Social defeat-induced anhedonia: Effects on operant sucrose-seeking behavior

Frontiers in Behavioral Neuroscience

Volumn 9, Issue AUGUST, 2015, Pages

  Riga, Danai ^a   Theijs, J Trisna ^a   De Vries, Taco J ^a,b   Smit, August B ^a   Spijker, Sabine ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Anhedonia; Depression; Guanfacine; Social defeat induced persistent stress (SDPS); Sucrose self administration

Indexed keywords

ANHEDONIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATION; CONTROLLED STUDY; DEPRESSION; DRUG ABUSE; EXPERIMENTAL SOCIAL BEHAVIOR TEST; INSTRUMENTAL CONDITIONING; MALE; MEMORY DISORDER; MOTIVATION; NONHUMAN; PSYCHOSOCIAL WITHDRAWAL; RAT; REINFORCEMENT; REWARD; SHORT TERM MEMORY; SOCIAL BEHAVIOR; SOCIAL DEFEAT; SOCIAL DEFEAT INDUCED PERSISTENT STRESS PARADIGM; SOCIAL ISOLATION; SPATIAL MEMORY; SUGAR INTAKE;

EID: 84940198093     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2015.00195     Document Type: Article

References (80)

1. Akkerman, S., Prickaerts, J., Steinbusch, H. W., and Blokland, A. (2012). Object recognition testing: statistical considerations.Behav. Brain Res. 232, 317-322. doi: 10.1016/j.bbr.2012.03.024
2. American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders: DSM-5™, 5th Edn.Arlington, VA: American Psychiatric Publishing, Inc.
3. Anisman, H., and Matheson, K. (2005). Stress, depression, and anhedonia: caveats concerning animal models. Neurosci. Biobehav. Rev. 29, 525-546. doi: 10.1016/j.neubiorev.2005.03.007
4. Artola, A., Von Frijtag, J. C., Fermont, P. C., Gispen, W. H., Schrama, L. H., Kamal, A., et al. (2006). Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur. J. Neurosci.23, 261-272. doi: 10.1111/j.1460-9568.2005.04552.x
5. 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
6. Bai, M., Zhang, L., Zhu, X., Zhang, Y., Zhang, S., and Xue, L. (2014). Comparison of depressive behaviors induced by three stress paradigms in rats. Physiol. Behav. 131, 81-86. doi: 10.1016/j.physbeh.2014.04.019
7. Barr, A. M., and Phillips, A. G. (1998). Chronic mild stress has no effect on responding by rats for sucrose under a progressive ratio schedule. Physiol. Behav. 64, 591-597. doi: 10.1016/S0031-9384(98)00060-2
8. Becker, C., Zeau, B., Rivat, C., Blugeot, A., Hamon, M., and Benoliel, J. J. (2008). Repeated social defeat-induced depression-like behavioral and biological alterations in rats: involvement of cholecystokinin. Mol. Psychiatry 13, 1079-1092. doi: 10.1038/sj.mp.4002097
9. Blanchard, R. J., McKittrick, C. R., and Blanchard, D. C. (2001). Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol. Behav. 73, 261-271. doi: 10.1016/S0031-9384(01)00449-8
10. Bondar, N. P., Kovalenko, I. L., Avgustinovich, D. F., Smagin, D. A., and Kudryavtseva, N. N. (2009). Anhedonia in the shadow of chronic social defeat stress, or when the experimental context matters. Open Behav. Sci. J. 3, 17-27. doi: 10.2174/1874230000903010017
11. Bruchas, M. R., Schindler, A. G., Shankar, H., Messinger, D. I., Miyatake, M., Land, B. B., et al. (2011). Selective p38alpha MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71, 498-511. doi: 10.1016/j.neuron.2011.06.011
12. Buwalda, B., De Boer, S. F., Schmidt, E. D., Felszeghy, K., Nyakas, C., Sgoifo, A., et al. (1999). Long-lasting deficient dexamethasone suppression of hypothalamic-pituitary-adrenocortical activation following peripheral CRF challenge in socially defeated rats. J. Neuroendocrinol. 11, 513-520. doi: 10.1046/j.1365-2826.1999.00350.x
13. Buwalda, B., Kole, M. H., Veenema, A. H., Huininga, M., De Boer, S. F., Korte, S. M., et al. (2005). Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neurosci. Biobehav. Rev. 29, 83-97. doi: 10.1016/j.neubiorev.2004.05.005
