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Inflammatory insults and mental health consequences: does timing matter when it comes to depression?

  • A. Du Preez (a1), J. Leveson (a1), P. A. Zunszain (a1) and C. M. Pariante (a1)

Abstract

It has become widely accepted that the immune system, and specifically increased levels of inflammation, play a role in the development of depression. However, not everyone with increased inflammation develops depression, and as with all other diseases, there are risk factors that may contribute to an increased vulnerability in certain individuals. One such risk factor could be the timing of an inflammatory exposure. Here, using a combination of PubMed, EMBASE, Ovid Medline and PsycINFO, we systematically reviewed whether exposure to medically related inflammation in utero, in childhood, and in adolescence, increases the risk for depression in adulthood. Moreover, we tried to determine whether there was sufficient evidence to identify a particular time point during the developmental trajectory in which an immune insult could be more damaging. While animal research shows that early life exposure to inflammation increases susceptibility to anxiety- and depressive-like behaviour, human studies surprisingly find little evidence to support the notion that medically related inflammation in utero and in adolescence contributes to an increased risk of developing depression in later life. However, we did find an association between childhood inflammation and later life depression, with most studies reporting a significantly increased risk of depression in adults who were exposed to inflammation as children. More robust clinical research, measuring direct markers of inflammation throughout the life course, is greatly needed to expand on, and definitively address, the important research questions raised in this review.

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This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

*Address for correspondence: A. Du Preez, MSc, BSc, Department of Psychological Medicine, Stress, Psychiatry and Immunology Laboratory, Institute of Psychiatry, King's College London, The James Black Centre, 125 Coldharbour Lane, London, SE5 9NU, UK. (Email: andrea.du_preez@kcl.ac.uk)

References

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Aaltonen, R, Heikkinen, T, Hakala, K, Laine, K, Alanen, A (2005). Transfer of proinflammatory cytokines across term placenta. Obstetrics and Gynecology 106, 802807.
Allan, CK, Newburger, JW, McGarth, E, Elder, J, Psoinos, C, Laussen, PC, del Nido, PJ, Wypij, D, McGowen, FX Jr. (2010). The relationship between inflammatory activation and clinical outcome after infant cardiopulmonary bypass. Anesthesia Analgesia 111, 12441251.
Anderson, SE, Cohen, P, Naumova, EN, Jacques, PF, Must, A (2007). Adolescent obesity and risk for subsequent major depressive disorder and anxiety disorder: prospective evidence. Psychosomatic Medicine 69, 740747.
Areias, MEG, Pinto, CI, Vieira, PF, Teixeira, F, Coelho, R, Freitas, I, Matos, S, Castro, M, Sarmento, S, Viana, V, Quintas, J, Areias, JC (2013). Long term psychosocial outcomes of congenital heart disease in adolescents and young adults. Chinese Journal of Contemporary Pediatrics 15, 810816.
Betts, KS, Williams, GM, Najman, JM, Alati, R (2015). The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems. Depression and Anxiety 32, 8290.
Biaggi, A, Conroy, S, Pawlby, S, Pariante, CM (2016). Identifying the women at risk of antenatal anxiety and depression: a systematic review. Journal of Affective Disorders 191, 6277.
Bilbo, SD, Levkoff, LH, Mahoney, JH, Watkins, LR, Rudy, JW, Maier, SF (2005). Neonatal infection induces memory impairments following an immune challenge in adulthood. Behavioral Neuroscience 119, 293301.
Bonaccorso, S, Marino, V, Biondi, M, Grimaldi, F, Ippoliti, F, Maes, M (2002). Depression induced by treatment with interferon-alpha in patients affected by hepatitis C virus. Journal of Affective Disorders 72, 237241.
Bosch, NM, Riese, H, Reijneveld, Sa., Bakker, MP, Verhulst, FC, Ormel, J, Oldehinkel, AJ (2012). Timing matters: long term effects of adversities from prenatal period up to adolescence on adolescents’ cortisol stress response. The TRAILS study. Psychoneuroendocrinology 37, 14391447.
