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Resting-state brain alteration after a single dose of SSRI administration predicts 8-week remission of patients with major depressive disorder

Published online by Cambridge University Press:  04 October 2016

Y. Cheng ,
J. Xu ,
D. Arnone ,
B. Nie ,
H. Yu ,
H. Jiang ,
Y. Bai ,
C. Luo ,
R. A. A. Campbell  and
B. Shan
...Show all authors
Y. Cheng
Affiliation:
Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China
J. Xu
Affiliation:
Department of Internal Medicine, First Affiliated Hospital of Kunming Medical University, Kunming, China
D. Arnone
Affiliation:
Department of Psychological Medicine, Centre for Affective Disorders, King's College London, London, UK
B. Nie
Affiliation:
Key Laboratory of Nuclear Analysis Techniques, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, China
H. Yu
Affiliation:
Magnetic Resonance Imaging Center, the First Hospital of Kunming City, Kunming, China
H. Jiang
Affiliation:
Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China
Y. Bai
Affiliation:
Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China
C. Luo
Affiliation:
Magnetic Resonance Imaging Center, the First Hospital of Kunming City, Kunming, China
R. A. A. Campbell
Affiliation:
Department of Neuroscience, Cold Spring Harbor Laboratory, New York, USA
B. Shan
Affiliation:
Key Laboratory of Nuclear Analysis Techniques, Institute of High Energy Physics, Chinese Academy of Sciences, Beijing, China
L. Xu
Affiliation:
Key Laboratory of Animal Models and Human Disease Mechanisms, Chinese Academy of Sciences & Yunnan Province, Kunming Institute of Zoology, Kunming, China
X. Xu*
Affiliation:
Department of Psychiatry, First Affiliated Hospital of Kunming Medical University, Kunming, China
*
*Address for correspondence: X. Xu, MD, Department of Psychiatry, the First Affiliated Hospital of Kunming Medical University, 295 Xichang Road, Kunming 650032, People's Republic of China. (Email: [email protected], [email protected])
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Abstract

Background

The present study investigated alteration of brain resting-state activity induced by antidepressant treatment and attempted to investigate whether treatment efficacy can be predicted at an early stage of pharmacological treatment.

Method

Forty-eight first-episode medication-free patients diagnosed with major depression received treatment with escitalopram. Resting-state functional magnetic resonance imaging was administered prior to treatment, 5 h after the first dose, during the course of pharmacological treatment (week 4) and at endpoint (week 8). Resting-state activity was evaluated in the course of the 8-week treatment and in relation to clinical improvement.

Results

Escitalopram dynamically modified resting-state activity in depression during the treatment. After 5 h the antidepressant induced a significant decrease in the signal in the occipital cortex and an increase in the dorsolateral and dorsomedial prefrontal cortices and middle cingulate cortex. Furthermore, while remitters demonstrated more obvious changes following treatment, these were more modest in non-responders suggesting possible tonic and dynamic differences in the serotonergic system. Changes after 5 h in the caudate, occipital and temporal cortices were the best predictor of clinical remission at endpoint.

Conclusions

This study revealed the possibility of using the measurement of resting-state neural changes a few hours after acute administration of antidepressant to identify individuals likely to remit after a few weeks of treatment.

Keywords

Escitalopramfirst-episodefractional amplitude of low-frequency fluctuation (fALFF)major depressive disorderneuroimagingremissionresting-state fMRI
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 3 , February 2017 , pp. 438 - 450
Copyright
Copyright © Cambridge University Press 2016 

