Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures

Paola Magioncalda, Matteo Martino, Benedetta Conio, Andrea Escelsior, Niccolò Piaggio, Andrea Presta, Valentina Marozzi, Giulio Rocchi, Loris Anastasio, Linda Vassallo, Francesca Ferri, Zirui Huang, Luca Roccatagliata, Matteo Pardini, Georg Franz Josef Northoff, Mario Amore

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Introduction: The cortical midline structures seem to be involved in the modulation of different resting state networks, such as the default mode network (DMN) and salience network (SN). Alterations in these systems, in particular in the perigenual anterior cingulate cortex (PACC), seem to play a central role in bipolar disorder (BD). However, the exact role of the PACC, and its functional connections to other midline regions (within and outside DMN) still remains unclear in BD. Methods: We investigated functional connectivity (FC), standard deviation (SD, as a measure of neuronal variability) and their correlation in bipolar patients (n=40) versus healthy controls (n=40), in the PACC and in its connections in different frequency bands (standard: 0.01-0.10 Hz; Slow-5: 0.01-0.027 Hz; Slow-4: 0.027-0.073 Hz). Finally, we studied the correlations between FC alterations and clinical-neuropsychological parameters and we explored whether subgroups of patients in different phases of the illness present different patterns of FC abnormalities. Results: We found in BD decreased FC (especially in Slow-5) from the PACC to other regions located predominantly in the posterior DMN (such as the posterior cingulate cortex (PCC) and inferior temporal gyrus) and in the SN (such as the supragenual anterior cingulate cortex and ventrolateral prefrontal cortex). Second, we found in BD a decoupling between PACC-based FC and variability in the various target regions (without alteration in variability itself). Finally, in our subgroups explorative analysis, we found a decrease in FC between the PACC and supragenual ACC (in depressive phase) and between the PACC and PCC (in manic phase). Conclusions: These findings suggest that in BD the communication, that is, information transfer, between the different cortical midline regions within the cingulate gyrus does not seem to work properly. This may result in dysbalance between different resting state networks like the DMN and SN. A deficit in the anterior DMN-SN connectivity could lead to an abnormal shifting toward the DMN, while a deficit in the anterior DMN-posterior DMN connectivity could lead to an abnormal shifting toward the SN, resulting in excessive focusing on internal contents and reduced transition from idea to action or in excessive focusing on external contents and increased transition from idea to action, respectively, which could represent central dimensions of depression and mania. If confirmed, they could represent diagnostic markers in BD. © 2014 Wiley Periodicals, Inc.
Original languageEnglish
Pages (from-to)666-682
Number of pages17
JournalHuman Brain Mapping
Volume36
Issue number2
DOIs
Publication statusPublished - 2015

Fingerprint

Gyrus Cinguli
Bipolar Disorder
Temporal Lobe
Prefrontal Cortex
Communication
Depression

Keywords

  • Bipolar disorder
  • Default mode network
  • Functional connectivity
  • Neuronal variability
  • Perigenual anterior cingulate cortex
  • Resting state fMRI
  • adult
  • anterior cingulate
  • Article
  • bipolar disorder
  • brain function
  • brain structure
  • brain tissue
  • cingulate gyrus
  • comparative study
  • controlled study
  • depression
  • female
  • functional connectivity
  • functional magnetic resonance imaging
  • human
  • inferior temporal gyrus
  • major clinical study
  • male
  • mania
  • mental patient
  • nerve cell
  • nuclear magnetic resonance scanner
  • posterior cingulate
  • prefrontal cortex
  • priority journal
  • resting state network
  • Young Mania Rating Scale
  • adolescent
  • brain
  • brain mapping
  • middle aged
  • nerve tract
  • neuropsychological test
  • nuclear magnetic resonance imaging
  • pathophysiology
  • rest
  • young adult
  • Adolescent
  • Adult
  • Bipolar Disorder
  • Brain
  • Brain Mapping
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Neural Pathways
  • Neuropsychological Tests
  • Rest
  • Young Adult

Cite this

Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures. / Magioncalda, Paola; Martino, Matteo; Conio, Benedetta; Escelsior, Andrea; Piaggio, Niccolò; Presta, Andrea; Marozzi, Valentina; Rocchi, Giulio; Anastasio, Loris; Vassallo, Linda; Ferri, Francesca; Huang, Zirui; Roccatagliata, Luca; Pardini, Matteo; Northoff, Georg Franz Josef; Amore, Mario.