Brown, AS, Susser, ES, Lin, SP, Gorman, JM (1995). Affective disorders in Holland after prenatal exposure to the 1957 A2 influenza epidemic. Biological Psychiatry 38, 270273.
Bufalino, C, Hepgul, N, Aguglia, E, Pariante, CM (2013). The role of immune genes in the association between depression and inflammation: a review of recent clinical studies. Brain, Behavior, and Immunity 31, 3147.
Calle, MC, Fernandez, ML (2012). Inflammation and type 2 diabetes. Diabetes & Metabolism 38, 183191.
Capuron, L, Ravaud, A, Gualde, N, Bosmans, E, Dantzer, R, Maes, M, Neveu, PJ (2001). Association between immune activation and early depressive symptoms in cancer patients treated with interleukin-2-based therapy. Psychoneuroendocrinology 26, 797808.
Chen, MH, Su, TP, Chen, YS, Hsu, JW, Huang, KL, Chang, WH, Bai, YM (2013). Allergic rhinitis in adolescence increases the risk of depression in later life: a nationwide population-based prospective cohort study. Journal of Affective Disorders 145, 4953.
Chovatiya, R, Medzhitov, R (2014). Stress, inflammation, and defense of homeostasis. Molecular Cell 54, 281288.
Clark, C, Caldwell, T, Power, C, Stansfeld, SA (2010). Does the influence of childhood adversity on psychopathology persist across the lifecourse? A 45-year prospective epidemiologic study. Annals of Epidemiology 20, 385394.
Cohen, P, Pine, DS, Must, A, Kasen, S, Brook, J (1998). Prospective associations between somatic illness and mental illness from childhood to adulthood. American Journal of Epidemiology 147, 232239.
Colman, I, Jones, PB, Kuh, D, Weeks, M, Naicker, K, Richards, M, Croudace, TJ (2014). Early development, stress and depression across the life course: pathways to depression in a national British birth cohort. Psychological Medicine 44, 28452854.
de Jong, AJ, Kloppenburg, M, Toes, REM, Ioan-Facsinay, A (2014). Fatty acids, lipid mediators, and T-cell function. Frontiers in Immunology 5, 39.
Dietert, RR, Etzel, RA, Chen, D, Halonen, M, Holladay, SD, Jarabek, AM, Peden, LDB, Pinkerton, K, Smialowicz, RJ, Zoetis, T (2000). Workshop to identify critical windows of exposure for children's health: immune and respiratory systems work group summary. Environmental Health Perspectives 108, 483490.
Dietert, RR (2013). Developmental immunotoxicity, perinatal programming, and non-communicable diseases: focus on human studies. Advances in Medicine 2014, 118.
Donath, MY, Shoelson, SE (2011). Type 2 diabetes as an inflammatory disease. Nature Reviews. Immunology 11, 98107.
Ferro, MA, Boyle, MH (2015). The impact of chronic physical illness, maternal depressive symptoms, family functioning, and self-esteem on symptoms of anxiety and depression in children. Journal of Abnormal Child Psychology 43, 177187.
Galic, MA, Riazi, K, Heida, JG, Mouihate, A, Fournier, NM, Spencer, SJ, Kalynchuk, LE, Teskey, GC, Pittman, QJ (2008). Postnatal inflammation increases seizure susceptibility in adult rats. Journal of Neuroscience 28, 69046913.
Gaughan, DM, Hughes, MD, Oleske, JM, Malee, K, Carol, A, Nachman, S, Malee, K, Gore, CA, Nachman, S (2004). Psychiatric hospitalizations among children and youths with human immunodeficiency virus infection. Pediatrics 113, 544551.
Goodwin, RD (2011). Association between infection early in life and mental disorders among youth in the community: a cross-sectional study. BMC Public Health 11, 878.
Gunnar, MR, Brodersen, L, Krueger, K, Rigatuso, J (1996). Dampening of adrenocortical responses during infancy: normative changes and individual differences. Child Development 67, 877889.
Gunnar, MR, Donzella, B (2002). Social regulation of the cortisol levels in early human development. Psychoneuroendocrinology 27, 199220.
