The Rodent Forced Swim Test Measures Stress-Coping Strategy, Not Depression-like Behavior

ACS Chemical Neuroscience

Volumn 8, Issue 5, 2017, Pages 955-960

  Commons, Kathryn G ^a   Cholanians, Aram B ^a   Babb, Jessica A ^a   Ehlinger, Daniel G ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

addiction; antidepressants; autism; behavior; Porsolt; serotonin; Stress

Indexed keywords

ANTIDEPRESSANT AGENT;

AUTISM; BRAIN DEPTH STIMULATION; COPING BEHAVIOR; DEPRESSION; FACE VALIDITY; FEEDING BEHAVIOR; FORCED SWIM TEST; GENETIC MODEL; HUMAN; PREDICTIVE VALIDITY; PRIORITY JOURNAL; REVIEW; TAIL SUSPENSION TEST; ANIMAL; ANIMAL BEHAVIOR; DISEASE MODEL; MENTAL STRESS; MOUSE; PHYSIOLOGY; PSYCHOLOGY; RAT; SWIMMING;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; BEHAVIOR, ANIMAL; DEPRESSION; DISEASE MODELS, ANIMAL; MICE; RATS; STRESS, PSYCHOLOGICAL; SWIMMING;

EID: 85019595468     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/acschemneuro.7b00042     Document Type: Review

References (67)

