Learning and memory impairments in a neuroendocrine mouse model of anxiety/depression

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Darcet, Flavie ^a   Mendez David, Indira ^a   Tritschler, Laurent ^a   Gardier, Alain M ^a   Guilloux, Jean Philippe ^a   David, Denis J ^a  

^a University of Paris XI   (France)

Author keywords

Anxiety depression model; Associative memory; Cognitive flexibility; Cognitive impairments; Corticosterone; Depression; Recognition memory; Spatial learning maze

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; ASSOCIATIVE MEMORY; BARNES MAZE TEST; COGNITIVE DEFECT; CONTROLLED STUDY; DEPRESSION; DISEASE ASSOCIATION; EPISODIC MEMORY; LEARNING DISORDER; LONG TERM MEMORY; MALE; MEMORY DISORDER; MENTAL PERFORMANCE; MORRIS WATER MAZE TEST; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; RECOGNITION; SHORT TERM MEMORY; SPATIAL LEARNING; SPATIAL MEMORY; STATE DEPENDENT LEARNING;

EID: 84899673958     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00136     Document Type: Article

References (73)

1. Aisa, B., Tordera, R., Lasheras, B., Del Rio, J., and Ramirez, M. J. (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology 32, 256-266. doi: 10.1016/j.psyneuen.2006.12.013
2. Austin, M. P., Mitchell, P., and Goodwin, G. M. (2001). Cognitive deficits in depression: possible implications for functional neuropathology. Br. J. Psychiatry 178, 200-206. doi: 10.1192/bjp.178.3.200
3. Bertaina-Anglade, V., Enjuanes, E., Morillon, D., and Drieu La Rochelle, C. (2006). The object recognition task in rats and mice: a simple and rapid model in safety pharmacology to detect amnesic properties of a new chemical entity. J. Pharmacol. Toxicol. Methods 54, 99-105. doi: 10.1016/j.vascn.2006.04.001
4. Bisagno, V., Ferrini, M., Rios, H., Zieher, L. M., and Wikinski, S. I. (2000). Chronic corticosterone impairs inhibitory avoidance in rats: possible link with atrophy of hippocampal CA3 neurons. Pharmacol. Biochem. Behav. 66, 235-240. doi: 10.1016/S0091-3057(00)00265-3
5. Bodnoff, S. R., Humphreys, A. G., Lehman, J. C., Diamond, D. M., Rose, G. M., and Meaney, M. J. (1995). Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J. Neurosci. 15, 61-69.
6. Bondi, C. O., Rodriguez, G., Gould, G. G., Frazer, A., and Morilak, D. A. (2008). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33, 320-331. doi: 10.1038/sj.npp.1301410
7. Bourke, C., Porter, R. J., Carter, J. D., McIntosh, V. V., Jordan, J., Bell, C., et al. (2012). Comparison of neuropsychological functioning and emotional processing in major depression and social anxiety disorder subjects, and matched healthy controls. Aust. N.Z. J. Psychiatry 46, 972-981. doi: 10.1177/0004867412451502
8. Cerqueira, J. J., Mailliet, F., Almeida, O. F., Jay, T. M., and Sousa, N. (2007). The prefrontal cortex as a key target of the maladaptive response to stress. J. Neurosci. 27, 2781-2787. doi: 10.1523/JNEUROSCI.4372-06.2007
9. Cerqueira, J. J., Pego, J. M., Taipa, R., Bessa, J. M., Almeida, O. F., and Sousa, N. (2005). Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J. Neurosci. 25, 7792-7800. doi: 10.1523/JNEUROSCI.1598-05.2005
10. Clark, D. A. (2009). Cognitive behavioral therapy for anxiety and depression: possibilities and limitations of a transdiagnostic perspective. Cogn. Behav. Ther. 38(Suppl. 1), 29-34. doi: 10.1080/16506070902980745
11. Coburn-Litvak, P. S., Pothakos, K., Tata, D. A., McCloskey, D. P., and Anderson, B. J. (2003). Chronic administration of corticosterone impairs spatial reference memory before spatial working memory in rats. Neurobiol. Learn. Mem. 80, 11-23. doi: 10.1016/S1074-7427(03)00019-4