Hannet, I, Erkeller-Yuksel, F, Lydyard, P, Debruy, M (1992). Developmental and maturational changes in human blood lymphocyte subpopulations. Immunology Today 13, 215218.
Hansson, G (2005). Inflammation, atherosclerosis, and coronary artery disease. New England Journal of Medicine 352, 16851695.
Hare, DL, Toukhsati, SR, Johansson, P, Jaarsma, T (2014). Depression and cardiovascular disease: a clinical review. European Heart Journal 35, 13651372.
Haroon, E, Raison, CL, Miller, AH (2012). Psychoneuroimmunology meets Neuropsychopharmacology: translational implications of the impact of inflammation on behavior. Neuropsychopharmacology 37, 137162.
Herva, A, Laitinen, J, Miettunen, J, Veijola, J, Karvonen, JT, Läksy, K, Joukamaa, M (2006). Obesity and depression: results from the longitudinal Northern Finland 1966 Birth Cohort Study. International Journal of Obesity 30, 520527.
Holladay, SD, Smialowicz, RJ (2000). Development of the murine and human immune system: differential effects of immunotoxicants depend on time of exposure. Environmental Health Perspectives 108, 463473.
Holt, PG, Jones, CA (2000). The development of the immune system during pregnancy and early life. Allergy 55, 688697.
Horikawa, N, Yamazaki, T, Izumi, N, Uchihara, M (2003). Incidence and clinical course of major depression in patients with chronic hepatitis type C undergoing interferon-alpha therapy: a prospective study. General Hospital Psychiatry 25, 3438.
Jacobson, AM, Hauser, ST, Willett, JB, Wolfsdorf, JI, Dvorak, R, Herman, L, de Groot, M (1997). Psychological Adjustment to IDDM: 10 year follow-up of an onset cohort of child and adolescent patients. Diabetes Care 20, 811818.
Johnson, MH (2001). Functional brain development in humans. Nature Reviews. Neuroscience 2, 475483.
Kalmakis, KA, Chandler, GE (2015). Health consequences of adverse childhood experiences: a systematic review. Journal of the American Association of Nurse Practitioners 27, 457465.
Kessler, RC, Berglund, P, Demler, O, Jin, R, Merikangas, KR, Walters, EE (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Archives of General Psychiatry 62, 593602.
Khandaker, GM, Pearson, RM, Zammit, S, Lewis, G, Jones, PB (2014). Association of serum interleukin 6 and C-reactive protein in childhood with depression and psychosis in young adult life. JAMA Psychiatry 71, 11211128.
Kiecolt-Glaser, JK, Derry, HM, Fagundes, CP (2015). Inflammation: depression fans the flames and feasts on the heat. American Journal of Psychiatry 72, 10751091.
Knuesel, I, Chicha, L, Britschgi, M, Schobel, SA, Bodmer, M, Hellings, JA, Toovey, S, Prinssen, EP (2014). Maternal immune activation and abnormal brain development across CNS disorders. Nature Reviews Neurology 10, 643660.
Kokkonen, J, Kokkonen, ER (1993). Prevalence of mental disorders in young adults with chronic physical diseases since childhood as identified by the Present State Examination and the CATEGO program. Acta Psychiatrica Scandinavica 87, 239243.
Kovacs, M, Goldston, D, Obrosky, DS, Scott, MS, Bonar, LK (1997). Psychiatric disorders in youths with T1D: rates and risk factors. Diabetes Care 20, 3644.
Kredel, LI, Siegmund, B (2014). Adipose-tissue and intestinal inflammation – visceral obesity and creeping fat. Frontiers in Immunology 5, 112.
Larson, MC, White, BP, Cochran, A, Donzella, B, Gunnar, M (1998). Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. Developmental Psychobiology 33, 327337.
Lašaitė, L, Ostrauskas, R, Žalinkevičius, R, Jurgevičienė, NRL (2015). Profile of mood states in adult type 1 diabetes mellitus men and women with disease onset in childhood and in adulthood. Journal of Pediatric Endocrinology and Metabolism 28, 279285.
