939.
12. Stephan KE, Friston KJ, Frith CD. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull 2009; 35: 509-527.
13. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 2011; 473: 221-225.
14. Sullivan PF, Kendler KS, Neale MC. Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch Gen Psychiatry 2003; 60: 1187-1192.
15. Hoffman RE, Hampson M. Functional connectivity studies of patients with auditory verbal hallucinations. Front Hum Neurosci 2012; 6: 6.
16. Allen P, Modinos G, Hubl D, Shields G, Cachia A, Jardri R et al. Neuroimaging auditory hallucinations in schizophrenia: from neuroanatomy to neurochemistry and beyond. Schizophr Bull 2012; 38: 695-703.
17. Jardri R, Thomas P, Delmaire C, Delion P, Pins D. The neurodynamic organization of modality-dependent hallucinations. Cereb Cortex 2013; doi:10.1093/cercor/ bhs082 (in press).
18. Hubl D, Koenig T, Strik W, Federspiel A, Kreis R, Boesch C et al. Pathways that make voices: white matter changes in auditory hallucinations. Arch Gen Psychiatry 2004; 61: 658-668.
19. Shergill SS, Kanaan RA, Chitnis XA, O'Daly O, Jones DK, Frangou S et al. A diffusion tensor imaging study of fasciculi in schizophrenia. Am J Psychiatry 2007; 164: 467-473.
20. Rotarska-Jagiela A, Oertel-Knoechel V, DeMartino F, van de Ven V, Formisano E, Roebroeck A et al. Anatomical brain connectivity and positive symptoms of schizophrenia: a diffusion tensor imaging study. Psychiatry Res 2009; 174: 9-16.
21. de Weijer AD, Neggers SF, Diederen KM, Mandl RW, Kahn RS, Pol HE et al. Aberrations in the arcuate fasciculus are associated with auditory verbal hallucinations in psychotic and in non-psychotic individuals. Hum Brain Mapp 2013; doi:10.1002/hbm.21463 (in press).
22. Catani M, Craig MC, Forkel SJ, Kanaan R, Picchioni M, Toulopoulou T et al. Altered integrity of perisylvian language pathways in schizophrenia: relationship to auditory hallucinations. Biol Psychiatry 2011; 70: 1143-1150.
23. de Weijer AD, Mandl RCW, Diederen KMJ, Neggers SFW, Kahn RS, Pol HEH et al. Microstructural alterations of the arcuate fasciculus in schizophrenia patients with frequent auditory verbal hallucinations. Schizophr Res 2011; 130: 68-77.
24. Johansen-Berg H, Rushworth MFS. Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 2009; 32: 75-94.
25. Dong Q, Welsh RC, Chenevert TL, Carlos RC, Maly-Sundgren P, Gomez-Hassan DM et al. Clinical applications of diffusion tensor imaging. J Magn Reson Imaging 2004; 19: 6-18.
26. Ashtari M, Cottone J, Ardekani BA, Cervellione K, Szeszko PR, Wu J et al. Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography. Arch Gen Psychiatry 2007; 64: 1270-1280.
27. Tamminga CA, Stan AD, Wagner AD. The hippocampal formation in schizophrenia. Am J Psychiatry 2010; 167: 1178-1193.
28. Liddle PF, Friston KJ, Frith CD, Hirsch SR, Jones T, Frackowiak RS. Patterns of cerebral blood flow in schizophrenia. Brit J Psychiatry 1992; 160: 179-186.
29. Silbersweig DA, Stern E, Frith C, Cahill C, Holmes A, Grootoonk S et al. A functional neuroanatomy of hallucinations in schizophrenia. Nature 1995; 378: 176-179.
30. Liddle PF, Lane CJ, Ngan ET. Immediate effects of risperidone on cortico - striato - thalamic loops and the hippocampus. Brit J Psychiatry 2000; 177: 402-407.
31. Behrendt R-P. Contribution of hippocampal region CA3 to consciousness and schizophrenic hallucinations. Neurosci Biobehav Rev 2010; 34: 1121-1136.