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References

Anderson, IM, Juhasz, G, Thomas, E, Downey, D, McKie, S, Deakin, JF, Elliott, R (2011). The effect of acute citalopram on face emotion processing in remitted depression: a pharmacoMRI study. European Neuropsychopharmacology 21, 140–148.CrossRefGoogle ScholarPubMed
APA, (2010). Practice Guideline for the Treatment of Patients with Major Depressive Disorder, 3rd edn. American Psychiatric Association: Arlington, VA.Google Scholar
Arnone, D, Job, D, Selvaraj, S, Abe, O, Amico, F, Cheng, Y, Colloby, SJ, O'Brien, JT, Frodl, T, Gotlib, IH, Ham, BJ, Kim, MJ, Koolschijn, PC, Perico, CA, Salvadore, G, Thomas, AJ, Van Tol, MJ, van der Wee, NJ, Veltman, DJ, Wagner, G, McIntosh, AM (2016). Computational meta-analysis of statistical parametric maps in major depression. Human Brain Mapping 37, 1393–1404.CrossRefGoogle ScholarPubMed
Artigas, F (1993). 5-HT and antidepressants: new views from microdialysis studies. Trends in Pharmacological Sciences 14, 262.CrossRefGoogle ScholarPubMed
Bauer, M, Pfennig, A, Severus, E, Whybrow, PC, Angst, J, Möller, H-J (2013). World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for biological treatment of unipolar depressive disorders, part 1: update 2013 on the acute and continuation treatment of unipolar depressive disorders. World Journal of Biological Psychiatry 14, 334–385.CrossRefGoogle ScholarPubMed
Beckmann, CF, DeLuca, M, Devlin, JT, Smith, SM (2005). Investigations into resting-state connectivity using independent component analysis. Philosophical Transactions of the Royal Society pf London, Series B: Biological Sciences 360, 1001–1013.CrossRefGoogle ScholarPubMed
Biswal, B, Zerrin Yetkin, F, Haughton, VM, Hyde, JS (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine 34, 537–541.CrossRefGoogle ScholarPubMed
Bozkurt, A, Zilles, K, Schleicher, A, Kamper, L, Arigita, ES, Uylings, H, Kötter, R (2005). Distributions of transmitter receptors in the macaque cingulate cortex. Neuroimage 25, 219–229.CrossRefGoogle ScholarPubMed
Carvalho, A, Cavalcante, J, Castelo, M, Lima, M (2007). Augmentation strategies for treatment-resistant depression: a literature review. Journal of Clinical Pharmacy and Therapeutics 32, 415–428.CrossRefGoogle ScholarPubMed
Celada, P, Puig, MV, Amargós-Bosch, M, Adell, A, Artigas, F (2004). The therapeutic role of 5-HT1A and 5-HT2A receptors in depression. Journal of Psychiatry and Neuroscience 29, 252.Google ScholarPubMed
Connolly, CG, Wu, J, Ho, TC, Hoeft, F, Wolkowitz, O, Eisendrath, S, Frank, G, Hendren, R, Max, JE, Paulus, MP (2013). Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biological Psychiatry 74, 898–907.CrossRefGoogle ScholarPubMed
Delaveau, P, Jabourian, M, Lemogne, C, Allaili, N, Choucha, W, Girault, N, Lehericy, S, Laredo, J, Fossati, P (2016). Antidepressant short-term and long-term brain effects during self-referential processing in major depression. Psychiatry Research 247, 17–24.CrossRefGoogle ScholarPubMed
Dichter, GS, Gibbs, D, Smoski, MJ (2015). A systematic review of relations between resting-state functional-MRI and treatment response in major depressive disorder. Journal of Affective Disorders 172, 8–17.CrossRefGoogle ScholarPubMed
el Mestikawy, S, Fargin, A, Raymond, JR, Gozlan, H, Hnatowich, M (1991). The 5-HT1A receptor: an overview of recent advances. Neurochemical Research 16, 1–10.CrossRefGoogle ScholarPubMed
First, MB, Spitzer, RL, Gibbon, M, Williams, JB (1996). Structured clinical Interview for DSM-IV Axis I Disorders. New York State Psychiatric Institute: New York.Google Scholar
