Neural correlates of improved executive function following erythropoietin treatment in mood disorders

Psychological Medicine

Volumn 46, Issue 8, 2016, Pages 1679-1691

  Miskowiak, K W ^a,b   Vinberg, M ^a   Glerup, L ^a   Paulson, O B ^a,b   Knudsen, G M ^a   Ehrenreich, H ^d   Harmer, C J ^e   Kessing, L V ^a   Siebner, H R ^a,b,c   Macoveanu, J ^a,b  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c BISPEBJERG HOSPITAL   (Denmark)

^d MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Bipolar disorder; cognition; dorsolateral prefrontal cortex; EPO; erythropoietin; executive function; fMRI; treatment resistant depression

Indexed keywords

ERYTHROPOIETIN;

ADULT; BIPOLAR DISORDER; BRAIN; COGNITIVE DEFECT; CONTROLLED STUDY; DIAGNOSTIC IMAGING; DOUBLE BLIND PROCEDURE; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; MAJOR DEPRESSION; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PSYCHOLOGY; RANDOMIZED CONTROLLED TRIAL; SHORT TERM MEMORY; SPATIAL MEMORY; TREATMENT OUTCOME; TREATMENT RESISTANT DEPRESSION;

ADULT; BIPOLAR DISORDER; BRAIN; COGNITIVE DYSFUNCTION; DEPRESSIVE DISORDER, MAJOR; DEPRESSIVE DISORDER, TREATMENT-RESISTANT; DOUBLE-BLIND METHOD; ERYTHROPOIETIN; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; SPATIAL MEMORY; TREATMENT OUTCOME;

EID: 84961392064     PISSN: 00332917     EISSN: 14698978     Source Type: Journal    
DOI: 10.1017/S0033291716000209     Document Type: Article

References (51)

