Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis

Jussi Alho; Juha M. Lahnakoski; Jonatan M. Panula; Eva Rikandi; Teemu Mäntylä; Maija Lindgren; Tuula Kieseppä; Jaana Suvisaari; Mikko Sams; Tuukka T. Raij

doi:10.1016/j.bpsc.2023.06.002

Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis

Jussi Alho^*, Juha M. Lahnakoski, Jonatan M. Panula, Eva Rikandi, Teemu Mäntylä, Maija Lindgren, Tuula Kieseppä, Jaana Suvisaari, Mikko Sams, Tuukka T. Raij^*

^*Corresponding author for this work

Department of Neuroscience and Biomedical Engineering

Research output: Contribution to journal › Article › Scientific › peer-review

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Abstract

Background: Previous functional magnetic resonance imaging studies have reported widespread brain functional connectivity alterations in patients with psychosis. These studies have mostly used either resting-state or simple-task paradigms, thereby compromising experimental control or ecological validity, respectively. Additionally, in a conventional functional magnetic resonance imaging intrasubject functional connectivity analysis, it is difficult to identify which connections relate to extrinsic (stimulus-induced) and which connections relate to intrinsic (non–stimulus-related) neural processes. Methods: To mitigate these limitations, we used intersubject functional connectivity (ISFC) to analyze longitudinal functional magnetic resonance imaging data collected while 36 individuals with first-episode psychosis (FEP) and 29 age- and sex-matched population control participants watched scenes from the fantasy movie Alice in Wonderland at baseline and again at 1-year follow-up. Furthermore, to allow unconfounded comparison and to overcome possible circularity of ISFC, we introduced a novel approach wherein ISFC in both the FEP and population control groups was calculated with respect to an independent group of participants (not included in the analyses). Results: Using this independent-reference ISFC approach, we found an interaction effect wherein the independent-reference ISFC in individuals with FEP, but not in the control group participants, was significantly stronger at baseline than at follow-up in a network centered in the hippocampus and involving thalamic, striatal, and cortical regions, such as the orbitofrontal cortex. Alleviation of positive symptoms, particularly delusions, from baseline to follow-up was correlated with decreased network connectivity in patients with FEP. Conclusions: These findings link deviation of naturalistic information processing in the hippocampus-centered network to positive symptoms.

Original language	English
Pages (from-to)	1197-1206
Number of pages	10
Journal	Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
Volume	8
Issue number	12
Early online date	2023
DOIs	https://doi.org/10.1016/j.bpsc.2023.06.002
Publication status	Published - Dec 2023
MoE publication type	A1 Journal article-refereed

Funding

This work was supported by the Sigrid Jusélius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union's Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]). We thank the study participants and Laura Hietapakka, Marita Kattelus, Sanna Leppänen, Tuula Mononen, Minna Holm, and Marjut Grainger for their contribution to data collection. The authors report no biomedical financial interests or potential conflicts of interest. This work was supported by the Sigrid Jusélius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union’s Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]).

Keywords

Functional connectivity
Functional magnetic resonance imaging (fMRI)
Hippocampus
Movie
Positive symptoms
Psychosis

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Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode PsychosisFinal published version, 1.5 MBLicence: CC BY

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Alho, J., Lahnakoski, J. M., Panula, J. M., Rikandi, E., Mäntylä, T., Lindgren, M., Kieseppä, T., Suvisaari, J., Sams, M., & Raij, T. T. (2023). Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 8(12), 1197-1206. https://doi.org/10.1016/j.bpsc.2023.06.002