Fransson, P, Skiöld, B, Horsch, S, Nordell, A, Blennow, M, Lagercrantz, H, Åden, U (2007). Resting-state networks in the infant brain. Proceedings of the National Academy of Sciences USA 104, 15531–15536.CrossRefGoogle ScholarPubMed
Hamilton, M (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology 32, 50–55.CrossRefGoogle ScholarPubMed
Hamilton, M (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Heller, AS, Johnstone, T, Peterson, MJ, Kolden, GG, Kalin, NH, Davidson, RJ (2013). Increased prefrontal cortex activity during negative emotion regulation as a predictor of depression symptom severity trajectory over 6 months. JAMA Psychiatry 70, 1181–1189.CrossRefGoogle ScholarPubMed
Küblböck, M, Woletz, M, Höflich, A, Sladky, R, Kranz, GS, Hoffmann, A, Lanzenberger, R, Windischberger, C (2014). Stability of low-frequency fluctuation amplitudes in prolonged resting-state fMRI. Neuroimage 103, 249–257.CrossRefGoogle ScholarPubMed
Kim, JM, Kim, SY, Stewart, R, Yoo, JA, Bae, KY, Jung, SW, Lee, MS, Yim, HW, Jun, TY (2011). Improvement within 2 weeks and later treatment outcomes in patients with depressive disorders: the CRESCEND study. Journal of Affective Disorders 129, 183–190.CrossRefGoogle ScholarPubMed
Klomp, A, van Wingen, G, de Ruiter, MB, Caan, MW, Denys, D, Reneman, L (2013). Test–retest reliability of task-related pharmacological MRI with a single-dose oral citalopram challenge. Neuroimage 75, 108–116.CrossRefGoogle ScholarPubMed
Komulainen, E, Heikkila, R, Meskanen, K, Raij, TT, Nummenmaa, L, Lahti, J, Jylha, P, Melartin, T, Harmer, CJ, Isometsa, E, Ekelund, J (2016). A single dose of mirtazapine attenuates neural responses to self-referential processing. Journal of Psychopharmacology 30, 23–32.CrossRefGoogle ScholarPubMed
Kraus, C, Ganger, S, Losak, J, Hahn, A, Savli, M, Kranz, GS, Baldinger, P, Windischberger, C, Kasper, S, Lanzenberger, R (2014). Gray matter and intrinsic network changes in the posterior cingulate cortex after selective serotonin reuptake inhibitor intake. Neuroimage 84, 236–244.CrossRefGoogle ScholarPubMed
Labuschagne, I, Croft, RJ, Phan, KL, Nathan, PJ (2010). Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: an event-related potential (ERP) investigation. Journal of Psychopharmacology 24, 1153–1164.CrossRefGoogle Scholar
Larsen, RS, Smith, IT, Miriyala, J, Han, JE, Corlew, RJ, Smith, SL, Philpot, BD (2014). Synapse-specific control of experience-dependent plasticity by presynaptic NMDA receptors. Neuron 83, 879–893.CrossRefGoogle ScholarPubMed
Liu, F, Guo, W, Liu, L, Long, Z, Ma, C, Xue, Z, Wang, Y, Li, J, Hu, M, Zhang, J (2013). Abnormal amplitude low-frequency oscillations in medication-naive, first-episode patients with major depressive disorder: a resting-state fMRI study. Journal of Affective Disorders 146, 401–406.CrossRefGoogle ScholarPubMed
Liu, J, Ren, L, Womer, FY, Wang, J, Fan, G, Jiang, W, Blumberg, HP, Tang, Y, Xu, K, Wang, F (2014). Alterations in amplitude of low frequency fluctuation in treatment-naïve major depressive disorder measured with resting-state fMRI. Human Brain Mapping 35, 4979–4988.CrossRefGoogle ScholarPubMed
Logothetis, NK, Pauls, J, Augath, M, Trinath, T, Oeltermann, A (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature 412, 150–157.CrossRefGoogle ScholarPubMed
Mantini, D, Perrucci, MG, Del Gratta, C, Romani, GL, Corbetta, M (2007). Electrophysiological signatures of resting state networks in the human brain. Proceedings of the National Academy of Sciences USA 104, 13170–13175.CrossRefGoogle ScholarPubMed
Mayberg, HS (1997). Limbic-cortical dysregulation: a proposed model of depression. Journal of Neuropsychiatry and Clinical Neurosciences 9, 471–81.Google ScholarPubMed
