Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder

Shin Teng, Chia-Feng Lu, Po-Shan Wang, Cheng-Ta Li, Pei-Chi Tu, Chih I. Hung, Tung-Ping Su, Yu-Te Wu

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Bipolar disorder is characterized by internally affective fluctuations. The abnormality of inherently mental state can be assessed using resting-state fMRI data without producing task-induced biases. In this study, we hypothesized that the resting-state connectivity related to the frontal, striatal, and thalamic regions, which were associated with mood regulations and cognitive functions, can be altered for bipolar disorder. We used the Pearson's correlation coefficients to estimate functional connectivity followed by the hierarchical modular analysis to categorize the resting-state functional regions of interest (ROIs). The selected functional connectivities associated with the striatal-thalamic circuit and default mode network (DMN) were compared between bipolar patients and healthy controls. Significantly decreased connectivity in the striatalthalamic circuit and between the striatal regions and the middle and posterior cingulate cortex was observed in the bipolar patients. We also observed that the bipolar patients exhibited significantly increased connectivity between the thalamic regions and the parahippocampus. No significant changes of connectivity related to the frontal regions in the DMN were observed. The changed resting-state connectivity related to the striatal-thalamic circuit might be an inherent basis for the altered emotional and cognitive processing in the bipolar patients. © 2014 Teng et al.
Original languageEnglish
JournalPLoS One
Volume9
Issue number5
DOIs
Publication statusPublished - 2014
Externally publishedYes

Fingerprint

Corpus Striatum
Bipolar Disorder
Networks (circuits)
Gyrus Cinguli
emotions
cognition
Cognition
cortex
Magnetic Resonance Imaging
Processing

Keywords

  • adult
  • anterior cingulate
  • article
  • bipolar disorder
  • brain region
  • clinical article
  • cognition
  • controlled study
  • corpus striatum
  • default mode network
  • female
  • frontal cortex
  • functional anatomy
  • hippocampus
  • human
  • male
  • neuromodulation
  • neuropathology
  • posterior cingulate
  • thalamus
  • algorithm
  • biological model
  • cingulate gyrus
  • connectome
  • image processing
  • middle aged
  • nerve cell network
  • nerve tract
  • nuclear magnetic resonance imaging
  • pathophysiology
  • procedures
  • radiography
  • rest
  • Adult
  • Algorithms
  • Bipolar Disorder
  • Connectome
  • Corpus Striatum
  • Female
  • Gyrus Cinguli
  • Humans
  • Image Processing, Computer-Assisted
  • Magnetic Resonance Imaging
  • Male
  • Middle Aged
  • Models, Neurological
  • Nerve Net
  • Neural Pathways
  • Rest
  • Thalamus

Cite this

Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder. / Teng, Shin; Lu, Chia-Feng; Wang, Po-Shan; Li, Cheng-Ta; Tu, Pei-Chi; Hung, Chih I.; Su, Tung-Ping; Wu, Yu-Te.

In: PLoS One, Vol. 9, No. 5, 2014.

