Functional dysconnectivity of the limbic loop of frontostriatal circuits in first‐episode, treatment‐naive schizophrenia
Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ‐related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology...
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| Veröffentlicht in: | Human brain mapping Jg. 39; H. 2; S. 747 - 757 |
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| Sprache: | Englisch |
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United States
John Wiley & Sons, Inc
01.02.2018
John Wiley and Sons Inc |
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| ISSN: | 1065-9471, 1097-0193, 1097-0193 |
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| Abstract | Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ‐related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology in first‐episode schizophrenia (FESZ). The goal of this study was to identify dysfunctions in discrete frontostriatal circuits that are associated with key features of FESZ. To this end, a case–control, cross‐sectional study was conducted, wherein resting‐state (RS) functional magnetic resonance (fMRI) data were collected from 37 treatment‐naïve FESZ patients and 29 healthy control (HC) subjects. Seed‐based FC analyses were performed by placing six bilateral pairs of seeds within
a priori
defined subdivisions of the striatum. We observed significantly decreased FC for the FESZ group relative to the HC group [
p
< .05, family‐wise error (FWE)‐corrected] in the limbic loop, but not in the sensorimotor or associative loops, of frontostriatal circuitry. Moreover, bilaterally decreased inferior ventral striatum/nucleus accumbens (VSi)‐dorsal anterior cingulate cortex (dACC) FC within the limbic loop correlated inversely with overall FESZ symptom severity and the disorganization factor score of PANSS. These findings provide new insight into the role of frontostriatal limbic loop hypoconnectivity in early‐stage schizophrenia pathology and suggest potential novel therapeutic targets. |
|---|---|
| AbstractList | Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ‐related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology in first‐episode schizophrenia (FESZ). The goal of this study was to identify dysfunctions in discrete frontostriatal circuits that are associated with key features of FESZ. To this end, a case–control, cross‐sectional study was conducted, wherein resting‐state (RS) functional magnetic resonance (fMRI) data were collected from 37 treatment‐naïve FESZ patients and 29 healthy control (HC) subjects. Seed‐based FC analyses were performed by placing six bilateral pairs of seeds within
a priori
defined subdivisions of the striatum. We observed significantly decreased FC for the FESZ group relative to the HC group [
p
< .05, family‐wise error (FWE)‐corrected] in the limbic loop, but not in the sensorimotor or associative loops, of frontostriatal circuitry. Moreover, bilaterally decreased inferior ventral striatum/nucleus accumbens (VSi)‐dorsal anterior cingulate cortex (dACC) FC within the limbic loop correlated inversely with overall FESZ symptom severity and the disorganization factor score of PANSS. These findings provide new insight into the role of frontostriatal limbic loop hypoconnectivity in early‐stage schizophrenia pathology and suggest potential novel therapeutic targets. Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ‐related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology in first‐episode schizophrenia (FESZ). The goal of this study was to identify dysfunctions in discrete frontostriatal circuits that are associated with key features of FESZ. To this end, a case–control, cross‐sectional study was conducted, wherein resting‐state (RS) functional magnetic resonance (fMRI) data were collected from 37 treatment‐naïve FESZ patients and 29 healthy control (HC) subjects. Seed‐based FC analyses were performed by placing six bilateral pairs of seeds within a priori defined subdivisions of the striatum. We observed significantly decreased FC for the FESZ group relative to the HC group [p < .05, family‐wise error (FWE)‐corrected] in the limbic loop, but not in the sensorimotor or associative loops, of frontostriatal circuitry. Moreover, bilaterally decreased inferior ventral striatum/nucleus accumbens (VSi)‐dorsal anterior cingulate cortex (dACC) FC within the limbic loop correlated inversely with overall FESZ symptom severity and the disorganization factor score of PANSS. These findings provide new insight into the role of frontostriatal limbic loop hypoconnectivity in early‐stage schizophrenia pathology and suggest potential novel therapeutic targets. Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ-related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology in first-episode schizophrenia (FESZ). The goal of this study was to identify dysfunctions in discrete frontostriatal circuits that are associated with key features of FESZ. To this end, a case-control, cross-sectional study was conducted, wherein resting-state (RS) functional magnetic resonance (fMRI) data were collected from 37 treatment-naïve FESZ patients and 29 healthy control (HC) subjects. Seed-based FC analyses were performed by placing six bilateral pairs of seeds within a priori defined subdivisions of the striatum. We observed significantly decreased FC for the FESZ group relative to the HC group [p < .05, family-wise error (FWE)-corrected] in the limbic loop, but not in the sensorimotor or associative loops, of frontostriatal circuitry. Moreover, bilaterally decreased inferior ventral striatum/nucleus accumbens (VSi)-dorsal anterior cingulate cortex (dACC) FC within the limbic loop correlated inversely with overall FESZ symptom severity and the disorganization factor score of PANSS. These findings provide new insight into the role of frontostriatal limbic loop hypoconnectivity in early-stage schizophrenia pathology and suggest potential novel therapeutic targets.Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have investigated SZ-related functional connectivity (FC) alterations in discrete frontostriatal circuits and their relationship with pathopsychology in first-episode schizophrenia (FESZ). The goal of this study was to identify dysfunctions in discrete frontostriatal circuits that are associated with key features of FESZ. To this end, a case-control, cross-sectional study was conducted, wherein resting-state (RS) functional magnetic resonance (fMRI) data were collected from 37 treatment-naïve FESZ patients and 29 healthy control (HC) subjects. Seed-based FC analyses were performed by placing six bilateral pairs of seeds within a priori defined subdivisions of the striatum. We observed significantly decreased FC for the FESZ group relative to the HC group [p < .05, family-wise error (FWE)-corrected] in the limbic loop, but not in the sensorimotor or associative loops, of frontostriatal circuitry. Moreover, bilaterally decreased inferior ventral striatum/nucleus accumbens (VSi)-dorsal anterior cingulate cortex (dACC) FC within the limbic loop correlated inversely with overall FESZ symptom severity and the disorganization factor score of PANSS. These findings provide new insight into the role of frontostriatal limbic loop hypoconnectivity in early-stage schizophrenia pathology and suggest potential novel therapeutic targets. |
| Author | Lin, Pan Wang, Xiang Yao, Shuqiao Kirkpatrick, Brian Wang, Xiaosheng Öngür, Dost Jovicich, Jorge Zhang, Bei Levitt, James J. |
| AuthorAffiliation | 2 Department of Human Anatomy and Neurobiology Xiangya School of Medicine, Central South University Changsha Hunan 410013 China 8 Center for Mind/Brain Sciences, University of Trento Mattarello 38100 Italy 4 Department of Psychology Experimental Psychology, Ludwig‐Maximilians‐Universität München 80802 Munich Germany 5 Department of Psychiatry & Behavioral Sciences University of Nevada School of Medicine Reno Nevada 89509 6 Department of Psychiatry Harvard Medical School and McLean Hospital Belmont Massachusetts 02478 1 Key Laboratory of Cognitive Science College of Biomedical Engineering, South‐Central University for Nationalities Wuhan 430074 China 3 Medical Psychological Center The Second Xiangya Hospital, Central South University Changsha Hunan 410011 China 7 Department of Psychiatry Harvard Medical School and VA Boston Healthcare System Boston Massachusetts 02215 |
