Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T00:48:26.292Z Has data issue: false hasContentIssue false
  • English
  • Français

Covariation between spontaneous neural activity in the insula and affective temperaments is related to sleep disturbance in individuals with major depressive disorder

Published online by Cambridge University Press:  16 December 2019

Huawang Wu ,
Yingjun Zheng ,
Qianqian Zhan ,
Jie Dong ,
Hongjun Peng ,
Jinguo Zhai ,
Jingping Zhao ,
Shenglin She  and
Chao Wu Open the ORCID record for Chao Wu [Opens in a new window]
Huawang Wu
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Yingjun Zheng
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Qianqian Zhan
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Jie Dong
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Hongjun Peng
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Jinguo Zhai
Affiliation:
School of Mental Health, Jining Medical University, Jining272067, China
Jingping Zhao
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Shenglin She*
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou510370, China
Chao Wu*
Affiliation:
School of Nursing, Peking University Health Science Center, Beijing100191, China
*
Author for correspondence: Shenglin She, E-mail: [email protected]; Chao Wu, E-mail: [email protected]
Author for correspondence: Shenglin She, E-mail: [email protected]; Chao Wu, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Affective temperaments have been considered antecedents of major depressive disorder (MDD). However, little is known about how the covariation between alterations in brain activity and distinct affective temperaments work collaboratively to contribute to MDD. Here, we focus on the insular cortex, a critical hub for the integration of subjective feelings, emotions, and motivations, to examine the neural correlates of affective temperaments and their relationship to depressive symptom dimensions.

Methods

Twenty-nine medication-free patients with MDD and 58 healthy controls underwent magnetic resonance imaging scanning and completed the Temperament Evaluation of Memphis, Pisa, Paris and San Diego (TEMPS). Patients also received assessments of the Hamilton Depression Rating Scale (HDRS). We used multivariate analyses of partial least squares regression and partial correlation analyses to explore the associations among the insular activity, affective temperaments, and depressive symptom dimensions.

Results

A profile (linear combination) of increased fractional amplitude of low-frequency fluctuations (fALFF) of the anterior insular subregions (left dorsal agranular–dysgranular insula and right ventral agranuar insula) was positively associated with an affective-temperament (depressive, irritable, anxious, and less hyperthymic) profile. The covariation between the insula-fALFF profile and the affective-temperament profile was significantly correlated with the sleep disturbance dimension (especially the middle and late insomnia scores) in the medication-free MDD patients.

Conclusions

The resting-state spontaneous activity of the anterior insula and affective temperaments collaboratively contribute to sleep disturbances in medication-free MDD patients. The approach used in this study provides a practical way to explore the relationship of multivariate measures in investigating the etiology of mental disorders.

