Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-28T16:03:56.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of selective serotonin reuptake inhibitor on prefrontal-striatal connectivity is dependent on the level of TNF-α in patients with major depressive disorder

Published online by Cambridge University Press:  06 December 2018

Kai Liu ,
Xiaohua Zhao ,
Xiaobing Lu ,
Xiaoxia Zhu ,
Hui Chen ,
Mengmeng Wang ,
Weixin Yan ,
Linlin Jing ,
Yanjia Deng  and
Lin Yu
...Show all authors
Kai Liu
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China Medical Imaging Department, Nanfang Hospital, Southern Medical University, Guangzhou, China
Xiaohua Zhao
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China
Xiaobing Lu
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou, China
Xiaoxia Zhu
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China
Hui Chen
Affiliation:
Medical Imaging Department, Nanfang Hospital, Southern Medical University, Guangzhou, China
Mengmeng Wang
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China
Weixin Yan
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China
Linlin Jing
Affiliation:
TCM Integrated Hospital of Southern Medical University, Southern Medical University, Guangzhou, China
Yanjia Deng
Affiliation:
Medical Imaging Department, Nanfang Hospital, Southern Medical University, Guangzhou, China
Lin Yu
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou, China
Huawang Wu
Affiliation:
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou, China
Ge Wen*
Affiliation:
Medical Imaging Department, Nanfang Hospital, Southern Medical University, Guangzhou, China
Xuegang Sun*
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China Key Laboratory of Ministry of Education for TCM Viscera-State Theory and Applications, Liaoning University of Traditional Chinese Medicine, Shenyang, China
Zhiping Lv*
Affiliation:
School of Traditional Chinese Medicine, Southern Medical University, Guangzhou, China
*
Author for correspondence: Zhiping Lv, E-mail: [email protected] and Ge Wen, E-mail: [email protected]; Xuegang Sun, E-mail: [email protected]
Author for correspondence: Zhiping Lv, E-mail: [email protected] and Ge Wen, E-mail: [email protected]; Xuegang Sun, E-mail: [email protected]
Author for correspondence: Zhiping Lv, E-mail: [email protected] and Ge Wen, E-mail: [email protected]; Xuegang Sun, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

We hypothesize that the tumor necrosis factor-α (TNF-α) may play a role in disturbing the effect of selective serotonin reuptake inhibitor (SSRI) on the striatal connectivity in patients with major depressive disorder (MDD).

Methods

We performed a longitudinal observation by combining resting-state functional magnetic resonance imaging (rs-fMRI) and biochemical analyses to identify the abnormal striatal connectivity in MDD patients, and to evaluate the effect of TNF-α level on these abnormal connectivities during SSRI treatment. Eighty-five rs-fMRI scans were collected from 25 MDD patients and 35 healthy controls, and the scans were repeated for all the patients before and after a 6-week SSRI treatment. Whole-brain voxel-wise functional connectivity (FC) was calculated by correlating the rs-fMRI time courses between each voxel and the striatal seeds (i.e. spherical regions placed at the striatums). The level of TNF-α in serum was evaluated by Milliplex assay. Factorial analysis was performed to assess the interaction effects of ‘TNF-α × treatment’ in the regions with between-group FC difference.

Results

Compared with controls, MDD patients showed significantly higher striatal FC in the medial prefrontal cortex (MPFC) and bilateral middle/superior temporal cortices before SSRI treatment (p < 0.001, uncorrected). Moreover, a significant interaction effect of ‘TNF-α × treatment’ was found in MPFC-striatum FC in MDD patients (p = 0.002), and the significance remained after adjusted for age, gender, head motion, and episode of disease.

Conclusion

These findings provide evidence that treatment-related brain connectivity change is dependent on the TNF-α level in MDD patients, and the MPFC-striatum connectivities possibly serve as an important target in the brain.

Keywords

Major depressive disorderresting-state functional connectivityselective serotonin reuptake inhibitorstriatumtumor necrosis factor-α
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 15 , November 2019 , pp. 2608 - 2616
Copyright
Copyright © Cambridge University Press 2018 

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 paper.