Research output: Contribution to journalArticle

Teng, S, Lu, C-F, Wang, P-S, Li, C-T, Tu, P-C, Hung, CI, Su, T-P & Wu, Y-T 2014, 'Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder', PLoS One, vol. 9, no. 5. https://doi.org/10.1371/journal.pone.0096422
Teng, Shin ; Lu, Chia-Feng ; Wang, Po-Shan ; Li, Cheng-Ta ; Tu, Pei-Chi ; Hung, Chih I. ; Su, Tung-Ping ; Wu, Yu-Te. / Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder. In: PLoS One. 2014 ; Vol. 9, No. 5.
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title = "Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder",
abstract = "Bipolar disorder is characterized by internally affective fluctuations. The abnormality of inherently mental state can be assessed using resting-state fMRI data without producing task-induced biases. In this study, we hypothesized that the resting-state connectivity related to the frontal, striatal, and thalamic regions, which were associated with mood regulations and cognitive functions, can be altered for bipolar disorder. We used the Pearson's correlation coefficients to estimate functional connectivity followed by the hierarchical modular analysis to categorize the resting-state functional regions of interest (ROIs). The selected functional connectivities associated with the striatal-thalamic circuit and default mode network (DMN) were compared between bipolar patients and healthy controls. Significantly decreased connectivity in the striatalthalamic circuit and between the striatal regions and the middle and posterior cingulate cortex was observed in the bipolar patients. We also observed that the bipolar patients exhibited significantly increased connectivity between the thalamic regions and the parahippocampus. No significant changes of connectivity related to the frontal regions in the DMN were observed. The changed resting-state connectivity related to the striatal-thalamic circuit might be an inherent basis for the altered emotional and cognitive processing in the bipolar patients. {\circledC} 2014 Teng et al.",
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author = "Shin Teng and Chia-Feng Lu and Po-Shan Wang and Cheng-Ta Li and Pei-Chi Tu and Hung, {Chih I.} and Tung-Ping Su and Yu-Te Wu",
note = "被引用次數:1 Export Date: 31 March 2016 CODEN: POLNC 參考文獻: Merikangas, K.R., Akiskal, H.S., Angst, J., Greenberg, P.E., Hirschfeld, R.M.A., Petukhova, M., Kessler, R.C., Lifetime and 12-month prevalence of bipolar spectrum disorder in the national comorbidity survey replication (2007) Archives of General Psychiatry, 64 (5), pp. 543-552. , http://archpsyc.ama-assn.org/cgi/reprint/64/5/543.pdf, DOI 10.1001/archpsyc.64.5.543; Murray, C.J.L., Lopez, A.D., Global mortality, disability, and the contribution of risk factors: Global burden of disease study (1997) Lancet, 349 (9063), pp. 1436-1442. , DOI 10.1016/S0140-6736(96)07495-8; Bora, E., Yucel, M., Pantelis, C., Cognitive endophenotypes of bipolar disorder: A meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives (2009) Journal of Affective Disorders, 113, pp. 1-20; Minassian, A., Paulus, M.P., Perry, W., Increased sensitivity to error during decision-making in bipolar disorder patients with acute mania (2004) Journal of Affective Disorders, 82 (2), pp. 203-208. , DOI 10.1016/j.jad.2003.11.010, PII S0165032703003148; Clark, L., Iversen, S.D., Goodwin, G.M., Sustained attention deficit in bipolar disorder (2002) British Journal of Psychiatry, 180 (APR.), pp. 313-319. , DOI 10.1192/bjp.180.4.313; Zubieta, J.-K., Huguelet, P., O'Neil, R.L., Giordani, B.J., Cognitive function in euthymic Bipolar I Disorder (2001) Psychiatry Research, 102 (1), pp. 9-20. , DOI 10.1016/S0165-1781(01)00242-6, PII S0165178101002426; Metzger, C.D., Van Der Werf, Y.D., Walter, M., Functional mapping of thalamic nuclei and their integration into cortico-striatal-thalamo-cortical loops via ultra-high resolution imaging-from animal anatomy to in vivo imaging in humans (2013) Frontiers in Neuroscience, 7; Haber, S.N., Calzavara, R., The cortico-basal ganglia integrative network: The role of the thalamus (2009) Brain Research Bulletin, 78, pp. 69-74; Price, J.L., Drevets, W.C., Neural circuits underlying the pathophysiology of mood disorders (2012) Trends in Cognitive Sciences, 16, pp. 61-71; Haber, S.N., Kim, K.-S., Mailly, P., Calzavara, R., Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning (2006) Journal of Neuroscience, 26 (32), pp. 8368-8376. , http://www.jneurosci.org/cgi/reprint/26/32/8368.pdf, DOI 10.1523/JNEUROSCI.0271-06.2006; Calzavara, R., Mailly, P., Haber, S.N., Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: An anatomical substrate for cognition to action (2007) European Journal of Neuroscience, 26 (7), pp. 2005-2024. , DOI 10.1111/j.1460-9568.2007.05825.x; Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function (2001) Proceedings of the National Academy of Sciences of the United States of America, 98 (2), pp. 676-682. , DOI 10.1073/pnas.98.2.676; Cerullo, M.A., Adler, C.M., Delbello, M.P., Strakowski, S.M., The functional neuroanatomy of bipolar disorder (2009) International Review of Psychiatry, 21, pp. 314-322; Li, C.-T., Hsieh, J.-C., Wang, S.-J., Yang, B.-H., Bai, Y.-M., Differential relations between fronto-limbic metabolism and executive function in patients with remitted bipolar I and bipolar II disorder (2012) Bipolar Disorders, 14, pp. 831-842; 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language = "English",
volume = "9",
journal = "PLoS One",
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TY - JOUR

T1 - Altered resting-state functional connectivity of striatal-thalamic circuit in bipolar disorder

AU - Teng, Shin

AU - Lu, Chia-Feng

AU - Wang, Po-Shan

AU - Li, Cheng-Ta

AU - Tu, Pei-Chi

AU - Hung, Chih I.