14. Carnevali, L., Mastorci, F., Graiani, G., Razzoli, M., Trombini, M., Pico-Alfonso, M. A., et al. (2012). Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol. Behav. 106, 142-150. doi: 10.1016/j.physbeh.2012.01.022
15. Cella, M., Dymond, S., and Cooper, A. (2010). Impaired flexible decision-making in major depressive disorder. J. Affect. Disord. 124, 207-210. doi: 10.1016/j.jad.2009.11.013
16. Chentsova-Dutton, Y., and Hanley, K. (2010). The effects of anhedonia and depression on hedonic responses. Psychiatry Res.179, 176-180. doi: 10.1016/j.psychres.2009.06.013
17. Covington, H. E. III., Kikusui, T., Goodhue, J., Nikulina, E. M., Hammer, R. P. Jr., and Miczek, K. A. (2005). Brief social defeat stress: long lasting effects on cocaine taking during a binge and zif268 mRNA expression in the amygdala and prefrontal cortex.Neuropsychopharmacology 30, 310-321. doi: 10.1038/sj.npp.1300587
18. Covington, H. E. III., and Miczek, K. A. (2005). Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology 183, 331-340. doi: 10.1007/s00213-005-0190-5
19. De Jong, J. G., van Der Vegt, B. J., Buwalda, B., and Koolhaas, J. M. (2005). Social environment determines the long-term effects of social defeat. Physiol. Behav. 84, 87-95. doi: 10.1016/j.physbeh.2004.10.013
20. Der-Avakian, A., and Markou, A. (2012). The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci.35, 68-77. doi: 10.1016/j.tins.2011.11.005
21. Der-Avakian, A., Mazei-Robison, M. S., Kesby, J. P., Nestler, E. J., and Markou, A. (2014). Enduring deficits in brain reward function after chronic social defeat in rats: susceptibility, resilience, and antidepressant response. Biol. Psychiatry 76, 542-549. doi: 10.1016/j.biopsych.2014.01.013
22. Dere, E., Huston, J. P., and De Souza Silva, M. A. (2007). The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci. Biobehav. Rev. 31, 673-704. doi: 10.1016/j.neubiorev.2007.01.005
23. Diergaarde, L., van Mourik, Y., Pattij, T., Schoffelmeer, A. N., and De Vries, T. J. (2012). Poor impulse control predicts inelastic demand for nicotine but not alcohol in rats. Addict. Biol. 17, 576-587. doi: 10.1111/j.1369-1600.2011.00376.x
24. Disner, S. G., Beevers, C. G., Haigh, E. A., and Beck, A. T. (2011). Neural mechanisms of the cognitive model of depression.Nat. Rev. Neurosci. 12, 467-477. doi: 10.1038/nrn3027
25. Donahue, R. J., Muschamp, J. W., Russo, S. J., Nestler, E. J., and Carlezon, W. A. Jr. (2014). Effects of striatal DeltaFosB overexpression and ketamine on social defeat stress-induced anhedonia in mice. Biol. Psychiatry 76, 550-558. doi: 10.1016/j.biopsych.2013.12.014
26. Eshel, N., and Roiser, J. P. (2010). Reward and punishment processing in depression. Biol. Psychiatry 68, 118-124. doi: 10.1016/j.biopsych.2010.01.027
27. Fanous, S., Terwilliger, E. F., Hammer, R. P. Jr., and Nikulina, E. M. (2011). Viral depletion of VTA BDNF in rats modulates social behavior, consequences of intermittent social defeat stress, and long-term weight regulation. Neurosci. Lett. 502, 192-196. doi: 10.1016/j.neulet.2011.07.043
28. Femenia, T., Gomez-Galan, M., Lindskog, M., and Magara, S. (2012). Dysfunctional hippocampal activity affects emotion and cognition in mood disorders. Brain Res. 1476, 58-70. doi: 10.1016/j.brainres.2012.03.053
29. Fone, K. C., and Porkess, M. V. (2008). Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci. Biobehav. Rev. 32, 1087-1102. doi: 10.1016/j.neubiorev.2008.03.003
30. Forbes, N. F., Stewart, C. A., Matthews, K., and Reid, I. C. (1996). Chronic mild stress and sucrose consumption: validity as a model of depression. Physiol. Behav. 60, 1481-1484. doi: 10.1016/S0031-9384(96)00305-8