12. Cohen, S. J., Munchow, A. H., Rios, L. M., Zhang, G., Asgeirsdottir, H. N., and Stackman, R. W. Jr. (2013). The rodent hippocampus is essential for nonspatial object memory. Curr. Biol. 23, 1685-1690. doi: 10.1016/j.cub.2013.07.002
13. Couto, F. S., Batalha, V. L., Valadas, J. S., Data-Franca, J., Ribeiro, J. A., and Lopes, L. V. (2012). Escitalopram improves memory deficits induced by maternal separation in the rat. Eur. J. Pharmacol. 695, 71-75. doi: 10.1016/j.ejphar.2012.08.020
14. David, D. J., Samuels, B. A., Rainer, Q., Wang, J. W., Marsteller, D., Mendez, I., et al. (2009). Neurogenesis-dependent and-independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62, 479-493. doi: 10.1016/j.neuron.2009.04.017
15. Degl'innocenti, A., Agren, H., and Backman, L. (1998). Executive deficits in major depression. Acta Psychiatr. Scand. 97, 182-188. doi: 10.1111/j.1600-0447.1998.tb09985.x
16. Denny, C. A., Burghardt, N. S., Schachter, D. M., Hen, R., and Drew, M. R. (2012). 4-to 6-week-old adult-born hippocampal neurons influence novelty-evoked exploration and contextual fear conditioning. Hippocampus 22, 1188-1201. doi: 10.1002/hipo.20964
17. Deveney, C. M., and Deldin, P. J. (2006). A preliminary investigation of cognitive flexibility for emotional information in major depressive disorder and non-psychiatric controls. Emotion 6, 429-437. doi: 10.1037/1528-3542.6.3.429
18. Drew, M. R., Denny, C. A., and Hen, R. (2010). Arrest of adult hippocampal neurogenesis in mice impairs single-but not multiple-trial contextual fear conditioning. Behav. Neurosci. 124, 446-454. doi: 10.1037/a0020081
19. Egerhazi, A., Balla, P., Ritzl, A., Varga, Z., Frecska, E., and Berecz, R. (2013). Automated neuropsychological test battery in depression-preliminary data. Neuropsychopharmacol. Hung. 15, 5-11.
20. El Hage, W., Griebel, G., and Belzung, C. (2006). Long-term impaired memory following predatory stress in mice. Physiol. Behav. 87, 45-50. doi: 10.1016/j.physbeh.2005.08.039
21. Elizalde, N., Gil-Bea, F. J., Ramirez, M. J., Aisa, B., Lasheras, B., Del Rio, J., et al. (2008). Long-lasting behavioral effects and recognition memory deficit induced by chronic mild stress in mice: effect of antidepressant treatment. Psychopharmacology (Berl.) 199, 1-14. doi: 10.1007/s00213-007-1035-1
22. Ennaceur, A., and Delacour, J. (1988). A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav. Brain Res. 31, 47-59. doi: 10.1016/0166-4328(88)90157-X
23. Fava, M., Graves, L. M., Benazzi, F., Scalia, M. J., Iosifescu, D. V., Alpert, J. E., et al. (2006). A cross-sectional study of the prevalence of cognitive and physical symptoms during long-term antidepressant treatment. J. Clin. Psychiatry 67, 1754-1759. doi: 10.4088/JCP.v67n1113
24. Fossati, P., Coyette, F., Ergis, A. M., and Allilaire, J. F. (2002). Influence of age and executive functioning on verbal memory of inpatients with depression. J. Affect. Disord. 68, 261-271. doi: 10.1016/S0165-0327(00)00362-1
25. Garcia, R., Spennato, G., Nilsson-Todd, L., Moreau, J. L., and Deschaux, O. (2008). Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol. Learn. Mem. 89, 560-566. doi: 10.1016/j.nlm.2007.10.005
26. Garthe, A., Huang, Z., Kaczmarek, L., Filipkowski, R. K., and Kempermann, G. (2014). Not all water mazes are created equal: cyclin D2 knockout mice with constitutively suppressed adult hippocampal neurogenesis do show specific spatial learning deficits. Genes Brain Behav. 13, 357-364. doi: 10.1111/gbb.12130