Keywords

Affective temperamentsfractional amplitude of low-frequency fluctuationsinsulamajor depressive disorderpartial least squares
Type
Original Article
Information
Psychological Medicine , Volume 51 , Issue 5 , April 2021 , pp. 731 - 740
Check for updates
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Abdi, H. (2010). Partial least squares regression and projection on latent structure regression (PLS regression). Wiley Interdisciplinary Reviews Computational Statistics, 2, 97–106.CrossRefGoogle Scholar
Akiskal, H. S., & Akiskal, K. K. (2005a). TEMPS: Temperament Evaluation of Memphis, Pisa, Paris and San Diego. Journal of Affective Disorder, 85, 1–2.CrossRefGoogle Scholar
Akiskal, H. S., Akiskal, K. K., Haykal, R. F., Manning, J. S., & Connor, P. D. (2005). TEMPS-A: Progress towards validation of a self-rated clinical version of the temperament evaluation of the Memphis, Pisa, Paris, and San Diego autoquestionnaire. Journal of Affective Disorders, 85, 3–16.CrossRefGoogle ScholarPubMed
Akiskal, K. K., & Akiskal, H. S. (2005b). The theoretical underpinnings of affective temperaments: Implications for evolutionary foundations of bipolar disorder and human nature. Journal of Affective Disorders, 85, 231–239.CrossRefGoogle Scholar
Bechara, A. (2005). Decision making, impulse control and loss of willpower to resist drugs: A neurocognitive perspective. Nature Neuroscience, 8, 1458–1463.CrossRefGoogle ScholarPubMed
Cheng, W., Rolls, E. T., Ruan, H., & Feng, J. (2018). Functional connectivities in the brain that mediate the association between depressive problems and sleep quality. JAMA Psychiatry, 75, 1052–1061.CrossRefGoogle ScholarPubMed
Chouchou, F., Mauguiere, F., Vallayer, O., Catenoix, H., Isnard, J., Montavont, A., … Mazzola, L. (2019). How the insula speaks to the heart: Cardiac responses to insular stimulation in humans. Human Brain Mapping, 40, 2611–2622.CrossRefGoogle ScholarPubMed
Cole, M. W., Yarkoni, T., Repovs, G., Anticevic, A., & Braver, T. S. (2012). Global connectivity of prefrontal cortex predicts cognitive control and intelligence. The Journal of Neuroscience, 32, 8988–8999.CrossRefGoogle ScholarPubMed
Craig, A. D. (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews: Neuroscience, 10, 59–70.CrossRefGoogle Scholar
Craig, A. D. (2010). The sentient self. Brain Structure & Function, 214, 563–577.CrossRefGoogle ScholarPubMed
Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A., & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189–195.CrossRefGoogle ScholarPubMed
Damasio, A. (2003). Feelings of emotion and the self. Annals of the New York Academy of Sciences, 1001, 253–261.CrossRefGoogle ScholarPubMed
De Aguiar Ferreira, A., Vasconcelos, A. G., Neves, F. S., & Correa, H. (2014). Affective temperaments and antidepressant response in the clinical management of mood disorders. Journal of Affective Disorders, 155, 138–141.CrossRefGoogle ScholarPubMed
Diener, C., Kuehner, C., Brusniak, W., Ubl, B., Wessa, M., & Flor, H. (2012). A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. Neuroimage, 61, 677–685.CrossRefGoogle ScholarPubMed
Dolan, R. J. (2002). Emotion, cognition, and behavior. Science, 298, 1191–1194.CrossRefGoogle Scholar
Elias, L. R., Kohler, C. A., Stubbs, B., Maciel, B. R., Cavalcante, L. M., Vale, A. M., … Carvalho, A. F. (2017). Measuring affective temperaments: A systematic review of validation studies of the Temperament Evaluation in Memphis Pisa and San Diego (TEMPS) instruments. Journal of Affective Disorders, 212, 25–37.CrossRefGoogle Scholar
Fan, L., Li, H., Zhuo, J., Zhang, Y., Wang, J., Chen, L., … Jiang, T. (2016). The human brainnetome atlas: A new brain atlas based on Connectional Architecture. Cerebral Cortex, 26, 3508–3526.CrossRefGoogle Scholar