In: Human Brain Mapping, Vol. 36, No. 2, 2015, p. 666-682.

Research output: Contribution to journalArticle

Magioncalda, P, Martino, M, Conio, B, Escelsior, A, Piaggio, N, Presta, A, Marozzi, V, Rocchi, G, Anastasio, L, Vassallo, L, Ferri, F, Huang, Z, Roccatagliata, L, Pardini, M, Northoff, GFJ & Amore, M 2015, 'Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures', Human Brain Mapping, vol. 36, no. 2, pp. 666-682. https://doi.org/10.1002/hbm.22655
Magioncalda, Paola ; Martino, Matteo ; Conio, Benedetta ; Escelsior, Andrea ; Piaggio, Niccolò ; Presta, Andrea ; Marozzi, Valentina ; Rocchi, Giulio ; Anastasio, Loris ; Vassallo, Linda ; Ferri, Francesca ; Huang, Zirui ; Roccatagliata, Luca ; Pardini, Matteo ; Northoff, Georg Franz Josef ; Amore, Mario. / Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures. In: Human Brain Mapping. 2015 ; Vol. 36, No. 2. pp. 666-682.
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title = "Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures",
abstract = "Introduction: The cortical midline structures seem to be involved in the modulation of different resting state networks, such as the default mode network (DMN) and salience network (SN). Alterations in these systems, in particular in the perigenual anterior cingulate cortex (PACC), seem to play a central role in bipolar disorder (BD). However, the exact role of the PACC, and its functional connections to other midline regions (within and outside DMN) still remains unclear in BD. Methods: We investigated functional connectivity (FC), standard deviation (SD, as a measure of neuronal variability) and their correlation in bipolar patients (n=40) versus healthy controls (n=40), in the PACC and in its connections in different frequency bands (standard: 0.01-0.10 Hz; Slow-5: 0.01-0.027 Hz; Slow-4: 0.027-0.073 Hz). Finally, we studied the correlations between FC alterations and clinical-neuropsychological parameters and we explored whether subgroups of patients in different phases of the illness present different patterns of FC abnormalities. Results: We found in BD decreased FC (especially in Slow-5) from the PACC to other regions located predominantly in the posterior DMN (such as the posterior cingulate cortex (PCC) and inferior temporal gyrus) and in the SN (such as the supragenual anterior cingulate cortex and ventrolateral prefrontal cortex). Second, we found in BD a decoupling between PACC-based FC and variability in the various target regions (without alteration in variability itself). Finally, in our subgroups explorative analysis, we found a decrease in FC between the PACC and supragenual ACC (in depressive phase) and between the PACC and PCC (in manic phase). Conclusions: These findings suggest that in BD the communication, that is, information transfer, between the different cortical midline regions within the cingulate gyrus does not seem to work properly. This may result in dysbalance between different resting state networks like the DMN and SN. A deficit in the anterior DMN-SN connectivity could lead to an abnormal shifting toward the DMN, while a deficit in the anterior DMN-posterior DMN connectivity could lead to an abnormal shifting toward the SN, resulting in excessive focusing on internal contents and reduced transition from idea to action or in excessive focusing on external contents and increased transition from idea to action, respectively, which could represent central dimensions of depression and mania. If confirmed, they could represent diagnostic markers in BD. {\circledC} 2014 Wiley Periodicals, Inc.",
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author = "Paola Magioncalda and Matteo Martino and Benedetta Conio and Andrea Escelsior and Niccol{\`o} Piaggio and Andrea Presta and Valentina Marozzi and Giulio Rocchi and Loris Anastasio and Linda Vassallo and Francesca Ferri and Zirui Huang and Luca Roccatagliata and Matteo Pardini and Northoff, {Georg Franz Josef} and Mario Amore",
note = "Cited By :4 Export Date: 11 May 2016 CODEN: HBMAE Correspondence Address: Martino, M.; Ospedale San Martino, Largo Rosanna Benzi n.16, Italy Manufacturers: General Electric References: Akiskal, H.S., The prevalent clinical spectrum of bipolar disorders: beyond DSM-IV (1996) J Clin Psychopharmacol, 16, pp. 4S-14S; (1994) Diagnostic and Statistical Manual for Mental Disorders, , 4th ed. Washington: American Psychiatrich Association; Anand, A., Li, Y., Wang, Y., Lowe, M.J., Dzemidzic, M., Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression (2009) Psychiatry Res, 171, pp. 189-198; Arana, G.W., Rosenbaum, J.F., (2000) Handbook of Psychiatric Drug Therapy, , 4th ed. Philadelphia: Lippincott Williams & Wilkins; Baker, J.T., Holmes, A.J., Masters, G.A., Yeo, B.T., Krienen, F., Buckner, R.L., Ongur, D., Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder (2014) JAMA Psychiatry, 71, pp. 109-118; Baldessarini, R.J., (2013) Chemiotherapy in Psychiatry. Pharmacologic Basis of Treatments of Major Mental Illness, , 3rd ed. New York: Springer; Biswal, B., Yetkin, F.Z., Haughton, V.M., Hyde, J.S., Functional connectivity in the motor cortex of resting human brain using echo-planar MRI (1995) Magn Reson Med, 34, pp. 537-541; Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., The brain's default network: Anatomy, function, and relevance to disease (2008) Ann N Y Acad Sci, 1124, pp. 1-38; Buzsaki, G., Draguhn, A., Neuronal oscillations in cortical networks (2004) Science, 304, pp. 1926-1929; Cassano, G.B., Akiskal, H.S., Musetti, L., Perugi, G., Soriani, A., Mignani, V., Psychopathology, temperament, and past course in primary major depressions. 2. Toward a redefinition of bipolarity with a new semistructured interview for depression (1989) Psychopathology, 22, pp. 278-288; Chai, X.J., Whitfield-Gabrieli, S., Shinn, A.K., Gabrieli, J.D., Nieto Castanon, A., McCarthy, J.M., Cohen, B.M., Ongur, D., Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia (2011) Neuropsychopharmacology, 36, pp. 2009-2017; Christoff, K., Gordon, A.M., Smallwood, J., Smith, R., Schooler, J.W., Experience sampling during fMRI reveals default network and executive system contributions to mind wandering (2009) Proc Natl Acad Sci USA, 106, pp. 8719-8724; Conners, C.K., Epstein, J.N., Angold, A., Klaric, J., Continuous performance test performance in a normative epidemiological sample (2003) J Abnorm Child Psychol, 31, pp. 555-562; Cox, R.W., AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages (1996) Comput Biomed Res, 29, pp. 162-173; Davidson, R.J., Affective style, psychopathology, and resilience: Brain mechanisms and plasticity (2000) Am Psychol, 55, pp. 1196-1214; 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doi = "10.1002/hbm.22655",
language = "English",
volume = "36",
pages = "666--682",
journal = "Human Brain Mapping",
issn = "1065-9471",
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}