@article{8921112167ac44369315bd922c9cfc98,

title = "Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis",

abstract = "Background: Previous functional magnetic resonance imaging studies have reported widespread brain functional connectivity alterations in patients with psychosis. These studies have mostly used either resting-state or simple-task paradigms, thereby compromising experimental control or ecological validity, respectively. Additionally, in a conventional functional magnetic resonance imaging intrasubject functional connectivity analysis, it is difficult to identify which connections relate to extrinsic (stimulus-induced) and which connections relate to intrinsic (non–stimulus-related) neural processes. Methods: To mitigate these limitations, we used intersubject functional connectivity (ISFC) to analyze longitudinal functional magnetic resonance imaging data collected while 36 individuals with first-episode psychosis (FEP) and 29 age- and sex-matched population control participants watched scenes from the fantasy movie Alice in Wonderland at baseline and again at 1-year follow-up. Furthermore, to allow unconfounded comparison and to overcome possible circularity of ISFC, we introduced a novel approach wherein ISFC in both the FEP and population control groups was calculated with respect to an independent group of participants (not included in the analyses). Results: Using this independent-reference ISFC approach, we found an interaction effect wherein the independent-reference ISFC in individuals with FEP, but not in the control group participants, was significantly stronger at baseline than at follow-up in a network centered in the hippocampus and involving thalamic, striatal, and cortical regions, such as the orbitofrontal cortex. Alleviation of positive symptoms, particularly delusions, from baseline to follow-up was correlated with decreased network connectivity in patients with FEP. Conclusions: These findings link deviation of naturalistic information processing in the hippocampus-centered network to positive symptoms.",

keywords = "Functional connectivity, Functional magnetic resonance imaging (fMRI), Hippocampus, Movie, Positive symptoms, Psychosis",

author = "Jussi Alho and Lahnakoski, \{Juha M.\} and Panula, \{Jonatan M.\} and Eva Rikandi and Teemu M{\"a}ntyl{\"a} and Maija Lindgren and Tuula Kiesepp{\"a} and Jaana Suvisaari and Mikko Sams and Raij, \{Tuukka T.\}",

note = "Funding Information: This work was supported by the Sigrid Jus{\'e}lius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union's Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]). We thank the study participants and Laura Hietapakka, Marita Kattelus, Sanna Lepp{\"a}nen, Tuula Mononen, Minna Holm, and Marjut Grainger for their contribution to data collection. The authors report no biomedical financial interests or potential conflicts of interest. Funding Information: This work was supported by the Sigrid Jus{\'e}lius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union{\textquoteright}s Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]). Publisher Copyright: {\textcopyright} 2023 Society of Biological Psychiatry",

year = "2023",

month = dec,

doi = "10.1016/j.bpsc.2023.06.002",

language = "English",

volume = "8",

pages = "1197--1206",

journal = "Biological Psychiatry: Cognitive Neuroscience and Neuroimaging",

issn = "2451-9022",

publisher = "Elsevier",

number = "12",

}

Alho, J, Lahnakoski, JM, Panula, JM, Rikandi, E, Mäntylä, T, Lindgren, M, Kieseppä, T, Suvisaari, J, Sams, M & Raij, TT 2023, 'Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis', Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, vol. 8, no. 12, pp. 1197-1206. https://doi.org/10.1016/j.bpsc.2023.06.002

Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis. / Alho, Jussi; Lahnakoski, Juha M.; Panula, Jonatan M. et al.
In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, Vol. 8, No. 12, 12.2023, p. 1197-1206.

Research output: Contribution to journal › Article › Scientific › peer-review

TY - JOUR

T1 - Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis

AU - Alho, Jussi

AU - Lahnakoski, Juha M.

AU - Panula, Jonatan M.

AU - Rikandi, Eva

AU - Mäntylä, Teemu

AU - Lindgren, Maija

AU - Kieseppä, Tuula

AU - Suvisaari, Jaana

AU - Sams, Mikko

AU - Raij, Tuukka T.

N1 - Funding Information: This work was supported by the Sigrid Jusélius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union's Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]). We thank the study participants and Laura Hietapakka, Marita Kattelus, Sanna Leppänen, Tuula Mononen, Minna Holm, and Marjut Grainger for their contribution to data collection. The authors report no biomedical financial interests or potential conflicts of interest. Funding Information: This work was supported by the Sigrid Jusélius Foundation (to JS and TTR), the Finnish Cultural Foundation (to JML and JS), the Academy of Finland (Grant Nos. 278171 and 323035 [to JS] and Grant No. 315861 [to TTR]), the Finnish Medical Foundation (to JMP and TTR), the Medical Society of Finland (to JMP), state funding for university-level health research (Hospital District of Helsinki and Uusimaa, Grant Nos. TYH2013332, TYH2014228, and TYH2017128 [to TK]), and the European Union’s Seventh Framework Programme for project METSY (Grant No. 602478 [to JS]). Publisher Copyright: © 2023 Society of Biological Psychiatry