| AuthorAffiliation_xml | – name: 3 Medical Psychological Center The Second Xiangya Hospital, Central South University Changsha Hunan 410011 China – name: 1 Key Laboratory of Cognitive Science College of Biomedical Engineering, South‐Central University for Nationalities Wuhan 430074 China – name: 5 Department of Psychiatry & Behavioral Sciences University of Nevada School of Medicine Reno Nevada 89509 – name: 8 Center for Mind/Brain Sciences, University of Trento Mattarello 38100 Italy – name: 6 Department of Psychiatry Harvard Medical School and McLean Hospital Belmont Massachusetts 02478 – name: 7 Department of Psychiatry Harvard Medical School and VA Boston Healthcare System Boston Massachusetts 02215 – name: 2 Department of Human Anatomy and Neurobiology Xiangya School of Medicine, Central South University Changsha Hunan 410013 China – name: 4 Department of Psychology Experimental Psychology, Ludwig‐Maximilians‐Universität München 80802 Munich Germany |
| Author_xml | – sequence: 1 givenname: Pan surname: Lin fullname: Lin, Pan organization: Key Laboratory of Cognitive Science College of Biomedical Engineering, South‐Central University for Nationalities Wuhan 430074 China – sequence: 2 givenname: Xiaosheng surname: Wang fullname: Wang, Xiaosheng organization: Department of Human Anatomy and Neurobiology Xiangya School of Medicine, Central South University Changsha Hunan 410013 China – sequence: 3 givenname: Bei surname: Zhang fullname: Zhang, Bei organization: Medical Psychological Center The Second Xiangya Hospital, Central South University Changsha Hunan 410011 China, Department of Psychology Experimental Psychology, Ludwig‐Maximilians‐Universität München 80802 Munich Germany – sequence: 4 givenname: Brian surname: Kirkpatrick fullname: Kirkpatrick, Brian organization: Department of Psychiatry & Behavioral Sciences University of Nevada School of Medicine Reno Nevada 89509 – sequence: 5 givenname: Dost surname: Öngür fullname: Öngür, Dost organization: Department of Psychiatry Harvard Medical School and McLean Hospital Belmont Massachusetts 02478 – sequence: 6 givenname: James J. surname: Levitt fullname: Levitt, James J. organization: Department of Psychiatry Harvard Medical School and VA Boston Healthcare System Boston Massachusetts 02215 – sequence: 7 givenname: Jorge surname: Jovicich fullname: Jovicich, Jorge organization: Center for Mind/Brain Sciences, University of Trento Mattarello 38100 Italy – sequence: 8 givenname: Shuqiao surname: Yao fullname: Yao, Shuqiao organization: Medical Psychological Center The Second Xiangya Hospital, Central South University Changsha Hunan 410011 China – sequence: 9 givenname: Xiang orcidid: 0000-0001-9258-2017 surname: Wang fullname: Wang, Xiang organization: Medical Psychological Center The Second Xiangya Hospital, Central South University Changsha Hunan 410011 China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29094787$$D View this record in MEDLINE/PubMed |
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| Keywords | dorsal anterior cingulate cortex resting-state functional connectivity ventral striatum first-episode schizophrenia frontostriatal circuits |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Pan Lin and Xiaosheng Wang contributed equally to this work. Funding information National Natural Science Foundation of China, Grant/Award Number: 31671144, 61473221, 81471104; New Century Excellent Talents in University at the Chinese Ministry of Education, Grant/Award Number: NCET‐12‐0557 |
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| Snippet | Frontostriatal circuits dysfunction has been implicated in the etiology and psychopathology of patients with schizophrenia (SZ). However, few studies have... |
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| SubjectTerms | Brain - diagnostic imaging Brain - physiopathology Brain Mapping Case-Control Studies Circuits Cortex (cingulate) Cross-Sectional Studies Error correction Error detection Etiology Female Functional magnetic resonance imaging Humans Magnetic resonance imaging Male Mental disorders Neostriatum Neural Pathways - diagnostic imaging Neural Pathways - physiopathology Nucleus accumbens Patients Psychiatric Status Rating Scales Psychopathology Rest Schizophrenia Schizophrenia - diagnostic imaging Schizophrenia - physiopathology Seeds Sensorimotor system Subdivisions Young Adult |
| Title | Functional dysconnectivity of the limbic loop of frontostriatal circuits in first‐episode, treatment‐naive schizophrenia |
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