32. Oertel V, Rotarska-Jagiela A, van de Ven VG, Haenschel C, Maurer K, Linden DE. Visual hallucinations in schizophrenia investigated with functional magnetic resonance imaging. Psychiatry Res 2007; 156: 269-273.
33. Vignal J-P, Maillard L, McGonigal A, Chauvel P. The dreamy state: hallucinations of autobiographic memory evoked by temporal lobe stimulations and seizures. Brain 2007; 130: 88-99.
34. Sui J, Yu Q, He H, Pearlson GD, Calhoun VD. A selective review of multimodal fusion methods in schizophrenia. Front Hum Neurosci 2012; 6: 27.
35. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, Frackowiak RS et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci USA 2000; 97: 4398-4403.
36. Kay SR, Fiszbein A, Opler LA. The Positive and Negative Syndrome Scale (PANSS) for Schizophrenia. Schizophr Bull 1987; 13: 261-276.
37. Andreasen NC. Methods for assessing positive and negative symptoms. Mod Probl Pharmacopsychiatry 1990; 24: 73-88.
38. Gardner DM, Murphy AL, O'Donnell H, Centorrino F, Baldessarini RJ. International Consensus Study of Antipsychotic Dosing. Am J Psychiatry 2010; 167: 686-693.
39. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004; 23(Supplement 1): S208-S219.
40. David CN, Greenstein D, Clasen L, Gochman P, Miller R, Tossell JW et al. Childhood Onset Schizophrenia: High Rate of Visual Hallucinations. J Am Acad Child Adolesc Psychiatry 2011; 50: 681-686.e3.
41. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage 2006; 31: 1487-1505.
42. Rueckert D, Sonoda LI, Hayes C, Hill DL, Leach MO, Hawkes DJ. Nonrigid registration using free-form deformations: application to breast MR images. IEEE Trans Med Imaging 1999; 18: 712-721.
43. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 1995; 33: 636-647.
44. Goebel R, Esposito F, Formisano E. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp 2006; 27: 392-401.
45. Patenaude B, Smith SM, Kennedy DN, Jenkinson MA. Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage 2011; 56: 907-22.
46. Frisoni GB, Sabattoli F, Lee AD, Dutton RA, Toga AW, Thompson PM. In vivo neuropathology of the hippocampal formation in AD: a radial mapping MR-based study. NeuroImage 2006; 32: 104-110.
47. Thierry A-M, Gioanni Y, De'ge'né tais E, Glowinski J. Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus 2000; 10: 411-419.
48. Howes OD, Kapur S. The Dopamine Hypothesis of Schizophrenia: Version III - The Final Common Pathway. Schizophr Bull 2009; 35: 549-562.
49. Howes OD, Shotbolt P, Bloomfield M, Daalman K, Demjaha A, Diederen KMJ et al. Dopaminergic function in the psychosis spectrum: an [18F]-DOPA imaging study in healthy individuals with auditory hallucinations. Schizophr Bull 2013; doi:10.1093/schbul/sbr195 (in press).
50. Shim YS, Kim J-S, Shon YM, Chung Y-A, Ahn K-J, Yang D-W. A serial study of regional cerebral blood flow deficits in patients with left anterior thalamic infarction: anatomical and neuropsychological correlates. J Neurol Sci 2008; 266: 84-91.
51. Byrne JH, Gray L. Neuroscience Online: An Electronic Textbook for the Neurosciences http://nba.uth.tmc.edu/neuroscience/. Department of Neurobiology and Anatomy - The University of Texas Medical School at Houston (UTHealth)r 1997-2012, all rights reserved:.
52. Ojemann GA. Cortical Organization of Language. J Neurosci 1991; 11: 2281-7.
53. Diederen KM, Daalman K, de Weijer AD, Neggers SF, Van Gastel W, Blom JD et al. Auditory hallucinations elicit similar brain activation in psychotic and nonpsychotic individuals. Schizophr Bull 2011; 38: 1074-1082.