AU - Su, Tung-Ping

AU - Wu, Yu-Te

N1 - 被引用次數:1 Export Date: 31 March 2016 CODEN: POLNC 參考文獻: Merikangas, K.R., Akiskal, H.S., Angst, J., Greenberg, P.E., Hirschfeld, R.M.A., Petukhova, M., Kessler, R.C., Lifetime and 12-month prevalence of bipolar spectrum disorder in the national comorbidity survey replication (2007) Archives of General Psychiatry, 64 (5), pp. 543-552. , http://archpsyc.ama-assn.org/cgi/reprint/64/5/543.pdf, DOI 10.1001/archpsyc.64.5.543; Murray, C.J.L., Lopez, A.D., Global mortality, disability, and the contribution of risk factors: Global burden of disease study (1997) Lancet, 349 (9063), pp. 1436-1442. , DOI 10.1016/S0140-6736(96)07495-8; Bora, E., Yucel, M., Pantelis, C., Cognitive endophenotypes of bipolar disorder: A meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives (2009) Journal of Affective Disorders, 113, pp. 1-20; Minassian, A., Paulus, M.P., Perry, W., Increased sensitivity to error during decision-making in bipolar disorder patients with acute mania (2004) Journal of Affective Disorders, 82 (2), pp. 203-208. , DOI 10.1016/j.jad.2003.11.010, PII S0165032703003148; Clark, L., Iversen, S.D., Goodwin, G.M., Sustained attention deficit in bipolar disorder (2002) British Journal of Psychiatry, 180 (APR.), pp. 313-319. , DOI 10.1192/bjp.180.4.313; Zubieta, J.-K., Huguelet, P., O'Neil, R.L., Giordani, B.J., Cognitive function in euthymic Bipolar I Disorder (2001) Psychiatry Research, 102 (1), pp. 9-20. , DOI 10.1016/S0165-1781(01)00242-6, PII S0165178101002426; Metzger, C.D., Van Der Werf, Y.D., Walter, M., Functional mapping of thalamic nuclei and their integration into cortico-striatal-thalamo-cortical loops via ultra-high resolution imaging-from animal anatomy to in vivo imaging in humans (2013) Frontiers in Neuroscience, 7; Haber, S.N., Calzavara, R., The cortico-basal ganglia integrative network: The role of the thalamus (2009) Brain Research Bulletin, 78, pp. 69-74; Price, J.L., Drevets, W.C., Neural circuits underlying the pathophysiology of mood disorders (2012) Trends in Cognitive Sciences, 16, pp. 61-71; Haber, S.N., Kim, K.-S., Mailly, P., Calzavara, R., Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning (2006) Journal of Neuroscience, 26 (32), pp. 8368-8376. , http://www.jneurosci.org/cgi/reprint/26/32/8368.pdf, DOI 10.1523/JNEUROSCI.0271-06.2006; Calzavara, R., Mailly, P., Haber, S.N., Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: An anatomical substrate for cognition to action (2007) European Journal of Neuroscience, 26 (7), pp. 2005-2024. , DOI 10.1111/j.1460-9568.2007.05825.x; Raichle, M.E., MacLeod, A.M., Snyder, A.Z., Powers, W.J., Gusnard, D.A., Shulman, G.L., A default mode of brain function (2001) Proceedings of the National Academy of Sciences of the United States of America, 98 (2), pp. 676-682. , DOI 10.1073/pnas.98.2.676; Cerullo, M.A., Adler, C.M., Delbello, M.P., Strakowski, S.M., The functional neuroanatomy of bipolar disorder (2009) International Review of Psychiatry, 21, pp. 314-322; Li, C.-T., Hsieh, J.-C., Wang, S.-J., Yang, B.-H., Bai, Y.-M., Differential relations between fronto-limbic metabolism and executive function in patients with remitted bipolar I and bipolar II disorder (2012) Bipolar Disorders, 14, pp. 831-842; Hwang, J., In, K.L., Dager, S.R., Friedman, S.D., Jung, S.O., Jun, Y.L., Seog, J.K., Renshaw, P.F., Basal ganglia shape alterations in bipolar disorder (2006) American Journal of Psychiatry, 163 (2), pp. 276-285. , DOI 10.1176/appi.ajp.163.2.276; Lyoo, I.K., Sung, Y.H., Dager, S.R., Friedman, S.D., Lee, J.-Y., Kim, S.J., Kim, N., Renshaw, P.F., Regional cerebral cortical thinning in bipolar disorder (2006) Bipolar Disorders, 8 (1), pp. 65-74. , DOI 10.1111/j.1399-5618.2006.00284.x; Wilke, M., Kowatch, R.A., Delbello, M.P., Mills, N.P., Holland, S.K., Voxel-based morphometry in adolescents with bipolar disorder: First results (2004) Psychiatry Research - Neuroimaging, 131 (1), pp. 57-69. , DOI 10.1016/j.pscychresns.2004.01.004, PII S0925492704000381; Chepenik, L.G., Raffo, M., Hampson, M., Lacadie, C., Wang, F., Functional connectivity between ventral prefrontal cortex and amygdala at low frequency in the resting state in bipolar disorder (2010) Psychiatry Research: Neuroimaging, 182, pp. 207-210; 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PY - 2014