References

Bartra, O, McGuire, JT and Kable, JW (2013) The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 76, 412–427.Google Scholar
Bay-Richter, C, Janelidze, S, Hallberg, L and Brundin, L (2011) Changes in behaviour and cytokine expression upon a peripheral immune challenge. Behavioural Brain Research 222, 193–199.Google Scholar
Boomsma, DI, Willemsen, G, Sullivan, PF, Heutink, P, Meijer, P, Sondervan, D, Kluft, C, Smit, G, Nolen, WA, Zitman, FG, Smit, JH, Hoogendijk, WJ, van Dyck, R, de Geus, EJ and Penninx, BW (2008) Genome-wide association of major depression: description of samples for the GAIN Major Depressive Disorder Study: NTR and NESDA biobank projects. European Journal of Human Genetics 16, 335–342.Google Scholar
Cullen, KR, Westlund, MK, Klimes-Dougan, B, Mueller, BA, Houri, A, Eberly, LE and Lim, KO (2014) Abnormal amygdala resting-state functional connectivity in adolescent depression. JAMA Psychiatry 71, 1138–1147.10.1001/jamapsychiatry.2014.1087Google Scholar
Dowlati, Y, Herrmann, N, Swardfager, W, Liu, H, Sham, L, Reim, EK and Lanctot, KL (2010) A meta-analysis of cytokines in major depression. Biological Psychiatry 67, 446–457.Google Scholar
Eller, T, Vasar, V, Shlik, J and Maron, E (2008) Pro-inflammatory cytokines and treatment response to escitalopram in major depressive disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry 32, 445–450.Google Scholar
Felger, JC, Li, Z, Haroon, E, Woolwine, BJ, Jung, MY, Hu, X and Miller, AH (2016) Inflammation is associated with decreased functional connectivity within corticostriatal reward circuitry in depression. Molecular Psychiatry 21, 1358–1365.Google Scholar
First, MB, Gibbon, M and Williams, JBW (2002) Structured Clinical Interview for DSM-IV-TR Axis I Disorders research version, patient edition (SCID-I/P). Biometrics Research. New York: NY State Psychiatric Institute 111, 6058–6062.Google Scholar
Gadek-Michalska, A, Tadeusz, J, Rachwalska, P and Bugajski, J (2013) Cytokines, prostaglandins and nitric oxide in the regulation of stress-response systems. Pharmacological Reports 65, 1655–1662.Google Scholar
Grimm, S, Ernst, J, Boesiger, P, Schuepbach, D, Hell, D, Boeker, H and Northoff, G (2009) Increased self-focus in major depressive disorder is related to neural abnormalities in subcortical-cortical midline structures. Human Brain Mapping 30, 2617–2627.10.1002/hbm.20693Google Scholar
Guillemin, GJ, Smythe, G, Takikawa, O and Brew, BJ (2005) Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia 49, 15–23.10.1002/glia.20090Google Scholar
Hamilton, JP, Chen, G, Thomason, ME, Schwartz, ME and Gotlib, IH (2011) Investigating neural primacy in major depressive disorder: multivariate granger causality analysis of resting-state fMRI time-series data. Molecular Psychiatry 16, 763–772.Google Scholar
Hanson, JL, Knodt, AR, Brigidi, BD and Hariri, AR (2018) Heightened connectivity between the ventral striatum and medial prefrontal cortex as a biomarker for stress-related psychopathology: understanding interactive effects of early and more recent stress. Psychological Medicine 48, 1835–1843.Google Scholar
Heller, AS (2016) Cortical-subcortical interactions in depression: from animal models to human psychopathology. Frontiers in Systems Neuroscience 10, 20.Google Scholar
Ho, TC, Yang, G, Wu, J, Cassey, P, Brown, SD, Hoang, N, Chan, M, Connolly, CG, Henje-Blom, E, Duncan, LG, Chesney, MA, Paulus, MP, Max, JE, Patel, R, Simmons, AN and Yang, TT (2014) Functional connectivity of negative emotional processing in adolescent depression. Journal Affective Disorder 155, 65–74.Google Scholar
Hughes, MM, Connor, TJ and Harkin, A (2016) Stress-related immune markers in depression: implications for treatment. International Journal of Neuropsychopharmacology 19, 1–19.Google Scholar