Fitzgerald, P. B., Laird, A. R., Maller, J., & Daskalakis, Z. J. (2008). A meta-analytic study of changes in brain activation in depression. Human Brain Mapping, 29, 683–695.CrossRefGoogle ScholarPubMed
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology Neurosurgery & Psychiatry, 23, 56.CrossRefGoogle ScholarPubMed
Harshaw, C. (2015). Interoceptive dysfunction: Toward an integrated framework for understanding somatic and affective disturbance in depression. Psychological Bulletin, 141, 311–363.CrossRefGoogle ScholarPubMed
Hatano, K., Terao, T., Hayashi, T., Hirakawa, H., Makino, M., Mizokami, Y., … Shimomura, T. (2019). Affective temperaments are associated with the white matter microstructure in healthy participants. Bipolar Disorder, 21, 539–546.CrossRefGoogle ScholarPubMed
Jabbi, M., Kippenhan, J. S., Kohn, P., Marenco, S., Mervis, C. B., Morris, C. A., … Berman, K. F. (2012). The Williams syndrome chromosome 7q11.23 hemideletion confers hypersocial, anxious personality coupled with altered insula structure and function. Proceedings of the National Academy of Sciences of the USA, 109, E860–E866.CrossRefGoogle ScholarPubMed
Kang, J., Bowman, F. D., Mayberg, H., & Liu, H. (2016). A depression network of functionally connected regions discovered via multi-attribute canonical correlation graphs. NeuroImage, 141, 431–441.CrossRefGoogle ScholarPubMed
Kawamura, Y., Akiyama, T., Shimada, T., Minato, T., Umekage, T., Noda, Y., … Akiskal, H. S. (2010). Six-year stability of affective temperaments as measured by TEMPS-A. Psychopathology, 43, 240–247.CrossRefGoogle ScholarPubMed
Kay, D. B., Karim, H. T., Soehner, A. M., Hasler, B. P., James, J. A., Germain, A., … Buysse, D. J. (2017). Subjective-objective sleep discrepancy is associated with alterations in regional glucose metabolism in patients with insomnia and good sleeper controls. Sleep, 40(11), zsx155.CrossRefGoogle ScholarPubMed
Kesebir, S., Gundogar, D., Kucuksubasi, Y., & Tatlidil Yaylaci, E. (2013). The relation between affective temperament and resilience in depression: A controlled study. Journal of Affective Disorders, 148, 352–356.CrossRefGoogle ScholarPubMed
Krishnan, A., Williams, L. J., Mcintosh, A. R., & Abdi, H. (2011). Partial least squares (PLS) methods for neuroimaging: A tutorial and review. Neuroimage, 56, 455–475.CrossRefGoogle ScholarPubMed
Kurth, F., Eickhoff, S. B., Schleicher, A., Hoemke, L., Zilles, K., & Amunts, K. (2010). Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cerebral Cortex, 20, 1448–1461.CrossRefGoogle ScholarPubMed
Leung, C. M., Wing, Y. K., Kwong, P. K., Lo, A., & Shum, K. (1999). Validation of the Chinese-Cantonese version of the hospital anxiety and depression scale and comparison with the Hamilton Rating Scale of Depression. Acta Psychiatrica Scandinavica, 100, 456–461.CrossRefGoogle ScholarPubMed
Lin, K., Xu, G., Miao, G., Ning, Y., Ouyang, H., Chen, X., … Akiskal, H. S. (2013). Psychometric properties of the Chinese (Mandarin) TEMPS-A: A population study of 985 non-clinical subjects in China. Journal of Affective Disorders, 147, 29–33.CrossRefGoogle ScholarPubMed
Liu, C. H., Guo, J., Lu, S. L., Tang, L. R., Fan, J., Wang, C. Y., … Liu, C. Z. (2018a). Increased salience network activity in patients with insomnia complaints in major depressive disorder. Frontiers in Psychiatry, 9, 93.CrossRefGoogle Scholar
Liu, C. H., Ma, X., Song, L. P., Fan, J., Wang, W. D., Lv, X. Y., … Wang, C. Y. (2015). Abnormal spontaneous neural activity in the anterior insular and anterior cingulate cortices in anxious depression. Behavioural Brain Research, 281, 339–347.CrossRefGoogle ScholarPubMed