1. Bora E, Harrison BJ, Yucel M, Pantelis C (2013). Cognitive impairment in euthymic major depressive disorder: A meta-analysis. Psychological Medicine 43, 2017-2026.
2. Bourne C, Aydemir O, Balanza-Martinez V, Bora E, Brissos S, Cavanagh JT, Clark L, Cubukcuoglu Z, Dias VV, Dittmann S, Ferrier IN, Fleck DE, Frangou S, Gallagher P, Jones L, Kieseppa T, Martinez-Aran A, Melle I, Moore PB, Mur M, Pfennig A, Raust A, Senturk V, Simonsen C, Smith DJ, Bio DS, Soeiro-de-Souza MG, Stoddart SD, Sundet K, Szoke A, Thompson JM, Torrent C, Zalla T, Craddock N, Andreassen OA, Leboyer M, Vieta E, Bauer M, Worhunsky PD, Tzagarakis C, Rogers RD, Geddes JR, Goodwin GM (2013). Neuropsychological testing of cognitive impairment in euthymic bipolar disorder: An individual patient data meta-analysis. Acta Psychiatrica Scandinavica 128, 149-162.
3. Brines ML, Ghezzi P, Keenan S, Agnello D, de Lanerolle NC, Cerami C, Itri LM, Cerami A (2000). Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proceedings of the National Academy of Sciences USA 97, 10526-10531.
4. Callicott JH, Mattay VS, Bertolino A, Finn K, Coppola R, Frank JA, Goldberg TE, Weinberger DR (1999). Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cerebral Cortex 9, 20-26.
5. Carlson PJ, Singh JB, Zarate Jr. CA, Drevets WC, Manji HK (2006). Neural circuitry and neuroplasticity inmood disorders: insights for novel therapeutic targets. NeuroRx 3, 22-41.
6. Demant KM, Almer GM, Vinberg M, Kessing LV, Miskowiak KW (2013). Effects of cognitive remediation on cognitive dysfunction in partially or fully remitted patients with bipolar disorder: study protocol for a randomized controlled trial. Trials 14, 378.
7. Demant KM, Vinberg M, Kessing LV, Miskowiak KW (2015). Effects of cognitive remediation on cognitive dysfunction in partially or fully remitted individuals with bipolar disorder: results of a randomised controlled trial. PLoS ONE 10, e0127955.
8. Depp CA, Mausbach BT, Harmell AL, Savla GN, Bowie CR, Harvey PD, Patterson TL (2012). Meta-analysis of the association between cognitive abilities and everyday functioning in bipolar disorder. Bipolar Disorder 14, 217-226.
9. Dias VV, Balanza-Martinez V, Soeiro-de-Souza MG, Moreno RA, Figueira ML, Machado-Vieira R, Vieta E (2012). Pharmacological approaches in bipolar disorder and the impact on cognition: A critical overview. Acta Psychiatrica Scandinavica 126, 315-331.
10. Ehrenreich H, Degner D, Meller J, Brines M, Béhé M, Hasselblatt M, Woldt H, Falkai P, Knerlich F, Jacob S, von Ahsen N, Maier W, Brück W, Rüther E, Cerami A, Becker W, Sirén AL (2004). Erythropoietin: A candidate compound for neuroprotection in schizophrenia. Molecular Psychiatry 9, 42-54.
11. Ehrenreich H, Fischer B, Norra C, Schellenberger F, Stender N, Stiefel M, Siren AL, Paulus W, Nave KA, Gold R, Bartels C (2007a). Exploring recombinant human erythropoietin in chronic progressive multiple sclerosis. Brain 130, 2577-2588.
12. Ehrenreich H, Hinze-Selch D, Stawicki S, Aust C, Knolle-Veentjer S, Wilms S, Heinz G, Erdag S, Jahn H, Degner D, Ritzen M, Mohr A, Wagner M, Schneider U, Bohn M, Huber M, Czernik A, Pollmacher T, Maier W, Siren AL, Klosterkotter J, Falkai P, Ruther E, Aldenhoff JB, Krampe H (2007b). Improvement of cognitive functions in chronic schizophrenic patients by recombinant human erythropoietin. Molecular Psychiatry 12, 206-220.
13. Fernandez-Corcuera P, Salvador R, Monte GC, Salvador SS, Goikolea JM, Amann B, Moro N, Sans-Sansa B, Ortiz-Gil J, Vieta E, Maristany T, McKenna PJ, Pomarol-Clotet E (2013). Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. Journal of Affective Disorder 148, 170-178.
14. Filippi M, Riccitelli G, Mattioli F, Capra R, Stampatori C, Pagani E, Valsasina P, Copetti M, Falini A, Comi G, Rocca MA (2012). Multiple sclerosis: effects of cognitive rehabilitation on structural and functional MR imaging measures-an explorative study. Radiology 262, 932-940.
15. Garrett A, Kelly R, Gomez R, Keller J, Schatzberg AF, Reiss AL (2011). Aberrant brain activation during a working memory task in psychotic major depression. American Journal of Psychiatry 168, 173-182.
16. Ge XH, Zhu GJ, Geng DQ, Zhang ZJ, Liu CF (2012). Erythropoietin attenuates 6-hydroxydopamine-induced apoptosis via glycogen synthase kinase 3beta-mediated mitochondrial translocation of Bax in PC12 cells. Neurological Sciences 33, 1249-1256.
17. Gonzalez-Castillo J, Roopchansingh V, Bandettini PA, Bodurka J (2011). Physiological noise effects on the flip angle selection in BOLD fMRI. Neuroimage 54, 2764-2778.
18. Grier JB (1971). Nonparametric indices for sensitivity and bias: computing formulas. Psychological Bulletin 75, 424-429.
19. Harvey PO, Fossati P, Pochon JB, Levy R, Lebastard G, Lehericy S, Allilaire JF, Dubois B (2005). Cognitive control and brain resources in major depression: An fMRI study using the n-back task. Neuroimage 26, 860-869.
20. Jaeger J, Berns S, Uzelac S, Davis-Conway S (2006). Neurocognitive deficits and disability in major depressive disorder. Psychiatry Research 145, 39-48.
21. Kastner A, Grube S, El-Kordi A, Stepniak B, Friedrichs H, Sargin D, Schwitulla J, Begemann M, Giegling I, Miskowiak KW, Sperling S, Hannke K, Ramin A, Heinrich R, Gefeller O, Nave KA, Rujescu D, Ehrenreich H (2012). Common variants of the genes encoding erythropoietin and its receptor modulate cognitive performance in schizophrenia. Molecular Medicine 18, 1029-1040.
22. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 1233-1239.
23. Marsden WN (2013). Synaptic plasticity in depression: molecular, cellular and functional correlates. Progress in Neuropsychopharmacology and Biological Psychiatry 43, 168-184.