TY - JOUR

T1 - Functional connectivity and neuronal variability of resting state activity in bipolar disorder-reduction and decoupling in anterior cortical midline structures

AU - Magioncalda, Paola

AU - Martino, Matteo

AU - Conio, Benedetta

AU - Escelsior, Andrea

AU - Piaggio, Niccolò

AU - Presta, Andrea

AU - Marozzi, Valentina

AU - Rocchi, Giulio

AU - Anastasio, Loris

AU - Vassallo, Linda

AU - Ferri, Francesca

AU - Huang, Zirui

AU - Roccatagliata, Luca

AU - Pardini, Matteo

AU - Northoff, Georg Franz Josef

AU - Amore, Mario

N1 - Cited By :4 Export Date: 11 May 2016 CODEN: HBMAE Correspondence Address: Martino, M.; Ospedale San Martino, Largo Rosanna Benzi n.16, Italy Manufacturers: General Electric References: Akiskal, H.S., The prevalent clinical spectrum of bipolar disorders: beyond DSM-IV (1996) J Clin Psychopharmacol, 16, pp. 4S-14S; (1994) Diagnostic and Statistical Manual for Mental Disorders, , 4th ed. Washington: American Psychiatrich Association; Anand, A., Li, Y., Wang, Y., Lowe, M.J., Dzemidzic, M., Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression (2009) Psychiatry Res, 171, pp. 189-198; Arana, G.W., Rosenbaum, J.F., (2000) Handbook of Psychiatric Drug Therapy, , 4th ed. Philadelphia: Lippincott Williams & Wilkins; Baker, J.T., Holmes, A.J., Masters, G.A., Yeo, B.T., Krienen, F., Buckner, R.L., Ongur, D., Disruption of cortical association networks in schizophrenia and psychotic bipolar disorder (2014) JAMA Psychiatry, 71, pp. 109-118; Baldessarini, R.J., (2013) Chemiotherapy in Psychiatry. Pharmacologic Basis of Treatments of Major Mental Illness, , 3rd ed. New York: Springer; Biswal, B., Yetkin, F.Z., Haughton, V.M., Hyde, J.S., Functional connectivity in the motor cortex of resting human brain using echo-planar MRI (1995) Magn Reson Med, 34, pp. 537-541; Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L., The brain's default network: Anatomy, function, and relevance to disease (2008) Ann N Y Acad Sci, 1124, pp. 1-38; Buzsaki, G., Draguhn, A., Neuronal oscillations in cortical networks (2004) Science, 304, pp. 1926-1929; Cassano, G.B., Akiskal, H.S., Musetti, L., Perugi, G., Soriani, A., Mignani, V., Psychopathology, temperament, and past course in primary major depressions. 2. Toward a redefinition of bipolarity with a new semistructured interview for depression (1989) Psychopathology, 22, pp. 278-288; Chai, X.J., Whitfield-Gabrieli, S., Shinn, A.K., Gabrieli, J.D., Nieto Castanon, A., McCarthy, J.M., Cohen, B.M., Ongur, D., Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia (2011) Neuropsychopharmacology, 36, pp. 2009-2017; Christoff, K., Gordon, A.M., Smallwood, J., Smith, R., Schooler, J.W., Experience sampling during fMRI reveals default network and executive system contributions to mind wandering (2009) Proc Natl Acad Sci USA, 106, pp. 8719-8724; Conners, C.K., Epstein, J.N., Angold, A., Klaric, J., Continuous performance test performance in a normative epidemiological sample (2003) J Abnorm Child Psychol, 31, pp. 555-562; Cox, R.W., AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages (1996) Comput Biomed Res, 29, pp. 162-173; Davidson, R.J., Affective style, psychopathology, and resilience: Brain mechanisms and plasticity (2000) Am Psychol, 55, pp. 1196-1214; Davis, J.M., Chen, N., Dose response and dose equivalence of antipsychotics (2004) J Clin Psychopharmacol, 24, pp. 192-208; Di, X., Kim, E.H., Huang, C.C., Tsai, S.J., Lin, C.P., Biswal, B.B., The