Leckman-Westin, E, Cohen, PR, Stueve, A (2009). Maternal depression and mother–child interaction patterns: association with toddler problems and continuity of effects to late childhood. Journal of Child Psychology and Psychiatry 50, 11761184.
Lin, PY, Su, KP (2007). A meta-analytic review of double-blind, placebo-controlled trials of antidepressant efficacy of omega-3 fatty acids. Journal of Clinical Psychiatry 68, 10561061.
Lindert, J, Von Ehrenstein, OS, Grashow, R, Gal, G, Braehler, E, Weisskopf, MG (2014). Sexual and physical abuse in childhood is associated with depression and anxiety over the life course: systematic review and meta-analysis. International Journal of Public Health 59, 359372.
Loftis, JM, Hauser, P (2004). The phenomenology and treatment of interferon-induced depression. Journal of Affective Disorders 82, 175–90.
Luppino, FS, De Wit, LM, Bouvy, PF, Stijnen, T, Cuijpers, P, Penninx, BWJH, Zitman, FG (2015). Overweight, obesity, and depression. Archives of General Psychiatry 67, 220229.
Machón, RA, Mednick, SA, Huttunen, MO (1997). Adult major affective disorder after prenatal exposure to an influenza epidemic. Archives of General Psychiatry 54, 322328.
Mangge, H (2014). Antioxidants, inflammation and cardiovascular disease. World Journal of Cardiology 6, 462.
Marmorstein, NR, Iacono, WG, Legrand, L (2014). Obesity and depression in adolescence and beyond: reciprocal risks. International Journal of Obesity (2005) 38, 906911.
Martins, JG, Bentsen, H, Puri, BK (2012). Eicosapentaenoic acid appears to be the key omega-3 fatty acid component associated with efficacy in major depressive disorder: a critique of Bloch and Hannestad and updated meta-analysis. Molecular Psychiatry 17, 11441149.
McLaughlin, KA, Gadermann, AM, Hwang, I, Sampson, NA, Al-Hamzawi, A, Andrade, LH, Angermeyer, MC, Benjet, C, Bromet, EJ, Bruffaerts, R, Caldas-de-Almeida, JM, De Girolamo, G, De Graaf, R, Florescu, S, Gureje, O, Haro, JM, Hinkov, HR, Horiguchi, I, Hu, C, Karam, AN, Kovess-Masfety, V, Lee, S, Murphy, SD, Nizamie, SH, Posada-Villa, J, Williams, DR, Kessler, RC (2012). Parent psychopathology and offspring mental disorders: results from the WHO World Mental Health Surveys. British Journal of Psychiatry 200, 290299.
Mellins, Ca, Smith, R, O'Driscoll, P, Magder, LS, Brouwers, P, Chase, C, Blasini, I, Hittleman, J, Llorente, A, Matzen, E (2003). High rates of behavioral problems in perinatally HIV-infected children are not linked to HIV disease. Pediatrics 111, 384393.
Mezuk, B, Eaton, WW, Albrecht, S, Golden, SH (2008). Depression and type 2 diabetes over the lifespan: a meta-analysis. Diabetes Care 31, 23832390.
Miller, AH, Raison, CL (2015). The role of inflammation in depression: from evolutionary imperative to modern treatment target. Nature Reviews Immunology 16, 2234.
Mino, Y, Oshima, I, Okagami, K (2000). Mood disorders and influenza epidemics in Japan. Psychiatry and Clinical Neurosciences 54, 5965.
Moriceau, S, Sullivan, RM (2007). Neurobiology of infant attachment. Developmental Psychobiology 47, 230242.
Nabi, H, Kivimäki, M, Suominen, S, Koskenvuo, M, Singh-Manoux, A, Vahtera, J (2010). Does depression predict coronary heart disease and cerebrovascular disease equally well? The health and social support prospective cohort study. International Journal of Epidemiology 39, 10161024.
Nomura, Y, Marks, DJ, Grossman, B, Yoon, M, Loudon, H, Stone, J, Halperin, JM (2012). Exposure to gestational diabetes mellitus and low socioeconomic status: effects on neurocognitive development and risk of attention-deficit/hyperactivity disorder in offspring. Archives of Pediatrics and Adolescent Medicine 166, 337343.