24. Matsuo K, Glahn DC, Peluso MA, Hatch JP, Monkul ES, Najt P, Sanches M, Zamarripa F, Li J, Lancaster JL, Fox PT, Gao JH, Soares JC (2007). Prefrontal hyperactivation during working memory task in untreated individuals with major depressive disorder. Molecular Psychiatry 12, 158-166.
25. McDonald JH (2014). Handbook of Biological Statistics. Sparky House Publishing: Baltimore, Maryland.
26. Meusel LA, Hall GB, Fougere P, McKinnon MC, MacQueen GM (2013). Neural correlates of cognitive remediation in patients with mood disorders. Psychiatry Research 214, 142-152.
27. Miskowiak K, Inkster B, O'Sullivan U, Selvaraj S, Goodwin GM, Harmer CJ (2008). Differential effects of erythropoietin on neural and cognitive measures of executive function 3 and 7 days post-administration. Experimental Brain Research 184, 313-321.
28. Miskowiak K, O'Sullivan U, Harmer CJ (2007). Erythropoietin enhances hippocampal response during memory retrieval in humans. Journal of Neuroscience 27, 2788-2792.
29. Miskowiak KW, Ehrenreich H, Christensen EM, Kessing LV, Vinberg M (2014a). Recombinant human erythropoietin to target cognitive dysfunction in bipolar disorder: A double-blind, randomized, placebo-controlled phase 2 trial. Journal of Clinical Psychiatry 75, 1347-1355.
30. Miskowiak KW, Favaron E, Hafizi S, Inkster B, Goodwin GM, Cowen PJ, Harmer CJ (2009). Effects of erythropoietin on emotional processing biases in patients with major depression: An exploratory fMRI study. Psychopharmacology (Berlin) 207, 133-142.
31. Miskowiak KW, Glerup L, Vestbo C, Harmer CJ, Reinecke A, Macoveanu J, Siebner HR, Kessing LV, Vinberg M (2014b). Different neural and cognitive response to emotional faces in healthy monozygotic twins at risk of depression. Psychological Medicine 45, 1447-1458.
32. Miskowiak KW, Vinberg M, Christensen EM, Bukh JD, Harmer CJ, Ehrenreich H, Kessing LV (2014c). Recombinant human erythropoietin for treating treatment-resistant depression: A double-blind, randomized, placebo-controlled phase 2 trial. Neuropsychopharmacology 39, 1399-1408.
33. Miskowiak KW, Vinberg M, Harmer CJ, Ehrenreich H, Kessing LV (2012). Erythropoietin: A candidate treatment for mood symptoms and memory dysfunction in depression. Psychopharmacology (Berlin) 219, 687-698.
34. Miskowiak KW, Vinberg M, Harmer CJ, Ehrenreich H, Knudsen GM, Macoveanu J, Hansen AR, Paulson OB, Siebner HR, Kessing LV (2010). Effects of erythropoietin on depressive symptoms and neurocognitive deficits in depression and bipolar disorder. Trials 11, 97.
35. Miskowiak KW, Vinberg M, Macoveanu J, Ehrenreich H, Koster N, Inkster B, Paulson OB, Kessing LV, Skimminge A, Siebner HR (2015). Effects of Erythropoietin on Hippocampal Volume and Memory in Mood Disorders. Biological Psychiatry 78, 270-277.
36. Nathan PJ, Phan KL, Harmer CJ, Mehta MA, Bullmore ET (2014). Increasing pharmacological knowledge about human neurological and psychiatric disorders through functional neuroimaging and its application in drug discovery. Current Opinion in Pharmacology 14, 54-61.
37. Pomarol-Clotet E, Alonso-Lana S, Moro N, Sarro S, Bonnin MC, Goikolea JM, Fernandez-Corcuera P, Amann BL, Romaguera A, Vieta E, Blanch J, McKenna PJ, Salvador R (2015). Brain functional changes across the different phases of Bipolar disorder. British Journal of Psychiatry 206, 136-144.
38. Porter RJ, Bowie CR, Jordan J, Malhi GS (2013). Cognitive remediation as a treatment for major depression: A rationale, review of evidence and recommendations for future research. Australian and New Zealand Journal of Psychiatry 47, 1165-1175.
39. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences 98, 676-682.
40. Ramsay IS, MacDonald AW III (2015). Brain correlates of cognitive remediation in Schizophrenia: Activation likelihood analysis shows preliminary evidence of neural target engagement. Schizophrenia Bulletin 41, 1276-1284.
41. 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.
42. Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biological Psychiatry 61, 198-209.
43. Siren AL, Fasshauer T, Bartels C, Ehrenreich H (2009). Therapeutic potential of erythropoietin and its structural or functional variants in the nervous system. Neurotherapeutics 6, 108-127.
44. Subramaniam K, Luks TL, Garrett C, Chung C, Fisher M, Nagarajan S, Vinogradov S (2014). Intensive cognitive training in schizophrenia enhances working memory and associated prefrontal cortical efficiency in a manner that drives long-term functional gains. Neuroimage 99, 281-292.
45. Talairach J, Tournoux P (1988). Co-planar Stereotaxic Atlas of the Human Brain. Thieme: New York.
46. Townsend J, Bookheimer SY, Foland-Ross LC, Sugar CA, Altshuler LL (2010). fMRI abnormalities in dorsolateral prefrontal cortex during a working memory task in manic, euthymic and depressed bipolar subjects. Psychiatry Research 182, 22-29.
47. Wager TD, Smith EE (2003). Neuroimaging studies of working memory: A meta-analysis. Cognive, Affective and Behavioral Neuroscience 3, 255-274.
48. Wang R, Foniok T, Wamsteeker JI, Qiao M, Tomanek B, Vivanco RA, Tuor UI (2006). Transient blood pressure changes affect the functional magnetic resonance imaging detection of cerebral activation. Neuroimage 31, 1-11.
49. Woolrich MW, Behrens TE, Beckmann CF, Jenkinson M, Smith SM (2004). Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21, 1732-1747.
50. Worsley KJ (2001). In Functional MRI: An Introduction to Methods (ed. P. M. Jezzars, P. Matthews and S. M. Smith) pp. 251-270. Oxford University Press: Oxford.
51. Zandbelt BB, Gladwin TE, Raemaekers M, van BM, Neggers SF, Kahn RS, Ramsey NF, Vink M (2008). Within-subject variation in BOLD-fMRI signal changes across repeated measurements: quantification and implications for sample size. Neuroimage 42, 196-206.