Iosif, RE, Ekdahl, CT, Ahlenius, H, Pronk, CJ, Bonde, S, Kokaia, Z, Jacobsen, SE and Lindvall, O (2006) Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. Journal of Neuroscience 26, 9703–9712.Google Scholar
Kaiser, RH, Andrews-Hanna, JR, Wager, TD and Pizzagalli, DA (2015) Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity. JAMA Psychiatry 72, 603–611.Google Scholar
Kim, HK, Nunes, PV, Oliveira, KC, Young, LT and Lafer, B (2016) Neuropathological relationship between major depression and dementia: a hypothetical model and review. Progress in Neuro-Psychopharmacology and Biological Psychiatry 67, 51–57.Google Scholar
Knowland, D, Lilascharoen, V, Pacia, CP, Shin, S, Wang, EH and Lim, BK (2017) Distinct ventral pallidal neural populations mediate separate symptoms of depression. Cell 170, 284–297.Google Scholar
Kong, Y, Deng, Y and Dai, Q (2015) Discriminative clustering and feature selection for brain MRI segmentation. IEEE Signal Processing Letters 22, 573–577.Google Scholar
Kuhn, S and Gallinat, J (2013) Resting-state brain activity in schizophrenia and major depression: a quantitative meta-analysis. Schizophrenia Bulletin 39, 358–365.Google Scholar
Liu, Z, Liu, J, Wang, J, Xu, J, Liu, Y, Sun, X, Su, L, Wang, JH and Jiang, Y (2014) Role of testis-specific high-mobility-group protein in transcriptional regulation of inducible nitric oxide synthase expression in the liver of endotoxic shock mice. FEBS Journal 281, 2202–2213.Google Scholar
Luking, KR, Repovs, G, Belden, AC, Gaffrey, MS, Botteron, KN, Luby, JL and Barch, DM (2011) Functional connectivity of the amygdala in early-childhood-onset depression. Journal of the American Academy of Child and Adolescent Psychiatry 50, 1027–1041.Google Scholar
Ma, K, Zhang, H and Baloch, Z (2016) Pathogenetic and therapeutic applications of tumor necrosis factor-α (TNF-α) in major depressive disorder: a systematic review. International Journal of Molecular Sciences 17, 733.Google Scholar
Manosso, LM, Neis, VB, Moretti, M, Daufenbach, JF, Freitas, AE, Colla, AR and Rodrigues, AL (2013) Antidepressant-like effect of alpha-tocopherol in a mouse model of depressive-like behavior induced by TNF-alpha. Progress in Neuro-Psychopharmacology and Biological Psychiatry 46, 48–57.Google Scholar
Marchetti, I, Koster, EH, Sonuga-Barke, EJ and De Raedt, R (2012) The default mode network and recurrent depression: a neurobiological model of cognitive risk factors. Neuropsychology Review 22, 229–251.Google Scholar
Miller, AH, Maletic, V and Raison, CL (2009) Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression. Biological Psychiatry 65, 732–741.Google Scholar
Monje, ML, Toda, H and Palmer, TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302, 1760–1765.Google Scholar
Muller, N, Schwarz, MJ, Dehning, S, Douhe, A, Cerovecki, A, Goldstein-Muller, B, Spellmann, I, Hetzel, G, Maino, K, Kleindienst, N, Moller, HJ, Arolt, V and Riedel, M (2006) The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Molecular Psychiatry 11, 680–684.Google Scholar
Muller, VI, Cieslik, EC, Serbanescu, I, Laird, AR, Fox, PT and Eickhoff, SB (2017) Altered brain activity in unipolar depression revisited: meta-analyses of neuroimaging studies. JAMA Psychiatry 74, 47–55.Google Scholar
Myint, AM and Kim, YK (2014) Network beyond IDO in psychiatric disorders: revisiting neurodegeneration hypothesis. Progress in Neuro-Psychopharmacology and Biological Psychiatry 48, 304–313.Google Scholar
Myint, AM, Kim, YK, Verkerk, R, Scharpe, S, Steinbusch, H and Leonard, B (2007) Kynurenine pathway in major depression: evidence of impaired neuroprotection. Journal of Affective Disorder 98, 143–151.Google Scholar
Oglodek, EA, Just, MJ, Szromek, AR and Araszkiewicz, A (2017) Assessing the serum concentration levels of NT-4/5, GPX-1, TNF-alpha, and l-arginine as biomediators of depression severity in first depressive episode patients with and without posttraumatic stress disorder. Pharmacological Reports 69, 1049–1058.Google Scholar