Osugi, Y, Hara, J, Kurahashi, H, Sakata, N, Inoue, M, Yumura-Yagi, K, Kawa-Ha, K, Okada, S, Tawa, A (1995). Age-related changes in surface antigens on peripheral lymphocytes of healthy children. Clinical and Experimental Immunology 100, 543548.
Packham, JC, Hall, MA, Pimm, TJ (2002). Long-term follow-up of 246 adults with juvenile idiopathic arthritis: social function, relationships and sexual activity. Rheumatology (Oxford, England) 41, 14401443.
Pang, D, Syed, S, Fine, P, Jones, PB (2009). No association between prenatal viral infection and depression in later life - A long-term cohort study of 6152 subjects. Canadian Journal of Psychiatry 54, 565570.
Pariante, CM, Lightman, SL (2008). The HPA axis in major depression: classical theories and new developments. Trends in Neurosciences 31, 464468.
Pawlby, S, Hay, D, Sharp, D, Cerith, SW, Pariante, CM (2011). Antenatal depression and offspring psychopathology: the influence of childhood maltreatment. British Journal of Psychiatry 199, 106112.
Payne, J (2014). State of the science: stress, inflammation, and cancer. Oncology Nursing Forum 41, 533540.
Plant, DT, Pariante, CM, Sharp, D, Pawlby, S (2015). Maternal depression during pregnancy and offspring depression in adulthood: role of child maltreatment. British Journal of Psychiatry 207, 213220.
Pless, IB, Cripps, Ha, Davies, JM, Wadsworth, ME (1989). Chronic physical illness in childhood: psychological and social effects in adolescence and adult life. Developmental Medicine and Child Neurology 31, 746755.
Räikkönen, K, Pesonen, A-K, Heinonen, K, Kajantie, E, Hovi, P, Järvenpää, A-L, Eriksson, JG, Andersson, S (2008). Depression in young adults with very low birth weight: the Helsinki study of very low-birth-weight adults. Archives of General Psychiatry 65, 290296.
Raison, CL, Demetrashvili, M, Capuron, L, Miller, AH (2005). Neuropsychiatric adverse effects of interferon-alpha: recognition and management. CNS Drugs 19, 105123.
Rice, D, Barone, S Jr. (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental Health Perspectives 108, 511533.
Rivest, S (2010). Interactions between the immune and neuroendocrine systems. Progress in Brain Research 181, 4353.
Roque, S, Mesquita, AR, Palha, JA, Sousa, N, Correia-Neves, M (2014). The behavioral and immunological impact of maternal separation: a matter of timing. Frontiers in Behavioral Neuroscience 8, 192.
Roxburgh, CSD, McMillan, DC (2014). Cancer and systemic inflammation: treat the tumour and treat the host. British Journal of Cancer 110, 1409–12.
Roza, SJ, Sc, M, Hofstra, MB, Van Der Ende, J, Verhulst, FC (2003). Stable prediction of mood and anxiety disorders based on behavioral and emotional problems in childhood: adolescence, and young adulthood. American Journal of Psychiatry 160, 21162121.
Sapolsky, RM, Meaney, MJ (1986). Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Research Reviews 11, 6576.
Sharma, R, Bolger, AP, Li, W, Davlouros, PA, Volk, H-D, Poole-Wilson, Pa, Coats, AJS, Gatzoulis, MA, Anker, SD (2003). Elevated circulating levels of inflammatory cytokines and bacterial endotoxin in adults with congenital heart disease. American Journal of Cardiology 92, 188193.
Shelton, RC, Miller, AH (2011). Inflammation in depression: is adiposity a cause? Dialogues in Clinical Neuroscience 13, 4153.
Simopoulos, AP (2002). Omega-3 fatty acids in inflammation and autoimmune diseases. Journal of the American College of Nutrition 21, 495505.
Slavich, GM, Irwin, MR (2014). From stress to inflammation and major depressive disorder: a social signal transduction theory of depression. Psychological Bulletin 140, 774815.