Y1 - 2014

N2 - Bipolar disorder is characterized by internally affective fluctuations. The abnormality of inherently mental state can be assessed using resting-state fMRI data without producing task-induced biases. In this study, we hypothesized that the resting-state connectivity related to the frontal, striatal, and thalamic regions, which were associated with mood regulations and cognitive functions, can be altered for bipolar disorder. We used the Pearson's correlation coefficients to estimate functional connectivity followed by the hierarchical modular analysis to categorize the resting-state functional regions of interest (ROIs). The selected functional connectivities associated with the striatal-thalamic circuit and default mode network (DMN) were compared between bipolar patients and healthy controls. Significantly decreased connectivity in the striatalthalamic circuit and between the striatal regions and the middle and posterior cingulate cortex was observed in the bipolar patients. We also observed that the bipolar patients exhibited significantly increased connectivity between the thalamic regions and the parahippocampus. No significant changes of connectivity related to the frontal regions in the DMN were observed. The changed resting-state connectivity related to the striatal-thalamic circuit might be an inherent basis for the altered emotional and cognitive processing in the bipolar patients. © 2014 Teng et al.

AB - Bipolar disorder is characterized by internally affective fluctuations. The abnormality of inherently mental state can be assessed using resting-state fMRI data without producing task-induced biases. In this study, we hypothesized that the resting-state connectivity related to the frontal, striatal, and thalamic regions, which were associated with mood regulations and cognitive functions, can be altered for bipolar disorder. We used the Pearson's correlation coefficients to estimate functional connectivity followed by the hierarchical modular analysis to categorize the resting-state functional regions of interest (ROIs). The selected functional connectivities associated with the striatal-thalamic circuit and default mode network (DMN) were compared between bipolar patients and healthy controls. Significantly decreased connectivity in the striatalthalamic circuit and between the striatal regions and the middle and posterior cingulate cortex was observed in the bipolar patients. We also observed that the bipolar patients exhibited significantly increased connectivity between the thalamic regions and the parahippocampus. No significant changes of connectivity related to the frontal regions in the DMN were observed. The changed resting-state connectivity related to the striatal-thalamic circuit might be an inherent basis for the altered emotional and cognitive processing in the bipolar patients. © 2014 Teng et al.

KW - adult

KW - anterior cingulate

KW - article

KW - bipolar disorder

KW - brain region

KW - clinical article

KW - cognition

KW - controlled study

KW - corpus striatum

KW - default mode network

KW - female

KW - frontal cortex

KW - functional anatomy

KW - hippocampus

KW - human

KW - male

KW - neuromodulation

KW - neuropathology

KW - posterior cingulate

KW - thalamus

KW - algorithm

KW - biological model

KW - cingulate gyrus

KW - connectome

KW - image processing

KW - middle aged

KW - nerve cell network

KW - nerve tract

KW - nuclear magnetic resonance imaging

KW - pathophysiology

KW - procedures

KW - radiography

KW - rest

KW - Adult

KW - Algorithms

KW - Bipolar Disorder

KW - Connectome

KW - Corpus Striatum

KW - Female

KW - Gyrus Cinguli

KW - Humans

KW - Image Processing, Computer-Assisted

KW - Magnetic Resonance Imaging

KW - Male

KW - Middle Aged

KW - Models, Neurological

KW - Nerve Net

KW - Neural Pathways

KW - Rest

KW - Thalamus

UR - http://www.scopus.com/inward/record.url?eid=2-s2.0-84900424920&partnerID=40&md5=8be16efd1d85c8a3c13f8e8d89fcca62

UR - https://www.scopus.com/results/citedbyresults.uri?sort=plf-f&cite=2-s2.0-84900424920&src=s&imp=t&sid=7698cc64b5f67d098141a9c312be4dd1&sot=cite&sdt=a&sl=0&origin=recordpage&editSaveSearch=&txGid=9961d332dc0e23b4fbbca32339e65883

U2 - 10.1371/journal.pone.0096422

DO - 10.1371/journal.pone.0096422

M3 - Article

VL - 9

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 5

ER -