Visual Hallucinations in Psychosis: The Curious Absence of the Primary Visual Cortex.
functional magnetic resonance imaging
schizophrenia
visual hallucinations
Journal
Schizophrenia bulletin
ISSN: 1745-1701
Titre abrégé: Schizophr Bull
Pays: United States
ID NLM: 0236760
Informations de publication
Date de publication:
24 02 2023
24 02 2023
Historique:
pmc-release:
25
02
2024
entrez:
25
2
2023
pubmed:
26
2
2023
medline:
3
3
2023
Statut:
ppublish
Résumé
Approximately one-third of patients with a psychotic disorder experience visual hallucinations (VH). While new, more targeted treatment options are warranted, the pathophysiology of VH remains largely unknown. Previous studies hypothesized that VH result from impaired functioning of the vision-related networks and impaired interaction between those networks, including a possible functional disconnection between the primary visual cortex (V1) and higher-order visual processing regions. Testing these hypotheses requires sufficient data on brain activation during actual VH, but such data are extremely scarce. We therefore recruited seven participants with a psychotic disorder who were scanned in a 3 T fMRI scanner while indicating the occurrence of VH by pressing a button. Following the scan session, we interviewed participants about the VH experienced during scanning. We then used the fMRI scans to identify regions with increased or decreased activity during VH periods versus baseline (no VH). In six participants, V1 was not activated during VH, and in one participant V1 showed decreased activation. All participants reported complex VH such as human-like beings, objects and/or animals, during which higher-order visual areas and regions belonging to the vision-related networks on attention and memory were activated. These results indicate that VH are associated with diffuse involvement of the vision-related networks, with the exception of V1. We therefore propose a model for the pathophysiology of psychotic VH in which a dissociation of higher-order visual processing areas from V1 biases conscious perception away from reality and towards internally generated percepts.
Sections du résumé
BACKGROUND AND HYPOTHESIS
Approximately one-third of patients with a psychotic disorder experience visual hallucinations (VH). While new, more targeted treatment options are warranted, the pathophysiology of VH remains largely unknown. Previous studies hypothesized that VH result from impaired functioning of the vision-related networks and impaired interaction between those networks, including a possible functional disconnection between the primary visual cortex (V1) and higher-order visual processing regions. Testing these hypotheses requires sufficient data on brain activation during actual VH, but such data are extremely scarce.
STUDY DESIGN
We therefore recruited seven participants with a psychotic disorder who were scanned in a 3 T fMRI scanner while indicating the occurrence of VH by pressing a button. Following the scan session, we interviewed participants about the VH experienced during scanning. We then used the fMRI scans to identify regions with increased or decreased activity during VH periods versus baseline (no VH).
STUDY RESULTS
In six participants, V1 was not activated during VH, and in one participant V1 showed decreased activation. All participants reported complex VH such as human-like beings, objects and/or animals, during which higher-order visual areas and regions belonging to the vision-related networks on attention and memory were activated.
DISCUSSION
These results indicate that VH are associated with diffuse involvement of the vision-related networks, with the exception of V1. We therefore propose a model for the pathophysiology of psychotic VH in which a dissociation of higher-order visual processing areas from V1 biases conscious perception away from reality and towards internally generated percepts.
Identifiants
pubmed: 36840543
pii: 7058009
doi: 10.1093/schbul/sbac140
pmc: PMC9960034
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
S68-S81Subventions
Organisme : Graduate School Medical Sciences
Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com.