27. Gomez, J. L., Lewis, M. J., Sebastian, V., Serrano, P., and Luine, V. N. (2013). Alcohol administration blocks stress-induced impairments in memory and anxiety, and alters hippocampal neurotransmitter receptor expression in male rats. Horm. Behav. 63, 659-666. doi: 10.1016/j.yhbeh.2013.01.007
28. Gomez, R. G., Posener, J. A., Keller, J., Debattista, C., Solvason, B., and Schatzberg, A. F. (2009). Effects of major depression diagnosis and cortisol levels on indices of neurocognitive function. Psychoneuroendocrinology 34, 1012-1018. doi: 10.1016/j.psyneuen.2009.01.017
29. Gotlib, I. H., and Joormann, J. (2010). Cognition and depression: current status and future directions. Annu. Rev. Clin. Psychol. 6, 285-312. doi: 10.1146/annurev.clinpsy.121208.131305
30. Gourley, S. L., and Taylor, J. R. (2009). Recapitulation and reversal of a persistent depression-like syndrome in rodents. Curr. Protoc. Neurosci. Chapter 9, Unit 9 32. doi: 10.1002/0471142301.ns0932s49
31. Griebel, G., Simiand, J., Serradeil-Le Gal, C., Wagnon, J., Pascal, M., Scatton, B., et al. (2002). Anxiolytic-and antidepressant-like effects of the non-peptide vasopressin V1b receptor antagonist, SSR149415, suggest an innovative approach for the treatment of stress-related disorders. Proc. Natl. Acad. Sci. U.S.A. 99, 6370-6375. doi: 10.1073/pnas.092012099
32. Guilloux, J. P., Seney, M., Edgar, N., and Sibille, E. (2011). Integrated behavioral z-scoring increases the sensitivity and reliability of behavioral phenotyping in mice: relevance to emotionality and sex. J. Neurosci. Methods 197, 21-31. doi: 10.1016/j.jneumeth.2011.01.019
33. Gumuslu, E., Mutlu, O., Sunnetci, D., Ulak, G., Celikyurt, I. K., Cine, N., et al. (2013). The effects of tianeptine, olanzapine and fluoxetine on the cognitive behaviors of unpredictable chronic mild stress-exposed mice. Drug Res. (Stuttg). 63, 532-539. doi: 10.1055/s-0033-1347237
34. Hammar, A., and Ardal, G. (2009). Cognitive functioning in major depression-a summary. Front. Hum. Neurosci. 3:26. doi: 10.3389/neuro.09.026.2009
35. Hammar, A., Lund, A., and Hugdahl, K. (2003). Long-lasting cognitive impairment in unipolar major depression: a 6-month follow-up study. Psychiatry Res. 118, 189-196. doi: 10.1016/S0165-1781(03)00075-1
36. Haridas, S., Kumar, M., and Manda, K. (2013). Melatonin ameliorates chronic mild stress induced behavioral dysfunctions in mice. Physiol. Behav. 119, 201-207. doi: 10.1016/j.physbeh.2013.06.015
37. Hasselbalch, B. J., Knorr, U., Hasselbalch, S. G., Gade, A., and Kessing, L. V. (2012). Cognitive deficits in the remitted state of unipolar depressive disorder. Neuropsychology 26, 642-651. doi: 10.1037/a0029301
38. Hinkelmann, K., Moritz, S., Botzenhardt, J., Riedesel, K., Wiedemann, K., Kellner, M., et al. (2009). Cognitive impairment in major depression: association with salivary cortisol. Biol. Psychiatry 66, 879-885. doi: 10.1016/j.biopsych.2009.06.023
39. Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D. Jr., Consiglio, A., Lie, D. C., et al. (2009). Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 16, 147-154. doi: 10.1101/lm.1172609
40. Lampe, I. K., Sitskoorn, M. M., and Heeren, T. J. (2004). Effects of recurrent major depressive disorder on behavior and cognitive function in female depressed patients. Psychiatry Res. 125, 73-79. doi: 10.1016/j.psychres.2003.12.004
41. Landro, N. I., Stiles, T. C., and Sletvold, H. (2001). Neuropsychological function in nonpsychotic unipolar major depression. Neuropsychiatry Neuropsychol. Behav. Neurol. 14, 233-240.
