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Research Paper

Spontaneous low-frequency fluctuations in the neural system for emotional perception in major psychiatric disorders: amplitude similarities and differences across frequency bands

Miao Chang, Elliot K. Edmiston, Fay Y. Womer, Qian Zhou, Shengnan Wei, Xiaowei Jiang, Yifang Zhou, Yuting Ye, Haiyan Huang, Xi-Nian Zuo, Ke Xu, Yanqing Tang and Fei Wang
J Psychiatry Neurosci March 01, 2019 44 (2) 132-141; DOI: https://doi.org/10.1503/jpn.170226
Miao Chang
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Elliot K. Edmiston
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Fay Y. Womer
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Qian Zhou
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Shengnan Wei
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Xiaowei Jiang
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Yifang Zhou
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Yuting Ye
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Haiyan Huang
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Xi-Nian Zuo
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Ke Xu
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Yanqing Tang
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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Fei Wang
From the Department of Radiology, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Jiang, Wang, Wei, Xu); the Department of Psychiatry, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Tang, Q. Zhou, Y. Zhou); the Brain Function Research Section, First Affiliated Hospital of China Medical University, Shenyang, Liaoning, PR China (Chang, Edmiston, Jiang, Tang, Wang, Wei, Xu, Q. Zhou, Y. Zhou); the Department of Psychiatry, Washington University School of Medicine, St. Louis, MO (Womer); the Division of Biostatistics, University of California, Berkeley, Berkeley, CA (Huang, Ye); the CAS Key Laboratory of Behavioral Science, Institute of Psychology, Beijing, PR China (Zuo); and the Department of Psychology, University of Chinese Academy of Sciences, Beijing, PR China (Zuo).
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    Fig. 1

    Significantly altered regions of ALFF values for slow-5 in participants with schizophrenia, bipolar disorder and major depressive disorder, and healthy controls (A) by ANCOVA, (B) between schizophrenia and controls, (C) between bipolar disorder and controls, and (D) between major depressive disorder and controls. Significant at p < 0.05, Alphasim correction. ALFF = amplitude of low-frequency fluctuation; ANCOVA = analysis of covariance.

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    Fig. 2

    Significantly altered regions of ALFF values for slow-4 in participants with schizophrenia, bipolar disorder and major depressive disorder, and healthy controls (A) by ANCOVA, (B) between schizophrenia and controls, (C) between bipolar disorder and controls, and (D) between major depressive disorder and controls. Significant at p < 0.05, Alphasim correction. ALFF = amplitude of low-frequency fluctuation; ANCOVA = analysis of covariance.

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    Fig. 3

    ALFF balance ratio in (A) slow-5 and (B) slow-4 for participants with schizophrenia, bipolar disorder or major depressive disorder, and healthy controls. Significant at pFDR < 0.05. ALFF = amplitude of low-frequency fluctuation; FDR = false discovery rate. ***p < 0.001.

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    Table 1

    Participant demographic characteristics, clinical characteristics and cognitive function

    CharacteristicGroup; mean ± SD or no. (%)Fp value
    Control (n = 183)Schizophrenia (n = 119)Bipolar disorder (n = 100)Major depressive disorder (n = 123)
    Age at scan, yr26.62 ± 8.0024.77 ± 9.0725.72 ± 7.8827.74 ± 9.762.596§0.052
    Male73 (40)54 (45)48 (48)34 (28)10.932§0.012
    Right-handed175 (96)107 (90)97 (97)116 (94)9.121§0.17
    Duration, mo—22.09 ± 36.4241.48 ± 56.1821.10 ± 39.246.605¶0.002
    First episode—84 (71)52 (52)97 (79)27.221¶< 0.001
    Medication—71 (60)65 (65)49 (40)20.746¶< 0.001
    Antidepressant—9 (8)28 (28)43 (35)27.007¶< 0.001
    Antipsychotic—65 (55)32 (32)4 (3)77.108¶< 0.001
    Mood stabilizer—4 (3)52 (52)0131.489¶< 0.001
    Hamilton Rating Scale for Depression*1.17 ± 1.688.01 ± 6.9811.74 ± 9.5421.37 ± 8.72198.298§< 0.001
    Brief Psychiatric Rating Scale†18.31 ± 0.8236.14 ± 14.0925.68 ± 8.4325.59 ± 6.1765.772§< 0.001
    Cognitive function (Wisconsin Card Sorting Test)‡
     Corrected responses32.31 ± 10.6617.39 ± 12.1725.44 ± 11.5225.03 ± 11.4811.100§< 0.001
     Categories completed4.32 ± 1.971.72 ± 1.903.00 ± 2.033.00 ± 1.9714.756§< 0.001
     Total errors15.69 ± 10.6630.62 ± 12.2222.56 ± 11.5223.29 ± 11.6310.569§< 0.001
     Perseverative errors5.76 ± 6.6814.70 ± 13.029.22 ± 9.379.67 ± 9.315.126§0.002
     Nonperseverative errors9.98 ± 5.5815.93 ± 8.6413.16 ± 7.0413.64 ± 6.046.033§0.001
    • SD = standard deviation.

    • ↵* Control, n = 162; schizophrenia, n = 83; bipolar disorder, n = 98; major depressive disorder, n = 122.