Liu, C. H., Ma, X., Yuan, Z., Song, L. P., Jing, B., Lu, H. Y., … Wang, C. Y. (2017). Decreased resting-state activity in the precuneus is associated with depressive episodes in recurrent depression. Journal of Clinical Psychiatry, 78, e372–e382.CrossRefGoogle ScholarPubMed
Liu, P., Taber-Thomas, B. C., Fu, X., & Perez-Edgar, K. E. (2018b). Biobehavioral markers of attention bias modification in temperamental risk for anxiety: A randomized control trial. Journal of American Academy of Child & Adolescent Psychiatry, 57, 103–110.CrossRefGoogle Scholar
Manoliu, A., Meng, C., Brandl, F., Doll, A., Tahmasian, M., Scherr, M., … Sorg, C. (2013). Insular dysfunction within the salience network is associated with severity of symptoms and aberrant inter-network connectivity in major depressive disorder. Frontiers in Human Neuroscience, 7, 930.Google ScholarPubMed
McIntosh, A. R., & Lobaugh, N. J. (2004). Partial least squares analysis of neuroimaging data: Applications and advances. Neuroimage 23(Suppl 1), S250–S263.CrossRefGoogle ScholarPubMed
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure & Function, 214, 655–667.CrossRefGoogle ScholarPubMed
Michalska, K. J., Feldman, J. S., Ivie, E. J., Shechner, T., Sequeira, S., Averbeck, B., … Pine, D. S. (2018). Early-childhood social reticence predicts SCR-BOLD coupling during fear extinction recall in preadolescent youth. Developmental Cognitive Neuroscience, 36, 100605.CrossRefGoogle ScholarPubMed
Moser, D. A., Doucet, G. E., Lee, W. H., Rasgon, A., Krinsky, H., Leibu, E., … Frangou, S. (2018). Multivariate associations among behavioral, clinical, and multimodal imaging phenotypes in patients with psychosis. JAMA psychiatry, 75, 386–395.CrossRefGoogle ScholarPubMed
Namkung, H., Kim, S. H., & Sawa, A. (2017). The Insula: An underestimated brain area in clinical neuroscience, psychiatry, and neurology. Trends in Neurosciences, 40, 200–207.CrossRefGoogle ScholarPubMed
Naqvi, N. H., & Bechara, A. (2009). The hidden island of addiction: The insula. Trends in Neurosciences, 32, 56–67.CrossRefGoogle ScholarPubMed
Otte, C., Gold, S. M., Penninx, B. W., Pariante, C. M., Etkin, A., Fava, M., … Schatzberg, A. F. (2016). Major depressive disorder. Nature Reviews Disease Primers, 2, 16065.CrossRefGoogle ScholarPubMed
Park, B., Palomares, J. A., Woo, M. A., Kang, D. W., Macey, P. M., Yan-Go, F. L., … Kumar, R. (2016). Aberrant insular functional network integrity in patients with obstructive sleep apnea. Sleep, 39, 989–1000.CrossRefGoogle ScholarPubMed
Perico, C. A., Skaf, C. R., Yamada, A., Duran, F., Buchpiguel, C. A., Castro, C. C., … Busatto, G. F. (2005). Relationship between regional cerebral blood flow and separate symptom clusters of major depression: A single photon emission computed tomography study using statistical parametric mapping. Neuroscience Letters, 384, 265–270.CrossRefGoogle ScholarPubMed
Perlis, M. L., Giles, D. E., Buysse, D. J., Thase, M. E., Tu, X., & Kupfer, D. J. (1997). Which depressive symptoms are related to which sleep electroencephalographic variables? Biological Psychiatry, 42, 904–913.CrossRefGoogle ScholarPubMed
Pompili, M., Baldessarini, R. J., Innamorati, M., Vazquez, G. H., Rihmer, Z., Gonda, X., … Girardi, P. (2018). Temperaments in psychotic and major affective disorders. Journal of Affective Disorders, 225, 195–200.CrossRefGoogle ScholarPubMed
Pompili, M., Innamorati, M., Gonda, X., Erbuto, D., Forte, A., Ricci, F., … Girardi, P. (2014). Characterization of patients with mood disorders for their prevalent temperament and level of hopelessness. Journal of Affective Disorders, 166, 285–291.CrossRefGoogle ScholarPubMed
