Mouse psychosocial stress reduces motivation and cognitive function in operant reward tests: A model for reward pathology with effects of agomelatine

European Neuropsychopharmacology

Volumn 26, Issue 9, 2016, Pages 1448-1464

  Bergamini, Giorgio ^a,b   Cathomas, Flurin ^a   Auer, Sandra ^a   Sigrist, Hannes ^a   Seifritz, Erich ^a,b   Patterson, Michael ^c   Gabriel, Cecilia ^d   Pryce, Christopher R ^a,b  

^a UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^d IRIS Institut de Recherches Internationales Servier   (France)

Author keywords

Agomelatine; Animal model; Circadian rhythm; Decreased motivation; Depression; Operant

Indexed keywords

5-HYDROXYTRYPTAMINE2C RECEPTOR, MOUSE; ACETAMIDE DERIVATIVE; AGOMELATINE; ANTIDEPRESSANT AGENT; INDOLE DERIVATIVE; MELATONIN; PYRIDINE DERIVATIVE; S32006; SACCHARIN; SEROTONIN 2C RECEPTOR; SEROTONIN ANTAGONIST;

ANIMAL; ANIMAL MODEL; C57BL MOUSE; CIRCADIAN RHYTHM; DOMINANT-SUBORDINATE RELATIONSHIP; DRUG EFFECTS; DRUG THERAPY; FEEDING BEHAVIOR; INSTRUMENTAL CONDITIONING; LABORATORY AUTOMATION; MALE; MENTAL STRESS; METABOLISM; MOTIVATION; PHYSIOLOGY; REVERSAL LEARNING; REWARD; SUGAR INTAKE;

ACETAMIDES; ANIMALS; ANTIDEPRESSIVE AGENTS; AUTOMATION, LABORATORY; CIRCADIAN RHYTHM; CONDITIONING, OPERANT; DIETARY SUCROSE; DOMINANCE-SUBORDINATION; FEEDING BEHAVIOR; INDOLES; MALE; MELATONIN; MICE, INBRED C57BL; MODELS, ANIMAL; MOTIVATION; PYRIDINES; RECEPTOR, SEROTONIN, 5-HT2C; REVERSAL LEARNING; REWARD; SACCHARIN; SEROTONIN ANTAGONISTS; STRESS, PSYCHOLOGICAL;

EID: 84995543304     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2016.06.009     Document Type: Article

References (57)