influence of the amplitude of low-frequency fluctuations on resting-state functional connectivity (2013) Front Hum Neurosci, 7, p. 118; Duncan, N.W., Wiebking, C., Northoff, G., Associations of regional GABA and glutamate with intrinsic and extrinsic neural activity in humans-A review of multimodal imaging studies (2014) Neurosci Biobehav Rev, 47 C, pp. 36-52; Fingelkurts, A.A., Kivisaari, R., Pekkonen, E., Ilmoniemi, R.J., Kahkonen, S., Local and remote functional connectivity of neocortex under the inhibition influence (2004) Neuroimage, 22, pp. 1390-1406; First, M.B., Spitzer, R.L., Gibbon, M., Williams, J.B.W., Benjamin, L., (1994) Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II), Version 2.0, , New York: Biometrics Research Department, New York State Psychiatric Institute; 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PY - 2015

Y1 - 2015

N2 - Introduction: The cortical midline structures seem to be involved in the modulation of different resting state networks, such as the default mode network (DMN) and salience network (SN). Alterations in these systems, in particular in the perigenual anterior cingulate cortex (PACC), seem to play a central role in bipolar disorder (BD). However, the exact role of the PACC, and its functional connections to other midline regions (within and outside DMN) still remains unclear in BD. Methods: We investigated functional connectivity (FC), standard deviation (SD, as a measure of neuronal variability) and their correlation in bipolar patients (n=40) versus healthy controls (n=40), in the PACC and in its connections in different frequency bands (standard: 0.01-0.10 Hz; Slow-5: 0.01-0.027 Hz; Slow-4: 0.027-0.073 Hz). Finally, we studied the correlations between FC alterations and clinical-neuropsychological parameters and we explored whether subgroups of patients in different phases of the illness present different patterns of FC abnormalities. Results: We found in BD decreased FC (especially in Slow-5) from the PACC to other regions located predominantly in the posterior DMN (such as the posterior cingulate cortex (PCC) and inferior temporal gyrus) and in the SN (such as the supragenual anterior cingulate cortex and ventrolateral prefrontal cortex). Second, we found in BD a decoupling between PACC-based FC and variability in the various target regions (without alteration in variability itself). Finally, in our subgroups explorative analysis, we found a decrease in FC between the PACC and supragenual ACC (in depressive phase) and between the PACC and PCC (in manic phase). Conclusions: These findings suggest that in BD the communication, that is, information transfer, between the different cortical midline regions within the cingulate gyrus does not seem to work properly. This may result in dysbalance between different resting state networks like the DMN and SN. A deficit in the anterior DMN-SN connectivity could lead to an abnormal shifting toward the DMN, while a deficit in the anterior DMN-posterior DMN connectivity could lead to an abnormal shifting toward the SN, resulting in excessive focusing on internal contents and reduced transition from idea to action or in excessive focusing on external contents and increased transition from idea to action, respectively, which could represent central dimensions of depression and mania. If confirmed, they could represent diagnostic markers in BD. © 2014 Wiley Periodicals, Inc.