Pompili, M., Innamorati, M., Gonda, X., Serafini, G., Sarno, S., Erbuto, D., … Girardi, P. (2013). Affective temperaments and hopelessness as predictors of health and social functioning in mood disorder patients: A prospective follow-up study. Journal of Affective Disorders, 150, 216–222.CrossRefGoogle ScholarPubMed
Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage, 59, 2142–2154.CrossRefGoogle ScholarPubMed
Rabkin, J. G., & Klein, D. F. (1987). The clinical measurement of depressive disorders. In A. J. Marsella, R. M. A. Hirschfeld, & M. M. Katz (Eds.), The measurement of depression (pp. 30–83). New York, NY, USA: Guilford Press.Google Scholar
Rihmer, Z., Akiskal, K. K., Rihmer, A., & Akiskal, H. S. (2010). Current research on affective temperaments. Current Opinion in Psychiatry, 23, 12–18.CrossRefGoogle ScholarPubMed
Rihmer, Z., Gonda, X., Torzsa, P., Kalabay, L., Akiskal, H. S., & Eory, A. (2013). Affective temperament, history of suicide attempt and family history of suicide in general practice patients. Journal of Affective Disorders, 149, 350–354.CrossRefGoogle ScholarPubMed
Rihmer, A., Rozsa, S., Rihmer, Z., Gonda, X., Akiskal, K. K., & Akiskal, H. S. (2009). Affective temperaments, as measured by TEMPS-A, among nonviolent suicide attempters. Journal of Affective Disorders, 116, 18–22.CrossRefGoogle ScholarPubMed
Rovai, L., Maremmani, A. G., Rugani, F., Bacciardi, S., Pacini, M., Dell'Osso, L., … Maremmani, I. (2013). Do Akiskal & Mallya's affective temperaments belong to the domain of pathology or to that of normality? European Review for Medical and Pharmacological Sciences, 17, 2065–2079.Google ScholarPubMed
Serafini, G., Pompili, M., Innamorati, M., Fusar-Poli, P., Akiskal, H. S., Rihmer, Z., … Tatarelli, R. (2011). Affective temperamental profiles are associated with white matter hyperintensity and suicidal risk in patients with mood disorders. Journal of Affective Disorders, 129, 47–55.CrossRefGoogle ScholarPubMed
Serafini, G., Pompili, M., Romano, A., Erbuto, D., Lamis, D. A., Moraschi, M., … Bozzao, A. (2017). Neural correlates in patients with major affective disorders: An fMRI study. CNS & Neurological Disorders Drug Targets, 16, 907–914.Google ScholarPubMed
Shi, M., Hu, J., Dong, X., Gao, Y., An, G., Liu, W., … Sun, X. (2008). Association of unipolar depression with gene polymorphisms in the serotonergic pathways in Han Chinese. Acta Neuropsychiatrica, 20, 139–144.CrossRefGoogle ScholarPubMed
Solmi, M., Zaninotto, L., Toffanin, T., Veronese, N., Lin, K., Stubbs, B., … Correll, C. U. (2016). A comparative meta-analysis of TEMPS scores across mood disorder patients, their first-degree relatives, healthy controls, and other psychiatric disorders. Journal of Affective Disorders, 196, 32–46.CrossRefGoogle ScholarPubMed
Sprengelmeyer, R., Steele, J. D., Mwangi, B., Kumar, P., Christmas, D., Milders, M., & Matthews, K. (2011). The insular cortex and the neuroanatomy of major depression. Journal of Affective Disorders, 133, 120–127.CrossRefGoogle ScholarPubMed
Stein, M. B., Simmons, A. N., Feinstein, J. S., & Paulus, M. P. (2007). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. American Journal of Psychiatry, 164, 318–327.CrossRefGoogle ScholarPubMed
Su, L., Cai, Y., Xu, Y., Dutt, A., Shi, S., & Bramon, E. (2014). Cerebral metabolism in major depressive disorder: A voxel-based meta-analysis of positron emission tomography studies. BMC Psychiatry, 14, 321.CrossRefGoogle ScholarPubMed
Tian, Y., & Zalesky, A. (2018). Characterizing the functional connectivity diversity of the insula cortex: Subregions, diversity curves and behavior. NeuroImage, 183, 716–733.CrossRefGoogle ScholarPubMed
Tondo, L., Vázquez, G. H., Sani, G., Pinna, M., & Baldessarini, R. J. (2018). Association of suicidal risk with ratings of affective temperaments. Journal of Affective Disorders, 229, 322–327.CrossRefGoogle ScholarPubMed
