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 inHuman brain mapping Vol. 40; no. 4; pp. 1344 - 1352
Main Authors Conio, Benedetta, Magioncalda, Paola, Martino, Matteo, Tumati, Shankar, Capobianco, Laura, Escelsior, Andrea, Adavastro, Giulia, Russo, Daniel, Amore, Mario, Inglese, Matilde, Northoff, Georg
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LanguageEnglish
Published Hoboken, USA 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.
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
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Keywords bipolar disorder
neuronal variability
sensorimotor network
resting state fMRI
temperament
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Paola Magioncalda and Matteo Martino contributed equally to this work
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  publication-title: Primary Psychiatry
– ident: e_1_2_8_6_1
  doi: 10.1016/j.jad.2003.10.012
– ident: e_1_2_8_53_1
  doi: 10.1016/j.jad.2014.07.037
– ident: e_1_2_8_32_1
  doi: 10.1371/journal.pone.0077336
– ident: e_1_2_8_42_1
  doi: 10.1097/00005053-192104000-00057
– ident: e_1_2_8_40_1
  doi: 10.1016/j.jad.2014.09.009
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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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Aggregation Database
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StartPage 1344
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
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhbm.24453
https://www.ncbi.nlm.nih.gov/pubmed/30367740
https://www.proquest.com/docview/2176291254
https://www.proquest.com/docview/2126916180
https://pubmed.ncbi.nlm.nih.gov/PMC6865768
Volume 40
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