1. Azzinnari, D., Sigrist, H., Staehli, S., Palme, R., Hildebrandt, T., Leparc, G., Hengerer, B., Seifritz, E., Pryce, C.R., Mouse social stress induces increased fear conditioning, helplessness and fatigue to physical challenge together with markers of altered immune and dopamine function. Neuropharmacology 85 (2014), 328–341.
2. Bari, A., Theobald, D.E., Caprioli, D., Mar, A.C., Aidoo-Micah, A., Dalley, J.W., Robbins, T.W., Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacol 35 (2010), 1290–1301.
3. Bergamini, G., Sigrist, H., Ferger, B., Singewald, N., Seifritz, E., Pryce, C.R., Depletion of nucleus accumbens dopamine leads to impaired reward and aversion processing in mice: relevance to motivation pathologies. Neuropharmacology 109 (2016), 306–319.
4. Bertaina-Anglade, V., Drieu la Rochelle, C., Boyer, P.-A., Mocaer, E., Antidepressant-like effects of agomelatine (S 20098) in the learned helplessness model. Behav. Pharmacol. 17 (2006), 703–713.
5. de Bodinat, C., Guardiola-Lemaitre, B., Mocaer, E., Renard, P., Munoz, C., Millan, M.J., Agomelatine, the first melatonergic antidepressant: discovery, characterization and development. Nat. Rev. Drug Discov. 9 (2010), 628–642.
6. Boulougouris, V., Glennon, J.C., Robbins, T.W., Dissociable effects of selective 5-HT2A and 5-HT2C receptor antagonists on serial spatial reversal learning in rats. Neuropsychopharmacol 33 (2008), 2007–2019.
7. Cathomas, F., Stegen, M., Sigrist, H., Schmid, L., Seifritz, E., Gassmann, M., Bettler, B., Pryce, C.R., Altered emotionality and neuronal excitability in mice lacking KCTD12, an auxillary subunit of GABAB receptors associated with mood disorders. Transl. Psychiatry, 5, 2015, e510., 10.1038/tp.2015.8.
8. Cathomas, F., Fuertig, R., Sigrist, H., Newman, G., Hoop, V., Bizzozzero, M., Mueller, A., Ceci, A., Hengerer, B., Seifritz, E., Fontana, A., Pryce, C.R., CD40-induced inflammation in mice leads to sustained emotional and cognitive dysfunctions coincident with altered tryptophan metabolsim: a model for depression-autoimmune disease comorbidity. Brain Behav. Immun. 50 (2015), 125–140.
9. Chamberlain, S.R., Müller, U., Blackwell, A.D., Clark, L., Robbins, T.W., Sahakian, B.J., Neurochemical modulation of response inhibition and probabilistic learning in humans. Science 311 (2006), 861–863.
10. Chenu, F., El Mansari, M., Blier, P., Electrophysiological effects of repeated administration of agomelatine on the dopamine, norepinephrine, and serotonin systems in the rat brain. Neuropsychopharmacology 38 (2013), 275–284.
11. Clarke, H.F., Dalley, J.W., Crofts, H.S., Robbins, T.W., Roberts, A.C., Cognitive inflexibility after prefrontal serotonin depletion. Science 304 (2004), 878–880.
12. Cools, R., Barker, R.A., Sahakian, B.J., Robbins, T.W., Enhanced or impaired cognitive function in Parkinson׳s disease as a function of dopaminergic medication and task demands. Cereb. Cortex 11 (2001), 1136–1143.
13. Cools, R., Clark, L., Owen, A.M., Robbins, T.W., Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic imaging. J. Neurosci. 22 (2002), 4563–4567.
14. Cools, R., Lewis, S.J.G., Clark, L., Barker, R.A., Robbins, T.W., L-DOPA disrupts activity in the nucleus accumbens during reversal learning in Parkinson׳s disease. Neuropsychopharmacology 32 (2007), 180–189.
15. Cuthbert, B.N., Research domain criteria: toward future psychiatric nosologies. Dialog. – Clin. Neurosci. 17 (2015), 89–97.
16. Cuthbert, B.N., Insel, T.R., Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med., 11, 2013, 126.
17. Dekeyne, A., Mannoury, L.C., Gobert, A., Brocco, M., Lejeune, F., Serres, F., Sharp, T., Daszuta, A., Soumier, A., Papp, M., Rivet, J.M., Flik, G., Cremers, T.I., Muller, O., Lavielle, G., Millan, M.J., S32006, a novel 5-HT2C receptor antagonist displaying broad-based antidepressant and anxiolytic properties in rodent models. Psychopharmacology 199 (2008), 549–568.
18. Di Giannantonio, M., Martinotti, G., Anhedonia and major depression: the role of agomelatine. Eur. Neuropsychopharmacol. 22 (2012), S505–S510.
19. Di Giovanni, G., Di Matteo, V., Benigno, P., Esposito, A., E, Central serotonin2C receptor: from physiology to pathology. Curr. Top. Med. Chem. 6 (2006), 1909–1925.
20. Dichter, G.S., Smoski, M.J., Kampov-Polevoy, A.B., Gallop, R., Garbutt, J.C., Unipolar depression does not moderate responses to the sweet taste test. Depress. Anxiety 27 (2010), 859–863.