Pan, PM, Sato, JR, Salum, GA, Rohde, LA, Gadelha, A, Zugman, A, Mari, J, Jackowski, A, Picon, F, Miguel, EC, Pine, DS, Leibenluft, E, Bressan, RA and Stringaris, A (2017) Ventral striatum functional connectivity as a predictor of adolescent depressive disorder in a longitudinal community-based sample. The American Journal of Psychiatry 174, 1112–1119.Google Scholar
Pessiglione, M, Schmidt, L, Draganski, B, Kalisch, R, Lau, H, Dolan, RJ and Frith, CD (2007) How the brain translates money into force: a neuroimaging study of subliminal motivation. Science 316, 904–906.Google Scholar
Petrulli, JR, Kalish, B, Nabulsi, NB, Huang, Y, Hannestad, J and Morris, ED (2017) Systemic inflammation enhances stimulant-induced striatal dopamine elevation. Translational Psychiatry 7, e1076.Google Scholar
Power, JD, Mitra, A, Laumann, TO, Snyder, AZ, Schlaggar, BL and Petersen, SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320–341.Google Scholar
Quevedo, K, Ng, R, Scott, H, Kodavaganti, S, Smyda, G, Diwadkar, V and Phillips, M (2017) Ventral striatum functional connectivity during rewards and losses and symptomatology in depressed patients. Biological Psychology 123, 62–73.Google Scholar
Root, DH, Melendez, RI, Zaborszky, L and Napier, TC (2015) The ventral pallidum: subregion-specific functional anatomy and roles in motivated behaviors. Progress in Neurobiology 130, 29–70.Google Scholar
Satterthwaite, TD, Kable, JW, Vandekar, L, Katchmar, N, Bassett, DS, Baldassano, CF, Ruparel, K, Elliott, MA, Sheline, YI, Gur, RC, Gur, RE, Davatzikos, C, Leibenluft, E, Thase, ME and Wolf, DH (2015) Common and dissociable dysfunction of the reward system in bipolar and unipolar depression. Neuropsychopharmacology 40, 2258–2268.Google Scholar
Schmidt, HD, Shelton, RC and Duman, RS (2011) Functional biomarkers of depression: diagnosis, treatment, and pathophysiology. Neuropsychopharmacology 36, 2375–2394.Google Scholar
Sheline, YI, Price, JL, Yan, Z and Mintun, MA (2010) Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences 107, 11020–11025.Google Scholar
Smith, KS, Tindell, AJ, Aldridge, JW and Berridge, KC (2009) Ventral pallidum roles in reward and motivation. Behavioural Brain Research 196, 155–167.Google Scholar
Sturup, J, Kristiansson, M and Lindqvist, P (2011) Violent behaviour by general psychiatric patients in Sweden - validation of Classification of Violence Risk (COVR) software. Psychiatry Research 188, 161–165.Google Scholar
Weissenbacher, A, Kasess, C, Gerstl, F, Lanzenberger, R, Moser, E and Windischberger, C (2009) Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. Neuroimage 47, 1408–1416.Google Scholar
Yamada, K, Iida, R, Miyamoto, Y, Saito, K, Sekikawa, K, Seishima, M and Nabeshima, T (2000) Neurobehavioral alterations in mice with a targeted deletion of the tumor necrosis factor-alpha gene: implications for emotional behavior. Journal of Neuroimmunology 111, 131–138.Google Scholar
Zeng, LL, Wang, D, Fox, MD, Sabuncu, M, Hu, D, Ge, M, Buckner, RL and Liu, H (2014) Neurobiological basis of head motion in brain imaging. Proceedings of the National Academy of Sciences 111, 6058–6062.Google Scholar
Zhao, X, Cao, F, Liu, Q, Li, X, Xu, G, Liu, G, Zhang, Y, Yang, X, Yi, S, Xu, F, Fan, K and Ma, J (2017) Behavioral, inflammatory and neurochemical disturbances in LPS and UCMS-induced mouse models of depression. Behavioural Brain Research 5, S0166–S4328.Google Scholar
Zhu, CB, Blakely, RD and Hewlett, WA (2006) The proinflammatory cytokines interleukin-1beta and tumor necrosis factor-alpha activate serotonin transporters. Neuropsychopharmacology 31, 2121–2131.Google Scholar
Supplementary material: File

Liu et al. supplementary material

Liu et al. supplementary material 1

Download Liu et al. supplementary material(File)
File 959 KB