Mayberg, HS, Silva, JA, Brannan, SK, Tekell, JL, Mahurin, RK, McGinnis, S, Jerabek, PA (2002). The functional neuroanatomy of the placebo effect. American Journal of Psychiatry 159, 728–737.CrossRefGoogle ScholarPubMed
McBean, DE, Ritchie, IM, Olverman, HJ, Kelly, PA (1999). Effects of the specific serotonin reuptake inhibitor, citalopram, upon local cerebral blood flow and glucose utilisation in the rat. Brain Research 847, 80–84.CrossRefGoogle ScholarPubMed
Owens, MJ, Rosenbaum, JF (2002). Escitalopram: a second-generation SSRI. CNS Spectrums 7, 34–39.CrossRefGoogle ScholarPubMed
Palmer, SM, Crewther, SG, Carey, LM (2015). A meta-analysis of changes in brain activity in clinical depression. Frontiers in Human Neuroscience 8, 1045.CrossRefGoogle ScholarPubMed
Perkins, AM, Arnone, D, Smallwood, J, Mobbs, D (2015). Thinking too much: self-generated thought as the engine of neuroticism. Trends in Cognitive Science 19, 492–498.CrossRefGoogle ScholarPubMed
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003). Neurobiology of emotion perception II: implications for major psychiatric disorders. Biological Psychiatry 54, 515–528.CrossRefGoogle ScholarPubMed
Posner, J, Hellerstein, DJ, Gat, I, Mechling, A, Klahr, K, Wang, Z, McGrath, PJ, Stewart, JW, Peterson, BS (2013). Antidepressants normalize the default mode network in patients with dysthymia. JAMA Psychiatry 70, 373–382.CrossRefGoogle ScholarPubMed
Price, JL, Drevets, WC (2010). Neurocircuitry of mood disorders. Neuropsychopharmacology 35, 192–216.CrossRefGoogle ScholarPubMed
Pytliak, M, Vargova, V, Mechirova, V, Felsoci, M (2011). Serotonin receptors - from molecular biology to clinical applications. Physiological Research 60, 15–25.CrossRefGoogle ScholarPubMed
Qi, R, Zhang, L, Wu, S, Zhong, J, Zhang, Z, Zhong, Y, Ni, L, Zhang, Z, Li, K, Jiao, Q (2012). Altered resting-state brain activity at functional MR imaging during the progression of hepatic encephalopathy. Radiology 264, 187–195.CrossRefGoogle ScholarPubMed
Quirk, GJ, Beer, JS (2006). Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Current Opinion in Neurobiology 16, 723–727.CrossRefGoogle ScholarPubMed
Rauch, A, Rainer, G, Logothetis, NK (2008). The effect of a serotonin-induced dissociation between spiking and perisynaptic activity on BOLD functional MRI. Proceedings of the National Academy of Sciences USA 105, 6759–6764.CrossRefGoogle ScholarPubMed
Rive, MM, van Rooijen, G, Veltman, DJ, Phillips, ML, Schene, AH, Ruhe, HG (2013). Neural correlates of dysfunctional emotion regulation in major depressive disorder. A systematic review of neuroimaging studies. Neuroscience & Biobehavioral Reviews 37, 2529–2553.CrossRefGoogle ScholarPubMed
Robinson, OJ, Overstreet, C, Allen, PS, Letkiewicz, A, Vytal, K, Pine, DS, Grillon, C (2013). The role of serotonin in the neurocircuitry of negative affective bias: serotonergic modulation of the dorsal medial prefrontal-amygdala ‘aversive amplification'circuit. Neuroimage 78, 217–223.CrossRefGoogle ScholarPubMed
Rush, A, Trivedi, M, Wisniewski, S, Nierenberg, A, Stewart, J, Warden, D, Niederehe, G, Thase, M, Lavori, P, Lebowitz, B (2006). Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR* D report. American Journal of Psychiatry 163, 1905–1917.CrossRefGoogle ScholarPubMed
Schölvinck, ML, Maier, A, Frank, QY, Duyn, JH, Leopold, DA (2010). Neural basis of global resting-state fMRI activity. Proceedings of the National Academy of Sciences USA 107, 10238–10243.CrossRefGoogle ScholarPubMed
Schwarz, AJ, Gozzi, A, Reese, T, Bifone, A (2007). In vivo mapping of functional connectivity in neurotransmitter systems using pharmacological MRI. Neuroimage 34, 1627–1636.CrossRefGoogle ScholarPubMed