54. Gloor P, Salanova V, Olivier A, Quesney LF. The human dorsal hippocampal commissure. an anatomically identifiable and functional pathway. Brain 1993; 116: 1249-1273.
55. Burgess PW, Veitch E, de Lacy Costello A, Shallice T. The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia 2000; 38: 848-63.
56. Catani M, Jones DK, Donato R, Ffytche DH. Occipito Temporal Connections in the Human Brain. Brain 2003; 126: 2093-2107.
57. Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, In Vivo, DT-MRI Study. Cereb Cortex 2005; 15: 854-869.
58. Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 2011; 12: 585-601.
59. Leutgeb JK, Leutgeb S, Treves A, Meyer R, Barnes CA, McNaughton BL et al. Progressive transformation of hippocampal neuronal representations in 'morphed' environments. Neuron 2005; 48: 345-358.
60. Van Essen DC. A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 1997; 385: 313-318.
61. Qiu A, Tuan TA, Woon PS, Abdul-Rahman MF, Graham S, Sim K. Hippocampalcortical structural connectivity disruptions in schizophrenia: An integrated perspective from hippocampal shape, cortical thickness, and integrity of white matter bundles. NeuroImage 2010; 52: 1181-1189.
62. Kuhn S, Musso F, Mobascher A, Warbrick T, Winterer G, Gallinat J. Hippocampal subfields predict positive symptoms in schizophrenia: first evidence from brain morphometry. Transl Psychiatry 2012; 2: e127.
63. Carter CS, Heckers S, Nichols T, Pine DS, Strother S. Optimizing the Design and Analysis of Clinical Functional Magnetic Resonance Imaging Research Studies. Biol Psychiatry 2008; 64: 842-849.
64. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007; 38: 95-113.
65. Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C et al. Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. NeuroImage 2009; 46: 786-802.
66. Yassa MA, Stark CE. A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. NeuroImage 2009; 44: 319-327.
67. Tahmasebi AM, Abolmaesumi P, Zheng ZZ, Munhall KG, Johnsrude IS. Reducing inter-subject anatomical variation: effect of normalization method on sensitivity of functional magnetic resonance imaging data analysis in auditory cortex and the superior temporal region. NeuroImage 2009; 47: 1522-1531.
68. Meyer-Lindenberg A. From maps to mechanisms through neuroimaging of schizophrenia. Nature 2010; 468: 194-202.
69. Hubl D, Dougoud-Chauvin V, Zeller M, Federspiel A, Boesch C, Strik W et al. Structural analysis of Heschl's gyrus in schizophrenia patients with auditory hallucinations. Neuropsychobiology 2010; 61: 1-9.
70. van Swam C, Federspiel A, Hubl D, Wiest R, Boesch C, Vermathen P et al. Possible dysregulation of cortical plasticity in auditory verbal hallucinations-a cortical thickness study in schizophrenia. J Psychiatr Res 2012; 46: 1015-1023.
71. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S et al. Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008; 31: 234-242.
72. Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R. Vulnerability genes or plasticity genes. Mol Psychiatry 2009; 14: 746-754.
73. Demeulemeester M, Amad A, Bubrovszky M, Pins D, Thomas P, Jardri R. What is the real effect of 1-Hz repetitive transcranial magnetic stimulation on hallucinations? Controlling for publication bias in neuromodulation trials. Biol Psychiatry 2012; 71: e15-16.
74. Hoffman RE, Hampson M, Wu K, Anderson AW, Gore JC, Buchanan RJ et al. Probing the pathophysiology of auditory/verbal hallucinations by combining functional magnetic resonance imaging and transcranial magnetic stimulation. Cerebral Cortex 2007; 17: 2733-2743.
75. Vercammen A, Knegtering H, Liemburg EJ, Boer JA, den, Aleman A. Functional connectivity of the temporo-parietal region in schizophrenia: effects of repetitive transcranial magnetic stimulation treatment of auditory hallucinations. J Psychiatr Res 2010; 44: 725-731.