Références
Cortex. 2008 Sep;44(8):1067-83
pubmed: 18586234
PLoS One. 2019 Aug 20;14(8):e0212379
pubmed: 31430277
Schizophr Bull. 2012 Jun;38(4):704-14
pubmed: 22368234
Optometry. 2009 Jul;80(7):360-6
pubmed: 19545849
Psychol Med. 2016 Jun;46(8):1735-47
pubmed: 26984533
Schizophr Bull. 2019 Feb 1;45(45 Suppl 1):S78-S87
pubmed: 30715541
Am J Geriatr Psychiatry. 2006 Feb;14(2):153-60
pubmed: 16473980
Arch Neurol. 2008 Jun;65(6):709-14
pubmed: 18541791
J Psychiatr Res. 1975 Nov;12(3):189-98
pubmed: 1202204
J Neurol Neurosurg Psychiatry. 2001 Jun;70(6):727-33
pubmed: 11385004
Neuroimage Clin. 2018;20:830-843
pubmed: 30273840
Schizophr Bull. 2014 Jul;40 Suppl 4:S233-45
pubmed: 24936084
Hum Brain Mapp. 2016 Jul;37(7):2571-86
pubmed: 27016153
Cereb Cortex. 2017 May 1;27(5):2984-2993
pubmed: 27226446
J Neurol Neurosurg Psychiatry. 2010 Nov;81(11):1280-7
pubmed: 20972204
Philos Trans R Soc Lond B Biol Sci. 2006 Dec 29;361(1476):2109-28
pubmed: 17118927
Neuroimage. 2001 Sep;14(3):661-73
pubmed: 11506539
Cereb Cortex. 2013 May;23(5):1108-17
pubmed: 22535908
Brain. 2008 Dec;131(Pt 12):3169-77
pubmed: 18854323
Neuroimage. 2011 Feb 1;54(3):2297-307
pubmed: 20869451
Prog Neurobiol. 2014 May;116:58-65
pubmed: 24525149
Trends Cogn Sci. 2011 Oct;15(10):483-506
pubmed: 21908230
Annu Rev Neurosci. 2005;28:157-89
pubmed: 16022593
Mov Disord. 2005 Feb;20(2):130-40
pubmed: 15486924
Schizophr Bull. 2023 Feb 24;49(Supplement_1):S68-S81
pubmed: 36840543
Psychiatry Res. 2020 Aug;290:113141
pubmed: 32521380
Mol Psychiatry. 2014 Feb;19(2):184-91
pubmed: 23318999
Schizophr Bull. 1987;13(2):261-76
pubmed: 3616518
Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6827-32
pubmed: 15096584
Am J Psychiatry. 2011 Jan;168(1):73-81
pubmed: 20952459
Psychiatry Res. 2019 Oct;280:112517
pubmed: 31446216
Iran J Psychiatry Behav Sci. 2016 Mar 15;10(1):e3561
pubmed: 27284279
Neuroimage Clin. 2018 Mar 01;18:682-693
pubmed: 29876260
Behav Brain Sci. 2005 Dec;28(6):737-57; discussion 757-94
pubmed: 16372931
Annu Rev Vis Sci. 2017 Sep 15;3:197-226
pubmed: 28617660
Neuroreport. 2000 Sep 28;11(14):3269-73
pubmed: 11043562
Elife. 2018 Aug 14;7:
pubmed: 30106371
Arch Gen Psychiatry. 2000 Nov;57(11):1033-8
pubmed: 11074868
Nat Neurosci. 1998 Dec;1(8):738-42
pubmed: 10196592
Brain. 2000 Oct;123 ( Pt 10):2055-64
pubmed: 11004123
Neuroimage. 2003 Dec;20(4):2259-70
pubmed: 14683727
Eur Rev Med Pharmacol Sci. 2012 Oct;16 Suppl 4:64-5
pubmed: 23090812
Neuropsychologia. 2003;41(5):565-74
pubmed: 12559149
Front Hum Neurosci. 2013 Apr 24;7:144
pubmed: 23630479
Prog Neurobiol. 2017 Jan;148:1-20
pubmed: 27890810
Neuropsychologia. 2014 Nov;64:134-44
pubmed: 25258247
Trends Cogn Sci. 2013 Jan;17(1):26-49
pubmed: 23265839
Cogn Neuropsychiatry. 2004 Feb-May;9(1-2):107-23
pubmed: 16571577
Nature. 1995 Nov 9;378(6553):176-9
pubmed: 7477318
Cereb Cortex. 2013 Jun;23(6):1362-77
pubmed: 22610393
Science. 2001 Sep 28;293(5539):2470-3
pubmed: 11577239
Neuroimage. 2015 May 15;112:267-277
pubmed: 25770991
Schizophr Res. 1998 Aug 17;32(3):137-50
pubmed: 9720119
Psychiatry Res. 2007 Dec 15;156(3):269-73
pubmed: 17976960
Neuroimage. 2003 Dec;20(4):1934-43
pubmed: 14683699
J Neurol Neurosurg Psychiatry. 2002 Nov;73(5):535-41
pubmed: 12397147
Mov Disord. 2019 Aug;34(8):1100-1111
pubmed: 31307115
Brain Stimul. 2019 Nov - Dec;12(6):1622-1624
pubmed: 31543281
Neuron. 1999 Mar;22(3):615-21
pubmed: 10197540
Annu Rev Vis Sci. 2015 Nov;1:351-371
pubmed: 28217740
Schizophr Bull. 2015 Jan;41(1):223-32
pubmed: 24619536
Nat Rev Neurosci. 2019 Oct;20(10):593-608
pubmed: 31492945