31. Fox, H., Sofuoglu, M., and Sinha, R. (2015). Guanfacine enhances inhibitory control and attentional shifting in early abstinent cocaine-dependent individuals. J. Psychopharmacol. 29, 312-323. doi: 10.1177/0269881114562464
32. Fox, H. C., Seo, D., Tuit, K., Hansen, J., Kimmerling, A., Morgan, P. T., et al. (2012). Guanfacine effects on stress, drug craving and prefrontal activation in cocaine dependent individuals: preliminary findings. J. Psychopharmacol. 26, 958-972. doi: 10.1177/0269881111430746
33. Fredriksson, I., Jayaram-Lindstrom, N., Wirf, M., Nylander, E., Nystrom, E., Jardemark, K., et al. (2015). Evaluation of guanfacine as a potential medication for alcohol use disorder in long-term drinking rats: behavioral and electrophysiological findings. Neuropsychopharmacology 40, 1130-1140. doi: 10.1038/npp.2014.294
34. Funk, D., Harding, S., Juzytsch, W., and Le, A. D. (2005). Effects of unconditioned and conditioned social defeat on alcohol self-administration and reinstatement of alcohol seeking in rats. Psychopharmacology 183, 341-349. doi: 10.1007/s00213-005-0194-1
35. Golden, S. A., Covington, H. E. III., Berton, O., and Russo, S. J. (2011). A standardized protocol for repeated social defeat stress in mice. Nat. Protoc. 6, 1183-1191. doi: 10.1038/nprot.2011.361
36. Hasler, G., Drevets, W. C., Manji, H. K., and Charney, D. S. (2004). Discovering endophenotypes for major depression.Neuropsychopharmacology 29, 1765-1781. doi: 10.1038/sj.npp.1300506
37. Heller, A. S., Johnstone, T., Shackman, A. J., Light, S. N., Peterson, M. J., Kolden, G. G., et al. (2009). Reduced capacity to sustain positive emotion in major depression reflects diminished maintenance of fronto-striatal brain activation. Proc. Natl. Acad. Sci. U.S.A. 106, 22445-22450. doi: 10.1073/pnas.0910651106
38. Henningsen, K., Andreasen, J. T., Bouzinova, E. V., Jayatissa, M. N., Jensen, M. S., Redrobe, J. P., et al. (2009). Cognitive deficits in the rat chronic mild stress model for depression: relation to anhedonic-like responses. Behav. Brain Res. 198, 136-141. doi: 10.1016/j.bbr.2008.10.039
39. Ho, N., and Sommers, M. (2013). Anhedonia: a concept analysis. Arch. Psychiatr. Nurs. 27, 121-129. doi: 10.1016/j.apnu.2013.02.001
40. Hodos, W. (1961). Progressive ratio as a measure of reward strength. Science 134, 943-944. doi: 10.1126/science.134.3483.943
41. Hollis, F., Duclot, F., Gunjan, A., and Kabbaj, M. (2011). Individual differences in the effect of social defeat on anhedonia and histone acetylation in the rat hippocampus. Horm. Behav. 59, 331-337. doi: 10.1016/j.yhbeh.2010.09.005
42. Hone-Blanchet, A., and Fecteau, S. (2014). Overlap of food addiction and substance use disorders definitions: analysis of animal and human studies. Neuropharmacology 85, 81-90. doi: 10.1016/j.neuropharm.2014.05.019
43. Kamal, A., van Der Harst, J. E., Kapteijn, C. M., Baars, A. J., Spruijt, B. M., and Ramakers, G. M. (2010). Announced reward counteracts the effects of chronic social stress on anticipatory behavior and hippocampal synaptic plasticity in rats. Exp. Brain Res. 201, 641-651. doi: 10.1007/s00221-009-2083-z
44. Keedwell, P. A., Andrew, C., Williams, S. C., Brammer, M. J., and Phillips, M. L. (2005). The neural correlates of anhedonia in major depressive disorder. Biol. Psychiatry 58, 843-853. doi: 10.1016/j.biopsych.2005.05.019
45. Krishnan, V., Han, M. H., Graham, D. L., Berton, O., Renthal, W., Russo, S. J., et al. (2007). Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404. doi: 10.1016/j.cell.2007.09.018