AB - Introduction: The cortical midline structures seem to be involved in the modulation of different resting state networks, such as the default mode network (DMN) and salience network (SN). Alterations in these systems, in particular in the perigenual anterior cingulate cortex (PACC), seem to play a central role in bipolar disorder (BD). However, the exact role of the PACC, and its functional connections to other midline regions (within and outside DMN) still remains unclear in BD. Methods: We investigated functional connectivity (FC), standard deviation (SD, as a measure of neuronal variability) and their correlation in bipolar patients (n=40) versus healthy controls (n=40), in the PACC and in its connections in different frequency bands (standard: 0.01-0.10 Hz; Slow-5: 0.01-0.027 Hz; Slow-4: 0.027-0.073 Hz). Finally, we studied the correlations between FC alterations and clinical-neuropsychological parameters and we explored whether subgroups of patients in different phases of the illness present different patterns of FC abnormalities. Results: We found in BD decreased FC (especially in Slow-5) from the PACC to other regions located predominantly in the posterior DMN (such as the posterior cingulate cortex (PCC) and inferior temporal gyrus) and in the SN (such as the supragenual anterior cingulate cortex and ventrolateral prefrontal cortex). Second, we found in BD a decoupling between PACC-based FC and variability in the various target regions (without alteration in variability itself). Finally, in our subgroups explorative analysis, we found a decrease in FC between the PACC and supragenual ACC (in depressive phase) and between the PACC and PCC (in manic phase). Conclusions: These findings suggest that in BD the communication, that is, information transfer, between the different cortical midline regions within the cingulate gyrus does not seem to work properly. This may result in dysbalance between different resting state networks like the DMN and SN. A deficit in the anterior DMN-SN connectivity could lead to an abnormal shifting toward the DMN, while a deficit in the anterior DMN-posterior DMN connectivity could lead to an abnormal shifting toward the SN, resulting in excessive focusing on internal contents and reduced transition from idea to action or in excessive focusing on external contents and increased transition from idea to action, respectively, which could represent central dimensions of depression and mania. If confirmed, they could represent diagnostic markers in BD. © 2014 Wiley Periodicals, Inc.

KW - Bipolar disorder

KW - Default mode network

KW - Functional connectivity

KW - Neuronal variability

KW - Perigenual anterior cingulate cortex

KW - Resting state fMRI

KW - adult

KW - anterior cingulate

KW - Article

KW - bipolar disorder

KW - brain function

KW - brain structure

KW - brain tissue

KW - cingulate gyrus

KW - comparative study

KW - controlled study

KW - depression

KW - female

KW - functional connectivity

KW - functional magnetic resonance imaging

KW - human

KW - inferior temporal gyrus

KW - major clinical study

KW - male

KW - mania

KW - mental patient

KW - nerve cell

KW - nuclear magnetic resonance scanner

KW - posterior cingulate

KW - prefrontal cortex

KW - priority journal

KW - resting state network

KW - Young Mania Rating Scale

KW - adolescent

KW - brain

KW - brain mapping

KW - middle aged

KW - nerve tract

KW - neuropsychological test

KW - nuclear magnetic resonance imaging

KW - pathophysiology

KW - rest

KW - young adult

KW - Adolescent

KW - Adult

KW - Bipolar Disorder

KW - Brain

KW - Brain Mapping

KW - Female

KW - Humans

KW - Magnetic Resonance Imaging

KW - Male

KW - Middle Aged

KW - Neural Pathways

KW - Neuropsychological Tests

KW - Rest

KW - Young Adult

U2 - 10.1002/hbm.22655

DO - 10.1002/hbm.22655

M3 - Article

C2 - 25307723

VL - 36

SP - 666

EP - 682

JO - Human Brain Mapping

JF - Human Brain Mapping

SN - 1065-9471

IS - 2

ER -