21. DSM-5, Diagnostic and Statistical Manual of Mental Disorders. 5th ed., 2013, Revision American Psychiatric Association, American Psychiatric Association, Washington, DC.
22. Eberle-Wang, K., Mikeladze, Z., Uryu, K., Chesselet, M.-F., Pattern of expression of the serotonin2C receptor messneger RNA in the basal ganglia of adult rats. J. Comp. Neurol. 384 (1997), 233–247.
23. Elliott, R., Sahakian, B.J., Herrod, J.J., Robbins, T.W., Paykel, E.S., Abnormal response to negative feedback in unipolar depression: evidence for a diagnosis specific impairment. J. Neurol. Neurosurg. Psychiatry 63 (1997), 74–82.
24. Elliott, R., Sahakian, B., McKay, A.P., Herrod, J.J., Robbins, T.W., Paykel, E.S., Neuropsychological impairments in unipolar depression: the influence of perceived failure on subsequent performance. Psychol. Med. 26 (1996), 975–989.
25. Evers, E.A.T., Cools, R., Clark, L., van der Veen, F.M., Jolles, J., Sahakian, B.J., Robbins, T.W., Serotonergic modulation of prefrontal cortex during negative feedback in probabilistic reversal learning. Neuropsychopharmacology 30 (2005), 1138–1147.
26. Floresco, S.B., Magyar, O., Ghods-Sharifi, S., Vexelman, C., Tse, M.T., Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacology 31 (2006), 297–309.
27. Fuertig, R., Azzinnari, D., Bergamini, G., Cathomas, F., Sigrist, H., Seifritz, E., Vavassori, S., Luippold, A., Hengerer, B., Ceci, A., Pryce, C.R., Mouse chronic social stress increases blood and brain kynurenine pathway activity and fear behaviour: Both effects are reversed by inhibition of indoleamine 2,3-dioxygenase. Brain Behav. Immun. 54 (2016), 59–72.
28. Golden, S.A., Covington, H.E., Berton, O., Russo, S.J., A standardized protocol for repeated social defeat stress in mice. Nat. Protoc. 6 (2011), 1183–1191.
29. Gumuslu, E., Mutlu, O., Sunnetci, D., Ulak, G., Celikyurt, I.K., Cine, N., Akar, F., Savli, H., Erden, F., The antidepressant agomelatine improves memory deterioration and upregulates CREB and BDNF gene expression levels in unpredictable chronic mild stress (UCMS) – exposed mice. Drug. Target Insights 8 (2014), 11–21.
30. ICD-10, 1994. International Statistical Classification of Diseases and Related Health Problems, 10th Revision.
31. Ineichen, C., Sigrist, H., Spinelli, S., Lesch, K.-P., Sautter, E., Seifritz, E., Pryce, C.R., Establishing a probabilistic reversal learning test in mice: evidence for the processes mediating reward-stay and punishment-shift behaviour and for their modulation by serotonin. Neuropharmacology 63 (2012), 1012–1021.
32. Jocham, G., Neumann, J., Klein, T.A., Danielmeier, C., Ullsperger, M., Adaptive coding of action values in the human rostral cingulate zone. J. Neurosci. 29 (2009), 7489–7496.
33. Kendler, K.S., Hettema, J.M., Butera, F., Gardner, C.O., Prescott, C.A., Life event dimensions of loss, humiliation, entrapment, and danger in the prediction of onsets of major depression and generalized anxiety. Arch. Gen. Psychiatry 60 (2003), 789–796.
34. Kennedy, S.H., Avedisova, A., Gimenez-Montesinos, N., Belaidi, C., de Bodinat, C., A placebo-controlled study of three agomelatine dose regimens (10 mg, 25 mg, 25–50 mg) in patients with major depressive disorder. Eur. Neuropsychopharmacol. 24 (2014), 553–563.
35. Kessler, R.C., The effects of stressful life events on depression. Annu. Rev. Psychol. 48 (1997), 191–214.
36. Krishnan, V., Han, M.-H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., LaPlant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K., Nestler, E.J., Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131 (2007), 391–404.
37. Kudryavtseva, N.N., Bakshtanovskaya, I.V., Koryakina, L.A., Social model of depression in mice of C57BL/6J strain. Pharm. Biochem. Behav. 38 (1991), 315–320.
38. Kumar, J., Chuang, J.-C., Na, E.S., Kuperman, A., Gillman, A.G., Mukherjee, S., Zigman, J.M., McClung, C.A., Lutter, M., Differential effects of chronic social stress and fluoxetine on meal patterns in mice. Appetite 64 (2013), 81–88.
39. Leventopoulos, M., Russig, H., Feldon, J., Pryce, C.R., Opacka-Juffry, J., Early deprivation leads to long-term reductions in motivation for reward and 5HT1A binding and both effects are reversed by fluoxetine. Neuropharmacology 56 (2009), 692–701.