Sheline, YI, Barch, DM, Price, JL, Rundle, MM, Vaishnavi, SN, Snyder, AZ, Mintun, MA, Wang, S, Coalson, RS, Raichle, ME (2009). The default mode network and self-referential processes in depression. Proceedings of the National Academy of Sciences USA 106, 1942–1947.CrossRefGoogle ScholarPubMed
Späti, J, Hänggi, J, Doerig, N, Ernst, J, Sambataro, F, Brakowski, J, Jäncke, L, grosse Holtforth, M, Seifritz, E, Spinelli, S (2015). Prefrontal thinning affects functional connectivity and regional homogeneity of the anterior cingulate cortex in depression. Neuropsychopharmacology 40, 1640–1648.CrossRefGoogle ScholarPubMed
Taylor, MJ, Freemantle, N, Geddes, JR, Bhagwagar, Z (2006). Early onset of selective serotonin reuptake inhibitor antidepressant action: systematic review and meta-analysis. Archives of General Psychiatry 63, 1217–1223.CrossRefGoogle ScholarPubMed
van de Ven, V, Wingen, M, Kuypers, KP, Ramaekers, JG, Formisano, E (2013). Escitalopram decreases cross-regional functional connectivity within the default-mode network. PLoS ONE 8, e68355.CrossRefGoogle ScholarPubMed
Wang, L, Li, K, Zhang, Q, Zeng, Y, Dai, W, Su, Y, Wang, G, Tan, Y, Jin, Z, Yu, X (2014 a). Short-term effects of escitalopram on regional brain function in first-episode drug-naive patients with major depressive disorder assessed by resting-state functional magnetic resonance imaging. Psychological Medicine 44, 1417–1426.CrossRefGoogle ScholarPubMed
Wang, LJ, Kuang, WH, Xu, JJ, Lei, D, Yang, YC (2014 b). Resting-state brain activation correlates with short-time antidepressant treatment outcome in drug-naive patients with major depressive disorder. Journal of International Medical Research 42, 966–975.CrossRefGoogle ScholarPubMed
Wise, T, Radua, J, Via, E, Cardoner, N, Abe, O, Adams, TM, Amico, F, Cheng, Y, Cole, JH, de Azevedo Marques Perico, C, Dickstein, DP, Farrow, TF, Frodl, T, Wagner, G, Gotlib, IH, Gruber, O, Ham, BJ, Job, DE, Kempton, MJ, Kim, MJ, Koolschijn, PC, Malhi, GS, Mataix-Cols, D, McIntosh, AM, Nugent, AC, O'Brien, JT, Pezzoli, S, Phillips, ML, Sachdev, PS, Salvadore, G, Selvaraj, S, Stanfield, AC, Thomas, AJ, van Tol, MJ, van der Wee, NJ, Veltman, DJ, Young, AH, Fu, CH, Cleare, AJ, Arnone, D (in press). Common and distinct patterns of grey-matter volume alteration in major depression and bipolar disorder: evidence from voxel-based meta-analysis. Molecular Psychiatry.Google Scholar
Wong, JJ, O'Daly, O, Mehta, MA, Young, AH, Stone, JM (2016). Ketamine modulates subgenual cingulate connectivity with the memory-related neural circuit-a mechanism of relevance to resistant depression? PeerJ 4, e1710.CrossRefGoogle ScholarPubMed
Yamamura, T, Okamoto, Y, Okada, G, Takaishi, Y, Takamura, M, Mantani, A, Kurata, A, Otagaki, Y, Yamashita, H, Yamawaki, S (2016). Association of thalamic hyperactivity with treatment-resistant depression and poor response in early treatment for major depression: a resting-state fMRI study using fractional amplitude of low-frequency fluctuations. Translational Psychiatry 6, e754.CrossRefGoogle ScholarPubMed
Yu-Feng, Z, Yong, H, Chao-Zhe, Z, Qing-Jiu, C, Man-Qiu, S, Meng, L, Li-Xia, T, Tian-Zi, J, Yu-Feng, W (2007). Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain and Development 29, 83–91.CrossRefGoogle Scholar
Zhou, Y, Wang, K, Liu, Y, Song, M, Song, SW, Jiang, T (2010). Spontaneous brain activity observed with functional magnetic resonance imaging as a potential biomarker in neuropsychiatric disorders. Cognitive Neurodynamics 4, 275–294.CrossRefGoogle ScholarPubMed
Zou, QH, Zhu, CZ, Yang, Y, Zuo, XN, Long, XY, Cao, QJ, Wang, YF, Zang, YF (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
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