42. Lee, R. S., Hermens, D. F., Porter, M. A., and Redoblado-Hodge, M. A. (2012). A meta-analysis of cognitive deficits in first-episode major depressive disorder. J. Affect. Disord. 140, 113-124. doi: 10.1016/j.jad.2011.10.023
43. Maccari, S., and Morley-Fletcher, S. (2007). Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32(Suppl. 1), S10-S15. doi: 10.1016/j.psyneuen.2007.06.005
44. Magarinos, A. M., and McEwen, B. S. (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69, 89-98. doi: 10.1016/0306-4522(95)00259-L
45. Marazziti, D., Consoli, G., Picchetti, M., Carlini, M., and Faravelli, L. (2010). Cognitive impairment in major depression. Eur. J. Pharmacol. 626, 83-86. doi: 10.1016/j.ejphar.2009.08.046
46. McDermott, L. M., and Ebmeier, K. P. (2009). A meta-analysis of depression severity and cognitive function. J. Affect. Disord. 119, 1-8. doi: 10.1016/j.jad.2009.04.022
47. McLay, R. N., Freeman, S. M., and Zadina, J. E. (1998). Chronic corticosterone impairs memory performance in the Barnes maze. Physiol. Behav. 63, 933-937. doi: 10.1016/S0031-9384(97)00529-5
48. Mendez-David, I., David, D. J., Darcet, F., Wu, M. V., Kerdine-Romer, S., Gardier, A. M., et al. (2014). Rapid anxiolytic effects of a 5-HT receptor agonist are mediated by a neurogenesis-independent mechanism. Neuropsychopharmacology. 39, 1366-1378. doi: 10.1038/npp.2013.332
49. Mendez-David, I., Hen, R., Gardier, A. M., and David, D. J. (2013b). Adult hippocampal neurogenesis: an actor in the antidepressant-like action. Ann. Pharm. Fr. 71, 143-149. doi: 10.1016/j.pharma.2013.02.006
50. Millan, M. J., Agid, Y., Brune, M., Bullmore, E. T., Carter, C. S., Clayton, N. S., et al. (2012). Cognitive dysfunction in psychiatric disorders: characteristics, causes and the quest for improved therapy. Nat. Rev. Drug Discov. 11, 141-168. doi: 10.1038/nrd3628
51. Murphy, F. C., Michael, A., and Sahakian, B. J. (2012). Emotion modulates cognitive flexibility in patients with major depression. Psychol. Med. 42, 1373-1382. doi: 10.1017/S0033291711002418
52. Murrough, J. W., Iacoviello, B., Neumeister, A., Charney, D. S., and Iosifescu, D. V. (2011). Cognitive dysfunction in depression: neurocircuitry and new therapeutic strategies. Neurobiol. Learn. Mem. 96, 553-563. doi: 10.1016/j.nlm.2011.06.006
53. Naegeli, K. J., O'connor, J. A., Banerjee, P., and Morilak, D. A. (2013). Effects of milnacipran on cognitive flexibility following chronic stress in rats. Eur. J. Pharmacol. 703, 62-66. doi: 10.1016/j.ejphar.2013.02.006
54. Naismith, S. L., Hickie, I. B., Turner, K., Little, C. L., Winter, V., Ward, P. B., et al. (2003). Neuropsychological performance in patients with depression is associated with clinical, etiological and genetic risk factors. J. Clin. Exp. Neuropsychol. 25, 866-877. doi: 10.1076/jcen.25.6.866.16472
55. Nestler, E. J., Barrot, M., Dileone, R. J., Eisch, A. J., Gold, S. J., and Monteggia, L. M. (2002). Neurobiology of depression. Neuron 34, 13-25. doi: 10.1016/S0896-6273(02)00653-0
56. Nikiforuk, A., and Popik, P. (2011). Long-lasting cognitive deficit induced by stress is alleviated by acute administration of antidepressants. Psychoneuroendocrinology 36, 28-39. doi: 10.1016/j.psyneuen.2010.06.001
57. Orsetti, M., Colella, L., Dellarole, A., Canonico, P. L., and Ghi, P. (2007). Modification of spatial recognition memory and object discrimination after chronic administration of haloperidol, amitriptyline, sodium valproate or olanzapine in normal and anhedonic rats. Int. J. Neuropsychopharmacol. 10, 345-357. doi: 10.1017/S1461145706006705