40. Mairesse, J., Silletti, V., Laloux, C., Zuena, A.R., Giovine, A., Consolazione, M., van Camp, G., Malagodi, M., Gaetini, S., Cianci, S., Catalani, A., Mennuni, G., Mazzetta, A., van Reeth, O., Gabriel, C., Mocaer, E., Nicoletti, F., Morley-Fletcher, S., Maccari, S., Chronic agomelatine treatment corrects the abnormalities in the circadian rhythm of motor activity and sleep/wake cycle induced by prenatal restrain stress in adult rats. Int. J. Neuropsychopharmacol. 16 (2013), 323–338.
41. Marrocco, J., Reynaert, M.-L., Gatta, E., Gabriel, C., Mocaer, E., Di Prisco, S., Merega, E., Pittaluga, A., Nicoletti, F., Maccari, S., Morley-Fletcher, S., Mairesse, J., The effects of antidepressant treatment in prenatally stressed rats support the glutamatergic hypothesis of stress-related disorders. J. Neurosci. 34 (2014), 2015–2024.
42. Martinotti, G., Sepede, G., Gambi, F., Di Iorio, G., De Beradis, D., Di Nicola, M., Onofri, M., Janiri, L., Di Giannantonio, M., Agomelatine versus venlafaxine XR in the treatment of anhedonia in major depressive disorder. J. Clin. Psychopharmacol. 32 (2012), 487–491.
43. Millan, M.J., Gobert, A., Lejeune, F., Dekeyne, A., Newman-Tancredi, A., Pasteau, V., Rivet, J.-M., Cussac, D., The novel melatonin agonist agomelatine (S20098) is an antagonist at 5-hydroxytryptamine2c receptors, blockade of which enhances the activity of frontocortical dopaminergic and adrenergic pathways. J. Pharmacol. Exp. Ther. 306 (2003), 954–964.
44. Morley-Fletcher, S., Mairesse, J., Soumier, A., Banasr, M., Fagioli, F., Gabriel, C., Mocaer, E., Daszuta, A., McEwen, B., Nicoletti, F., Maccari, S., Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats. Psychopharmacology 217 (2011), 301–313.
45. Papp, M., Gruca, P., Boyer, P.-A., Mocaer, E., Effect of agomelatine in the chronic mild stress model of depression in the rat. Neuropsychopharmacol 28 (2003), 694–703.
46. Patterson, Z.R., Khazall, R., MacKay, H., Anisman, H., Abizaid, A., Central ghrelin signaling mediates the metabolic response of C57BL/6 male mice to chronic social defeat stress. Endocrinology 154 (2013), 1080–1091.
47. Pompeiano, M., Palacios, J.M., Mengod, G., Distribution of the serotonin 5-HT2 reecptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res. Mol. Brain Res. 23 (1994), 163–178.
48. Pryce, C.R., Seifritz, E., A translational research framework for enhanced validity of mouse models of psychopathological states in depression. Psychoneuroendocrinology 36 (2011), 308–329.
49. Racagni, G., Riva, M.A., Molenti, R., Musazzi, L., Calabrese, F., Popoli, M., Tardito, D., Mode of action of agomelatine: Synergy between melatonergic and 5-HT2C receptors. World J. Biol. Psychiatry 12 (2011), 574–587.
50. Rainer, Q., Xia, L., Guilloux, J.-P., Gabriel, C., Mocaer, E., Hen, R., Enhamre, E., Gardier, A.M., David, D.J., Beneficial behavioural and neurogenic effects of agomelatine in a model of depression/anxiety. Int. J. Neuropsychopharmacol. 15 (2012), 321–335.
51. Salvador, A., Vinckier, F., Meyniel, F., Deakin, J.F.W., Harmer, C.J., Montejo, A.L., Jabourian, A.P., Gruget, C., Gabriel, C., Goodwin, G.M., Gaillard, R., Effects of Agomelatine Compared to Escitalopram on Motivation in Healthy Male and Female Volunteers After 9 Weeks of Treatment. 2014, European College of Neuropsychopharmacology, Berlin.
52. Sherdell, L., Waugh, C.E., Gotlib, I.H., Anticipatory pleasure predicts motivation for reward in major depression. J. Abnorm. Psychol. 121 (2012), 51–60.
53. Taylor Tavares, J.V., Clark, L., Furey, M.L., Williams, G.B., Sahakian, B., Drevets, W.C., Neural basis of abnormal response to negative feedback in unmedicated mood disorders. NeuroImage 42 (2008), 1118–1126.
54. Treadway, M.T., Bossaller, N., Shelton, R.C., Zald, D.H., Effort-based decision-making in major depressive disorder: a translational model of motivational anhedonia. J. Abnorm. Psychol. 121 (2012), 553–558.
55. Tye, K.M., Mirzabekov, J.J., Warden, M.R., Ferenczi, E.A., Tsai, H.-C., Finkelstein, J., Kim, S.-Y., Adhikari, A., Thompson, K.R., Andalman, A.S., Gunaydin, L.A., Witten, I.B., Deisseroth, K., Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493 (2013), 537–543.
56. Voigt, J.-P., Fink, H., Serotonin controlling feeding and satiety. Behav. Brain Res. 277 (2015), 14–31.
57. Willner, P., Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology 134 (1997), 319–329.