46. Le, A. D., Funk, D., Juzytsch, W., Coen, K., Navarre, B. M., Cifani, C., et al. (2011). Effect of prazosin and guanfacine on stress-induced reinstatement of alcohol and food seeking in rats. Psychopharmacology 218, 89-99. doi: 10.1007/s00213-011-2178-7
47. Lee, B., Tiefenbacher, S., Platt, D. M., and Spealman, R. D. (2004). Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29, 686-693. doi: 10.1038/sj.npp.1300391
48. Leistedt, S. J., and Linkowski, P. (2013). Brain, networks, depression, and more. Eur. Neuropsychopharmacol. 23, 55-62. doi: 10.1016/j.euroneuro.2012.10.011
49. McCabe, C., Cowen, P. J., and Harmer, C. J. (2009). Neural representation of reward in recovered depressed patients.Psychopharmacology 205, 667-677. doi: 10.1007/s00213-009-1573-9
50. McIntyre, R. S., Cha, D. S., Soczynska, J. K., Woldeyohannes, H. O., Gallaugher, L. A., Kudlow, P., et al. (2013). Cognitive deficits and functional outcomes in major depressive disorder: determinants, substrates, and treatment interventions. Depress. Anxiety 30, 515-527. doi: 10.1002/da.22063
51. McKee, S. A., Potenza, M. N., Kober, H., Sofuoglu, M., Arnsten, A. F., Picciotto, M. R., et al. (2015). A translational investigation targeting stress-reactivity and prefrontal cognitive control with guanfacine for smoking cessation. J. Psychopharmacol. 29, 300-311. doi: 10.1177/0269881114562091
52. Meerlo, P., Overkamp, G. J., Daan, S., van Den Hoofdakker, R. H., and Koolhaas, J. M. (1996). Changes in behaviour and body weight following a single or double social defeat in rats. Stress 1, 21-32. doi: 10.3109/10253899609001093
53. Miczek, K. A., Nikulina, E. M., Shimamoto, A., and Covington, H. E. III. (2011). Escalated or suppressed cocaine reward, tegmental BDNF, and accumbal dopamine caused by episodic versus continuous social stress in rats. J. Neurosci. 31, 9848-9857. doi: 10.1523/JNEUROSCI.0637-11.2011
54. 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
55. Muir, V. J., and Perry, C. M. (2010). Guanfacine extended-release: in attention deficit hyperactivity disorder. Drugs 70, 1693-1702. doi: 10.2165/11205940-000000000-00000
56. 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
57. Muto, J., Lee, H., Uwaya, A., Park, J., Nakajima, S., Nagata, K., et al. (2014). Oral administration of inosine produces antidepressant-like effects in mice. Sci. Rep. 4:4199. doi: 10.1038/srep04199
58. Nestler, E. J., and Hyman, S. E. (2010). Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169. doi: 10.1038/nn.2647
59. Nielsen, C. K., Arnt, J., and Sanchez, C. (2000). Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav. Brain Res. 107, 21-33. doi: 10.1016/S0166-4328(99)00110-2
60. Padrao, G., Mallorqui, A., Cucurell, D., Marco-Pallares, J., and Rodriguez-Fornells, A. (2013). Neurophysiological differences in reward processing in anhedonics. Cogn. Affect. Behav. Neurosci. 13, 102-115. doi: 10.3758/s13415-012-0119-5
61. Pizzagalli, D. A., Iosifescu, D., Hallett, L. A., Ratner, K. G., and Fava, M. (2008). Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. J. Psychiatr. Res. 43, 76-87. doi: 10.1016/j.jpsychires.2008.03.001
62. Pothion, S., Bizot, J. C., Trovero, F., and Belzung, C. (2004). Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav. Brain Res. 155, 135-146. doi: 10.1016/j.bbr.2004.04.008
63. Razzoli, M., Carboni, L., Andreoli, M., Ballottari, A., and Arban, R. (2011). Different susceptibility to social defeat stress of BalbC and C57BL6/J mice. Behav. Brain Res. 216, 100-108. doi: 10.1016/j.bbr.2010.07.014