58. Oury, F., Khrimian, L., Denny, C. A., Gardin, A., Chamouni, A., Goeden, N., et al. (2013). Maternal and offspring pools of osteocalcin influence brain development and functions. Cell 155, 228-241. doi: 10.1016/j.cell.2013.08.042
59. Patki, G., Solanki, N., Atrooz, F., Allam, F., and Salim, S. (2013). Depression, anxiety-like behavior and memory impairment are associated with increased oxidative stress and inflammation in a rat model of social stress. Brain Res. 1539, 73-86. doi: 10.1016/j.brainres.2013.09.033
60. Porter, R. J., Gallagher, P., Thompson, J. M., and Young, A. H. (2003). Neurocognitive impairment in drug-free patients with major depressive disorder. Br. J. Psychiatry 182, 214-220. doi: 10.1192/bjp.182.3.214
61. Ravnkilde, B., Videbech, P., Clemmensen, K., Egander, A., Rasmussen, N. A., and Rosenberg, R. (2002). Cognitive deficits in major depression. Scand. J. Psychol. 43, 239-251. doi: 10.1111/1467-9450.00292
62. Richter, S. H., Zeuch, B., Lankisch, K., Gass, P., Durstewitz, D., and Vollmayr, B. (2013). Where have I been? Where should I go? Spatial working memory on a radial arm maze in a rat model of depression. PLoS ONE 8:e62458. doi: 10.1371/journal.pone.0062458
63. Rudy, J. W., Huff, N. C., and Matus-Amat, P. (2004). Understanding contextual fear conditioning: insights from a two-process model. Neurosci. Biobehav. Rev. 28, 675-685. doi: 10.1016/j.neubiorev.2004.09.004
64. Sahay, A., Scobie, K. N., Hill, A. S., O'carroll, C. M., Kheirbek, M. A., Burghardt, N. S., et al. (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470. doi: 10.1038/nature09817
65. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., et al. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809. doi: 10.1126/science.1083328
66. Song, L., Che, W., Min-Wei, W., Murakami, Y., and Matsumoto, K. (2006). Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress. Pharmacol. Biochem. Behav. 83, 186-193. doi: 10.1016/j.pbb.2006.01.004
67. Sunyer, B., Patil, S., Höger, H., and Lubec, G. (2007). Barnes maze, a useful task to assess spatial reference memory in the mice. Protocol Exchange doi: 10.1038/nprot.2007.390
68. Surget, A., Saxe, M., Leman, S., Ibarguen-Vargas, Y., Chalon, S., Griebel, G., et al. (2008). Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol. Psychiatry64, 293-301. doi: 10.1016/j.biopsych.2008.02.022
69. Trivedi, M. H., and Greer, T. L. (2014). Cognitive dysfunction in unipolar depression: implications for treatment. J. Affect. Disord. 152-154, 19-27. doi: 10.1016/j.jad.2013.09.012
70. Vythilingam, M., Vermetten, E., Anderson, G. M., Luckenbaugh, D., Anderson, E. R., Snow, J., et al. (2004). Hippocampal volume, memory, and cortisol status in major depressive disorder: effects of treatment. Biol. Psychiatry 56, 101-112. doi: 10.1016/j.biopsych.2004.04.002
71. Watanabe, Y., Gould, E., Cameron, H. A., Daniels, D. C., and McEwen, B. S. (1992). Phenytoin prevents stress-and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 2, 431-435. doi: 10.1002/hipo.450020410
72. WHO. (2008). World Health Organization-The Global Burden of Disease-2004 Update. Geneva: WHO Library.
73. Wiskott, L., Rasch, M. J., and Kempermann, G. (2006). A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16, 329-343. doi: 10.1002/hipo.20167