    • ↵† Control, n = 101; schizophrenia, n = 114; bipolar disorder, n = 60; major depressive disorder, n = 56.

    • ↵‡ Control, n = 101; schizophrenia, n = 74; bipolar disorder, n = 45; major depressive disorder, n = 70.

    • ↵§ Among the healthy control, schizophrenia, bipolar disorder and major depressive disorder groups.

    • ↵¶ Among the schizophrenia, bipolar disorder and major depressive disorder groups.

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    Table 2

    ALFF values for slow-5 in brain regions showing significant group differences

    Brain regionBrodmann areaCluster size, voxels (mm3)Peak MNI coordinatesF
    xyz
    Anterior cerebral
     Right caudate nucleus, right putamen, right thalamic, right amygdala, right hippocampus, right parahippocampal gyrus47/34/25378 (756)915−319.139
     Right hippocampus, right parahippocampal gyrus36/20/28219 (428)27−36913.876
     Right ventral prefrontal cortex47/1164 (128)4233−68.741
     Right dorsal prefrontal cortex10/1176 (152)1860310.996
     Left caudate nucleus, left putamen, left thalamus, left amygdala, left hippocampus, left parahippocampal gyrus, left temporal pole, left insula, left anterior cingulate cortex, left orbitofrontal cortex, left ventral prefrontal cortex47/34/28/36/11862 (1724)−915−321.600
     Left anterior cingulate cortex10/3239 (78)−1248157.226
     Left temporal pole, left inferior temporal gyrus, left middle temporal gyrus21/20/3888 (176)−519−3010.692
     Left inferior temporal gyrus, left middle temporal gyrus21/2032 (64)−42−21−277.798
    Posterior cerebral
     Bilateral cuneus gyri, bilateral precuneus gyri, bilateral lingual gyri, bilateral calcarine cortices, bilateral fusiform gyri, bilateral posterior cingulate gyri18/19/17/30/31/231134 (2268)−3−93−614.155
     Left precentral gyrus3/4/1/276 (152)−51−154811.201
     Bilateral paracentral lobules5/430 (60)0−45669.864
    • ALFF = amplitude of low-frequency fluctuations; MNI = Montreal Neurological Institute.

    • View popup
    Table 3

    ALFF values for slow-4 in brain regions showing significant group differences

    Brain regionBrodmann areaCluster size, voxels (mm3)Peak MNI coordinatesF
    xyz
    Anterior cerebral
     Bilateral caudate nuclei, bilateral putamina, bilateral amygdalae, bilateral hippocampi, left temporal pole, bilateral orbitofrontal cortices, bilateral parahippocampal gyri, left insula, left anterior cingulate cortex, bilateral ventral prefrontal cortices, left inferior temporal gyri, right frontal pole, right dorsal prefrontal cortex47/11/36/25/10/34/382085 (4170)−915−315.810
     Right putamen27 (54)30038.803
     Right temporal pole3842 (84)30−3−429.195
     Left inferior temporal gyrus, left middle temporal gyrus20/2183 (166)−54−3−3012.662
    Posterior cerebral
     Bilateral cuneus gyri, bilateral precuneus gyri, bilateral lingual gyri, bilateral calcarine cortices, bilateral fusiform gyri, bilateral posterior cingulate gyri18/19/17/30/31/231328 (2656)9−87315.229
     Right middle occipital gyrus, right middle temporal gyrus, right inferior occipital gyrus, right inferior temporal gyrus37/19138 (276)45−66−1211.202
     Left middle occipital gyrus, left middle temporal gyrus, left inferior occipital gyrus37/1965 (130)−4578−610.446
     Left inferior temporal gyrus
     Right precentral gyrus628 (54)33−15669.39
     Right postcentral gyrus3/2/40/4/168 (136)45−24488.295
     Left postcentral gyrus3/4/1/294 (188)−54−154810.418
     Bilateral paracentral lobules6/5/4200 (400)−3−42609.524
    • ALFF = amplitude of low-frequency fluctuations; MNI = Montreal Neurological Institute.

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Journal of Psychiatry and Neuroscience: 44 (2)
J Psychiatry Neurosci
Vol. 44, Issue 2
1 Mar 2019
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Spontaneous low-frequency fluctuations in the neural system for emotional perception in major psychiatric disorders: amplitude similarities and differences across frequency bands
Miao Chang, Elliot K. Edmiston, Fay Y. Womer, Qian Zhou, Shengnan Wei, Xiaowei Jiang, Yifang Zhou, Yuting Ye, Haiyan Huang, Xi-Nian Zuo, Ke Xu, Yanqing Tang, Fei Wang
J Psychiatry Neurosci Mar 2019, 44 (2) 132-141; DOI: 10.1503/jpn.170226

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Spontaneous low-frequency fluctuations in the neural system for emotional perception in major psychiatric disorders: amplitude similarities and differences across frequency bands
Miao Chang, Elliot K. Edmiston, Fay Y. Womer, Qian Zhou, Shengnan Wei, Xiaowei Jiang, Yifang Zhou, Yuting Ye, Haiyan Huang, Xi-Nian Zuo, Ke Xu, Yanqing Tang, Fei Wang
J Psychiatry Neurosci Mar 2019, 44 (2) 132-141; DOI: 10.1503/jpn.170226
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