64. Reijmers, L. G., Hoekstra, K., Burbach, J. P., van Ree, J. M., and Spruijt, B. M. (2001). Long-term impairment of social memory in the rat after social defeat is not restored by desglycinamide-vasopressin. Neurosci. Lett. 305, 145-148. doi: 10.1016/S0304-3940(01)01834-1
65. Richardson, N. R., and Roberts, D. C. (1996). Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J. Neurosci. Methods 66, 1-11. doi: 10.1016/0165-0270(95)00153-0
66. Riga, D., Schmitz, L. J., van Der Harst, J. E., van Mourik, Y., Hoogendijk, W. J., Smit, A. B., et al. (2014). A sustained depressive state promotes a guanfacine reversible susceptibility to alcohol seeking in rats. Neuropsychopharmacology 39, 1115-1124. doi: 10.1038/npp.2013.311
67. Ruis, M. A., Te Brake, J. H., Buwalda, B., De Boer, S. F., Meerlo, P., Korte, S. M., et al. (1999). Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology24, 285-300. doi: 10.1016/S0306-4530(98)00050-X
68. Russo, S. J., and Nestler, E. J. (2013). The brain reward circuitry in mood disorders. Nat. Rev. Neurosci. 14, 609-625. doi: 10.1038/nrn3381
69. Rygula, R., Abumaria, N., Flugge, G., Fuchs, E., Ruther, E., and Havemann-Reinecke, U. (2005). Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav. Brain Res. 162, 127-134. doi: 10.1016/j.bbr.2005.03.009
70. Schlaepfer, T. E., Cohen, M. X., Frick, C., Kosel, M., Brodesser, D., Axmacher, N., et al. (2008). Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 33, 368-377. doi: 10.1038/sj.npp.1301408
71. Schrader, G. D. (1997). Does anhedonia correlate with depression severity in chronic depression? Compr. Psychiatry 38, 260-263. doi: 10.1016/S0010-440X(97)90057-2
72. Smith, R. J., and Aston-Jones, G. (2011). alpha(2) Adrenergic and imidazoline receptor agonists prevent cue-induced cocaine seeking. Biol. Psychiatry 70, 712-719. doi: 10.1016/j.biopsych.2011.06.010
73. Smoski, M. J., Felder, J., Bizzell, J., Green, S. R., Ernst, M., Lynch, T. R., et al. (2009). fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. J. Affect. Disord. 118, 69-78. doi: 10.1016/j.jad.2009.01.034
74. Sofuoglu, M., Devito, E. E., Waters, A. J., and Carroll, K. M. (2013). Cognitive enhancement as a treatment for drug addictions.Neuropharmacology 64, 452-463. doi: 10.1016/j.neuropharm.2012.06.021
75. Spijker, J., Bijl, R. V., De Graaf, R., and Nolen, W. A. (2001). Determinants of poor 1-year outcome of DSM-III-R major depression in the general population: results of the Netherlands Mental Health Survey and Incidence Study (NEMESIS). Acta Psychiatr. Scand. 103, 122-130. doi: 10.1034/j.1600-0447.2001.103002122.x
76. Treadway, M. T., and Zald, D. H. (2011). Reconsidering anhedonia in depression: lessons from translational neuroscience.Neurosci. Biobehav. Rev. 35, 537-555. doi: 10.1016/j.neubiorev.2010.06.006
77. van Bokhoven, P., Oomen, C. A., Hoogendijk, W. J., Smit, A. B., Lucassen, P. J., and Spijker, S. (2011). Reduction in hippocampal neurogenesis after social defeat is long-lasting and responsive to late antidepressant treatment. Eur. J. Neurosci.33, 1833-1840. doi: 10.1111/j.1460-9568.2011.07668.x
78. Von Frijtag, J. C., Reijmers, L. G., van Der Harst, J. E., Leus, I. E., van Den Bos, R., and Spruijt, B. M. (2000). Defeat followed by individual housing results in long-term impaired reward- and cognition-related behaviours in rats. Behav. Brain Res. 117, 137-146. doi: 10.1016/S0166-4328(00)00300-4
79. Vrieze, E., Pizzagalli, D. A., Demyttenaere, K., Hompes, T., Sienaert, P., De Boer, P., et al. (2013). Reduced reward learning predicts outcome in major depressive disorder. Biol. Psychiatry 73, 639-645. doi: 10.1016/j.biopsych.2012.10.014
80. Willner, P. (1997). Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology 134, 319-329. doi: 10.1007/s002130050456