Opposing patterns of neuronal variability in the sensorimotor network mediate cyclothymic and depressive temperaments
Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the r...
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Published in | Human brain mapping Vol. 40; no. 4; pp. 1344 - 1352 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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John Wiley & Sons, Inc
01.03.2019
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Abstract | Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the resting state signal—measured by fractional standard deviation (fSD) of Blood‐Oxygen‐Level Dependent signal—of the different large‐scale networks, that is, sensorimotor network (SMN), along with default‐mode, salience and central executive networks, in standard frequency band (SFB) and its sub‐frequencies slow4 and slow5, in a large sample of healthy subject (HC, n = 109), as well as in the various temperamental subgroups (i.e., cyclothymic, hyperthymic, depressive, and irritable). A replication study on an independent dataset of 121 HC was then performed. SMN fSD positively correlated with cyclothymic z‐score and was significantly increased in the cyclothymic temperament compared to the depressive temperament subgroups, in both SFB and slow4. We replicated our findings in the independent dataset. A relationship between cyclothymic temperament and neuronal variability, an index of intrinsic neuronal activity, in the SMN was found. Cyclothymic and depressive temperaments were associated with opposite changes in the SMN variability, resembling changes previously described in manic and depressive phases of BD. These findings shed a novel light on the neural basis of affective temperament and also carry important implications for the understanding of a potential dimensional continuum between affective temperaments and BD, on both psychological and neuronal levels. |
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AbstractList | Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the resting state signal—measured by fractional standard deviation (fSD) of Blood‐Oxygen‐Level Dependent signal—of the different large‐scale networks, that is, sensorimotor network (SMN), along with default‐mode, salience and central executive networks, in standard frequency band (SFB) and its sub‐frequencies slow4 and slow5, in a large sample of healthy subject (HC, n = 109), as well as in the various temperamental subgroups (i.e., cyclothymic, hyperthymic, depressive, and irritable). A replication study on an independent dataset of 121 HC was then performed. SMN fSD positively correlated with cyclothymic z‐score and was significantly increased in the cyclothymic temperament compared to the depressive temperament subgroups, in both SFB and slow4. We replicated our findings in the independent dataset. A relationship between cyclothymic temperament and neuronal variability, an index of intrinsic neuronal activity, in the SMN was found. Cyclothymic and depressive temperaments were associated with opposite changes in the SMN variability, resembling changes previously described in manic and depressive phases of BD. These findings shed a novel light on the neural basis of affective temperament and also carry important implications for the understanding of a potential dimensional continuum between affective temperaments and BD, on both psychological and neuronal levels. Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the resting state signal—measured by fractional standard deviation (fSD) of Blood‐Oxygen‐Level Dependent signal—of the different large‐scale networks, that is, sensorimotor network (SMN), along with default‐mode, salience and central executive networks, in standard frequency band (SFB) and its sub‐frequencies slow4 and slow5, in a large sample of healthy subject (HC, n = 109), as well as in the various temperamental subgroups (i.e., cyclothymic, hyperthymic, depressive, and irritable). A replication study on an independent dataset of 121 HC was then performed. SMN fSD positively correlated with cyclothymic z‐score and was significantly increased in the cyclothymic temperament compared to the depressive temperament subgroups, in both SFB and slow4. We replicated our findings in the independent dataset. A relationship between cyclothymic temperament and neuronal variability, an index of intrinsic neuronal activity, in the SMN was found. Cyclothymic and depressive temperaments were associated with opposite changes in the SMN variability, resembling changes previously described in manic and depressive phases of BD. These findings shed a novel light on the neural basis of affective temperament and also carry important implications for the understanding of a potential dimensional continuum between affective temperaments and BD, on both psychological and neuronal levels. Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the resting state signal-measured by fractional standard deviation (fSD) of Blood-Oxygen-Level Dependent signal-of the different large-scale networks, that is, sensorimotor network (SMN), along with default-mode, salience and central executive networks, in standard frequency band (SFB) and its sub-frequencies slow4 and slow5, in a large sample of healthy subject (HC, n = 109), as well as in the various temperamental subgroups (i.e., cyclothymic, hyperthymic, depressive, and irritable). A replication study on an independent dataset of 121 HC was then performed. SMN fSD positively correlated with cyclothymic z-score and was significantly increased in the cyclothymic temperament compared to the depressive temperament subgroups, in both SFB and slow4. We replicated our findings in the independent dataset. A relationship between cyclothymic temperament and neuronal variability, an index of intrinsic neuronal activity, in the SMN was found. Cyclothymic and depressive temperaments were associated with opposite changes in the SMN variability, resembling changes previously described in manic and depressive phases of BD. These findings shed a novel light on the neural basis of affective temperament and also carry important implications for the understanding of a potential dimensional continuum between affective temperaments and BD, on both psychological and neuronal levels.Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD). However, the neuronal basis of temperament is still unclear. We investigated the relationship of temperament with neuronal variability in the resting state signal-measured by fractional standard deviation (fSD) of Blood-Oxygen-Level Dependent signal-of the different large-scale networks, that is, sensorimotor network (SMN), along with default-mode, salience and central executive networks, in standard frequency band (SFB) and its sub-frequencies slow4 and slow5, in a large sample of healthy subject (HC, n = 109), as well as in the various temperamental subgroups (i.e., cyclothymic, hyperthymic, depressive, and irritable). A replication study on an independent dataset of 121 HC was then performed. SMN fSD positively correlated with cyclothymic z-score and was significantly increased in the cyclothymic temperament compared to the depressive temperament subgroups, in both SFB and slow4. We replicated our findings in the independent dataset. A relationship between cyclothymic temperament and neuronal variability, an index of intrinsic neuronal activity, in the SMN was found. Cyclothymic and depressive temperaments were associated with opposite changes in the SMN variability, resembling changes previously described in manic and depressive phases of BD. These findings shed a novel light on the neural basis of affective temperament and also carry important implications for the understanding of a potential dimensional continuum between affective temperaments and BD, on both psychological and neuronal levels. |
Author | Escelsior, Andrea Russo, Daniel Amore, Mario Inglese, Matilde Magioncalda, Paola Martino, Matteo Northoff, Georg Tumati, Shankar Conio, Benedetta Capobianco, Laura Adavastro, Giulia |
AuthorAffiliation | 2 IRCCS Ospedale Policlinico San Martino Genoa Italy 5 Brain and Mind Research Institute, Mind Brain Imaging and Neuroethics, Royal's Institute of Mental Health Research, University of Ottawa Ottawa Canada 7 Brain and Consciousness Research Centre Taipei Medical University‐Shuang Ho Hospital New Taipei City Taiwan 1 Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Psychiatry University of Genoa Genoa Italy 4 Department of Neurology, Radiology, and Neuroscience Icahn School of Medicine at Mount Sinai New York New York USA 8 Mental Health Centre Zhejiang University School of Medicine Hangzhou Zhejiang China 3 Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Neurology University of Genoa Genoa Italy 6 Centre for Cognition and Brain Disorders Hangzhou Normal University Hangzhou China |
AuthorAffiliation_xml | – name: 8 Mental Health Centre Zhejiang University School of Medicine Hangzhou Zhejiang China – name: 2 IRCCS Ospedale Policlinico San Martino Genoa Italy – name: 1 Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Psychiatry University of Genoa Genoa Italy – name: 3 Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health, Section of Neurology University of Genoa Genoa Italy – name: 5 Brain and Mind Research Institute, Mind Brain Imaging and Neuroethics, Royal's Institute of Mental Health Research, University of Ottawa Ottawa Canada – name: 6 Centre for Cognition and Brain Disorders Hangzhou Normal University Hangzhou China – name: 4 Department of Neurology, Radiology, and Neuroscience Icahn School of Medicine at Mount Sinai New York New York USA – name: 7 Brain and Consciousness Research Centre Taipei Medical University‐Shuang Ho Hospital New Taipei City Taiwan |
Author_xml | – sequence: 1 givenname: Benedetta orcidid: 0000-0002-8201-7193 surname: Conio fullname: Conio, Benedetta organization: IRCCS Ospedale Policlinico San Martino – sequence: 2 givenname: Paola surname: Magioncalda fullname: Magioncalda, Paola email: paola.magioncalda@gmail.com organization: IRCCS Ospedale Policlinico San Martino – sequence: 3 givenname: Matteo surname: Martino fullname: Martino, Matteo organization: IRCCS Ospedale Policlinico San Martino – sequence: 4 givenname: Shankar surname: Tumati fullname: Tumati, Shankar organization: Brain and Mind Research Institute, Mind Brain Imaging and Neuroethics, Royal's Institute of Mental Health Research, University of Ottawa – sequence: 5 givenname: Laura surname: Capobianco fullname: Capobianco, Laura organization: IRCCS Ospedale Policlinico San Martino – sequence: 6 givenname: Andrea surname: Escelsior fullname: Escelsior, Andrea organization: IRCCS Ospedale Policlinico San Martino – sequence: 7 givenname: Giulia surname: Adavastro fullname: Adavastro, Giulia organization: IRCCS Ospedale Policlinico San Martino – sequence: 8 givenname: Daniel surname: Russo fullname: Russo, Daniel organization: IRCCS Ospedale Policlinico San Martino – sequence: 9 givenname: Mario surname: Amore fullname: Amore, Mario organization: IRCCS Ospedale Policlinico San Martino – sequence: 10 givenname: Matilde surname: Inglese fullname: Inglese, Matilde organization: Icahn School of Medicine at Mount Sinai – sequence: 11 givenname: Georg surname: Northoff fullname: Northoff, Georg organization: Zhejiang University School of Medicine |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30367740$$D View this record in MEDLINE/PubMed |
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Keywords | bipolar disorder neuronal variability sensorimotor network resting state fMRI temperament |
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Snippet | Affective temperaments have been described since the early 20th century and may play a central role in psychiatric illnesses, such as bipolar disorder (BD).... |
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SubjectTerms | Adult Affect - physiology Bipolar disorder Brain - physiology Female Frequencies Humans Illnesses Magnetic Resonance Imaging Male Middle Aged Neural Pathways - physiology neuronal variability resting state fMRI sensorimotor network Sensorimotor system Subgroups temperament Temperament - physiology Variability |
Title | Opposing patterns of neuronal variability in the sensorimotor network mediate cyclothymic and depressive temperaments |
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