Slykerman, RF, Thompson, J, Waldie, K, Murphy, R, Wall, C, Mitchell, EA (2015). Maternal stress during pregnancy is associated with moderate to severe depression in 11-year-old children. Acta Paediatrica 104, 6874.
Spencer, SJ, Galic, MA, Pittman, QJ (2011). Neonatal programming of innate immune function. American Journal of Physiology. Endocrinology and Metabolism 300, E11E18.
Spencer, SJ, Martin, S, Mouihate, A, Pittman, QJ (2006). Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge. Neuropsychopharmacology 31, 19101918.
Strawbridge, R, Arnone, D, Danese, A, Papadopoulos, A, Herane Vives, A, Cleare, AJ (2015). Inflammation and clinical response to treatment in depression: a meta-analysis. European Neuropsychopharmacology 25, 15321543.
Sublette, EM, Ellis, SP, Geant, AL, Mann, JJ (2011). Meta-analysis: effects of eicosapentaenoic acid in clinical trials in depression. Journal of Clinical Psychiatry 72, 15771584.
Trotta, A, Murray, RM, Fisher, HL (2015). The impact of childhood adversity on the persistence of psychotic symptoms: a systematic review and meta-analysis. Psychological Medicine 45, 24812498.
Tuovinen, S, Räikkönen, K, Kajantie, E, Pesonen, AK, Heinonen, K, Osmond, C, Barker, DJP, Eriksson, JG (2010). Depressive symptoms in adulthood and intrauterine exposure to pre-eclampsia: The Helsinki birth cohort study. British Journal of Obstetrics and Gynaecology 117, 12361242.
Turecki, G, Ota, VK, Belangero, SI, Jackowski, A, Kaufman, J (2014). Early life adversity, genomic plasticity, and psychopathology. Lancet Psychiatry 1, 461466.
Valkanova, V, Ebmeier, KP, Allan, CL (2013). CRP, IL-6 and depression: a systematic review and meta-analysis of longitudinal studies. Journal of Affective Disorders 150, 736744.
Visser, HA, van Minnen, A, van Megen, H, Eikelenboom, M, Hoogendoorn, AW, Kaarsemaker, M, Balkom, AJ, van Oppen, P (2014). The relationship between adverse childhood experiences and symptom severity, chronicity, and comorbidity in patients with obsessive-compulsive disorder. Journal of Clinical Psychiatry 75, 10341039.
Walker, AK, Nakamura, T, Byrne, RJ, Naicker, S, Tynan, RJ, Hunter, M, Hodgson, DM (2009). Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology 34, 15151525.
Walker, FR, Hodyl, NA, Krivanek, KM, Hodgson, DM (2006). Early life host-bacteria relations and development: long-term individual differences in neuroimmune function following neonatal endotoxin challenge. Physiology & Behavior 87, 126134.
Walker, FR, Knott, B, Hodgson, DM (2008). Neonatal endotoxin exposure modifies the acoustic startle response and circulating levels of corticosterone in the adult rat but only following acute stress. Journal of Psychiatric Research 42, 10941103.
Walker, FR, March, J, Hodgson, DM (2004). Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat. Behavioural Brain Research 154, 6369.
Xu, G, Jing, J, Bowers, K, Liu, B, Bao, W (2014). Maternal diabetes and the risk of autism spectrum disorders in the offspring: a systematic review and meta-analysis. Journal of Autism and Developmental Disorders 44, 766775.
Zaretsky, MV, Alexander, JM, Byrd, W, Bawdon, RE (2004). Transfer of inflammatory cytokines across the placenta. Obstetrics and Gynecology 103, 546550.
Zunszain, PA, Anacker, C, Cattaneo, A, Carvalho, LA, Parainte, CM (2011). Glucocorticoids, cytokines and brain abnormalities in depression. Progress in Neuropsychopharmacology and Biological Psychiatry 35, 722729.
Zunszain, PA, Hepgul, N, Pariante, CM (2013). Inflammation and depression. Current Topics in Behavioural Neurosciences 14, 135151.

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