PY - 2023/12

Y1 - 2023/12

N2 - Background: Previous functional magnetic resonance imaging studies have reported widespread brain functional connectivity alterations in patients with psychosis. These studies have mostly used either resting-state or simple-task paradigms, thereby compromising experimental control or ecological validity, respectively. Additionally, in a conventional functional magnetic resonance imaging intrasubject functional connectivity analysis, it is difficult to identify which connections relate to extrinsic (stimulus-induced) and which connections relate to intrinsic (non–stimulus-related) neural processes. Methods: To mitigate these limitations, we used intersubject functional connectivity (ISFC) to analyze longitudinal functional magnetic resonance imaging data collected while 36 individuals with first-episode psychosis (FEP) and 29 age- and sex-matched population control participants watched scenes from the fantasy movie Alice in Wonderland at baseline and again at 1-year follow-up. Furthermore, to allow unconfounded comparison and to overcome possible circularity of ISFC, we introduced a novel approach wherein ISFC in both the FEP and population control groups was calculated with respect to an independent group of participants (not included in the analyses). Results: Using this independent-reference ISFC approach, we found an interaction effect wherein the independent-reference ISFC in individuals with FEP, but not in the control group participants, was significantly stronger at baseline than at follow-up in a network centered in the hippocampus and involving thalamic, striatal, and cortical regions, such as the orbitofrontal cortex. Alleviation of positive symptoms, particularly delusions, from baseline to follow-up was correlated with decreased network connectivity in patients with FEP. Conclusions: These findings link deviation of naturalistic information processing in the hippocampus-centered network to positive symptoms.

AB - Background: Previous functional magnetic resonance imaging studies have reported widespread brain functional connectivity alterations in patients with psychosis. These studies have mostly used either resting-state or simple-task paradigms, thereby compromising experimental control or ecological validity, respectively. Additionally, in a conventional functional magnetic resonance imaging intrasubject functional connectivity analysis, it is difficult to identify which connections relate to extrinsic (stimulus-induced) and which connections relate to intrinsic (non–stimulus-related) neural processes. Methods: To mitigate these limitations, we used intersubject functional connectivity (ISFC) to analyze longitudinal functional magnetic resonance imaging data collected while 36 individuals with first-episode psychosis (FEP) and 29 age- and sex-matched population control participants watched scenes from the fantasy movie Alice in Wonderland at baseline and again at 1-year follow-up. Furthermore, to allow unconfounded comparison and to overcome possible circularity of ISFC, we introduced a novel approach wherein ISFC in both the FEP and population control groups was calculated with respect to an independent group of participants (not included in the analyses). Results: Using this independent-reference ISFC approach, we found an interaction effect wherein the independent-reference ISFC in individuals with FEP, but not in the control group participants, was significantly stronger at baseline than at follow-up in a network centered in the hippocampus and involving thalamic, striatal, and cortical regions, such as the orbitofrontal cortex. Alleviation of positive symptoms, particularly delusions, from baseline to follow-up was correlated with decreased network connectivity in patients with FEP. Conclusions: These findings link deviation of naturalistic information processing in the hippocampus-centered network to positive symptoms.

KW - Functional connectivity

KW - Functional magnetic resonance imaging (fMRI)

KW - Hippocampus

KW - Movie

KW - Positive symptoms

KW - Psychosis

UR - https://www.scopus.com/pages/publications/85172286745

U2 - 10.1016/j.bpsc.2023.06.002

DO - 10.1016/j.bpsc.2023.06.002

M3 - Article

C2 - 37336263

AN - SCOPUS:85172286745

SN - 2451-9022

VL - 8

SP - 1197

EP - 1206

JO - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

JF - Biological Psychiatry: Cognitive Neuroscience and Neuroimaging

IS - 12

ER -

Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis

Abstract

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Hippocampus-Centered Network Is Associated With Positive Symptom Alleviation in Patients With First-Episode Psychosis

Abstract

Funding

Keywords

Access to Document

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