Tu, Y., Fang, J., Cao, J., Wang, Z., Park, J., Jorgenson, K., … Kong, J. (2018). A distinct biomarker of continuous transcutaneous vagus nerve stimulation treatment in major depressive disorder. Brain Stimulation, 11, 501–508.CrossRefGoogle ScholarPubMed
Uddin, L. Q. (2014). Salience processing and insular cortical function and dysfunction. Nature Reviews Neuroscience, 16, 55.CrossRefGoogle ScholarPubMed
Uddin, L. Q., Nomi, J. S., Hebert-Seropian, B., Ghaziri, J., & Boucher, O. (2017). Structure and function of the human Insula. Journal of Clinical Neurophysiology, 34, 300–306.CrossRefGoogle ScholarPubMed
Vazquez, G. H., Gonda, X., Lolich, M., Tondo, L., & Baldessarini, R. J. (2018). Suicidal risk and affective temperaments, evaluated with the TEMPS-A scale: A systematic review. Harvard Review of Psychiatry, 26, 8–18.CrossRefGoogle ScholarPubMed
Vertes, P. E., Rittman, T., Whitaker, K. J., Romero-Garcia, R., Vasa, F., Kitzbichler, M. G., … Bullmore, E. T. (2016). Gene transcription profiles associated with inter-modular hubs and connection distance in human functional magnetic resonance imaging networks. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 371, 1–13.CrossRefGoogle ScholarPubMed
Wang, C., Wu, H., Chen, F., Xu, J., Li, H., Li, H., & Wang, J. (2018). Disrupted functional connectivity patterns of the insula subregions in drug-free major depressive disorder. Journal of Affective Disorder, 234, 297–304.CrossRefGoogle ScholarPubMed
Wang, X., Zhen, Z., Song, Y., Huang, L., Kong, X., & Liu, J. (2016). The hierarchical structure of the face network revealed by its functional connectivity pattern. The Journal of Neuroscience, 36, 890–900.CrossRefGoogle ScholarPubMed
Wang, Y. Z., Han, Y., Zhao, J. J., Du, Y., Zhou, Y., Liu, Y., … Li, L. (2019). Brain activity in patients with deficiency versus excess patterns of major depression: A task fMRI study. Complementary Therapies in Medicine, 42, 292–297.CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2, 125–141.CrossRefGoogle ScholarPubMed
Whittle, S., Allen, N. B., Lubman, D. I., & Yucel, M. (2006). The neurobiological basis of temperament: Towards a better understanding of psychopathology. Neuroscience and Biobehavioral Reviews, 30, 511–525.CrossRefGoogle ScholarPubMed
Wiebking, C., Duncan, N. W., Tiret, B., Hayes, D. J., Marjanska, M., Doyon, J., … Northoff, G. (2014). GABA in the insula – a predictor of the neural response to interoceptive awareness. Neuroimage, 86, 10–18.CrossRefGoogle ScholarPubMed
World Medical Association (2013). WMA Declaration of Helsiniki-Ethical Principles for Medical Research Involving Human Subjects. https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/.Google Scholar
Yu, H. L., Liu, W. B., Wang, T., Huang, P. Y., Jie, L. Y., Sun, J. Z., … Zhang, M. M. (2017). Difference in resting-state fractional amplitude of low-frequency fluctuation between bipolar depression and unipolar depression patients. European Review for Medical and Pharmacological Sciences, 21, 1541–1550.Google ScholarPubMed
Zou, Q. H., Zhu, C. Z., Yang, Y., Zuo, X. N., Long, X. Y., Cao, Q. J., … Zang, Y. F. (2008). An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: Fractional ALFF. Journal of Neuroscience Methods, 172, 137–141.CrossRefGoogle ScholarPubMed
Zuo, X. N., Di, M. A., Kelly, C., Shehzad, Z. E., Gee, D. G., Klein, D. F. … Milham, M. P. (2010). The oscillating brain: Complex and reliable. Neuroimage, 49, 1432.CrossRefGoogle ScholarPubMed
Supplementary material: File

Wu et al. supplementary material

Figures S1-S2

Download Wu et al. supplementary material(File)
File 1.9 MB