1. Porsolt, R. D., Bertin, A., and Jalfre, M. (1977) Behavioral despair in mice: a primary screening test for antidepressants Arch Int. Pharmacodyn. Ther. 229 (2) 327-36
2. Porsolt, R. D., Le Pichon, M., and Jalfre, M. (1977) Depression: a new animal model sensitive to antidepressant treatments Nature 266 (5604) 730-2 10.1038/266730a0
3. Castagne, V., Moser, P., Roux, S., and Porsolt, R. D. (2011) Rodent models of depression: forced swim and tail suspension behavioral despair tests in rats and mice Curr. Protoc. Neurosci. 55, 8.10A 10.1002/0471142301.ns0810as55
4. Lucki, I. (1997) The forced swimming test as a model for core and component behavioral effects of antidepressant drugs Behav. Pharmacol. 8 (6-7) 523-32 10.1097/00008877-199711000-00010
5. Alfonso, J., Frasch, A. C., and Flugge, G. (2005) Chronic stress, depression and antidepressants: effects on gene transcription in the hippocampus Rev. Neurosci. 16 (1) 43-56 10.1515/REVNEURO.2005.16.1.43
6. Naughton, M., Dinan, T. G., and Scott, L. V. (2014) Corticotropin-releasing hormone and the hypothalamic-pituitary-adrenal axis in psychiatric disease Handb Clin Neurol 124, 69-91 10.1016/B978-0-444-59602-4.00005-8
7. Palazidou, E. (2012) The neurobiology of depression Br. Med. Bull. 101, 127-45 10.1093/bmb/lds004
8. Willner, P., Scheel-Kruger, J., and Belzung, C. (2013) The neurobiology of depression and antidepressant action Neurosci. Biobehav. Rev. 37 (10) 2331-71 10.1016/j.neubiorev.2012.12.007
9. Overstreet, D. H. (2012) Modeling depression in animal models Methods Mol. Biol. 829, 125-44 10.1007/978-1-61779-458-2-7
10. Pollak, D. D., Rey, C. E., and Monje, F. J. (2010) Rodent models in depression research: classical strategies and new directions Ann. Med. 42 (4) 252-64 10.3109/07853891003769957
11. Dalla, C., Pitychoutis, P. M., Kokras, N., and Papadopoulou-Daifoti, Z. (2010) Sex differences in response to stress and expression of depressive-like behaviours in the rat Curr. Top. Behav. Neurosci. 8, 97-118 10.1007/7854-2010-94
12. Veenema, A. H., Blume, A., Niederle, D., Buwalda, B., and Neumann, I. D. (2006) Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin Eur. J. Neurosci 24 (6) 1711-20 10.1111/j.1460-9568.2006.05045.x
13. Kalynchuk, L. E., Gregus, A., Boudreau, D., and Perrot-Sinal, T. S. (2004) Corticosterone increases depression-like behavior, with some effects on predator odor-induced defensive behavior, in male and female rats Behav. Neurosci. 118 (6) 1365-77 10.1037/0735-7044.118.6.1365
14. Johnson, S. A., Fournier, N. M., and Kalynchuk, L. E. (2006) Effect of different doses of corticosterone on depression-like behavior and HPA axis responses to a novel stressor Behav. Brain Res. 168 (2) 280-8 10.1016/j.bbr.2005.11.019
15. Gold, P. W., Machado-Vieira, R., and Pavlatou, M. G. (2015) Clinical and biochemical manifestations of depression: relation to the neurobiology of stress Neural Plast. 2015, 581976 10.1155/2015/581976
16. Dinan, T. G. (1996) Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function Life Sci. 58 (20) 1683-94 10.1016/0024-3205(96)00066-5
17. Lanfumey, L., Mannoury La Cour, C., Froger, N., and Hamon, M. (2000) 5-HT-HPA interactions in two models of transgenic mice relevant to major depression Neurochem. Res. 25 (9-10) 1199-206 10.1023/A:1007683810230
18. Mahar, I., Bambico, F. R., Mechawar, N., and Nobrega, J. N. (2014) Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects Neurosci. Biobehav. Rev. 38, 173-92 10.1016/j.neubiorev.2013.11.009
19. Pompili, M., Serafini, G., Innamorati, M., Moller-Leimkuhler, A. M., Giupponi, G., Girardi, P., Tatarelli, R., and Lester, D. (2010) The hypothalamic-pituitary-adrenal axis and serotonin abnormalities: a selective overview for the implications of suicide prevention Eur. Arch Psychiatry Clin Neurosci 260 (8) 583-600 10.1007/s00406-010-0108-z
20. Savitz, J. and Drevets, W. C. (2009) Bipolar and major depressive disorder: neuroimaging the developmental-degenerative divide Neurosci. Biobehav. Rev. 33 (5) 699-771 10.1016/j.neubiorev.2009.01.004
21. Duncan, G. E., Johnson, K. B., and Breese, G. R. (1993) Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity J. Neurosci. 13 (9) 3932-43
22. Duncan, G. E., Knapp, D. J., Johnson, K. B., and Breese, G. R. (1996) Functional classification of antidepressants based on antagonism of swim stress-induced fos-like immunoreactivity J. Pharmacol. Exp. Ther. 277 (2) 1076-89
23. O'Leary, O. F., Bechtholt, A. J., Crowley, J. J., Hill, T. E., Page, M. E., and Lucki, I. (2007) Depletion of serotonin and catecholamines block the acute behavioral response to different classes of antidepressant drugs in the mouse tail suspension test Psychopharmacology (Berl) 192 (3) 357-71 10.1007/s00213-007-0728-9
24. Mayberg, H. S., Lozano, A. M., Voon, V., McNeely, H. E., Seminowicz, D., Hamani, C., Schwalb, J. M., and Kennedy, S. H. (2005) Deep brain stimulation for treatment-resistant depression Neuron 45 (5) 651-60 10.1016/j.neuron.2005.02.014
25. Hamani, C. and Nobrega, J. N. (2010) Deep brain stimulation in clinical trials and animal models of depression Eur. J. Neurosci 32 (7) 1109-17 10.1111/j.1460-9568.2010.07414.x
26. Rea, E., Rummel, J., Schmidt, T. T., Hadar, R., Heinz, A., Mathe, A. A., and Winter, C. (2014) Anti-anhedonic effect of deep brain stimulation of the prefrontal cortex and the dopaminergic reward system in a genetic rat model of depression: an intracranial self-stimulation paradigm study Brain Stimul 7 (1) 21-8 10.1016/j.brs.2013.09.002
27. Bambico, F. R., Bregman, T., Diwan, M., Li, J., Darvish-Ghane, S., Li, Z., Laver, B., Amorim, B. O., Covolan, L., Nobrega, J. N., and Hamani, C. (2015) Neuroplasticity-dependent and -independent mechanisms of chronic deep brain stimulation in stressed rats Transl. Psychiatry 5, e674 10.1038/tp.2015.166
28. Lim, L. W., Prickaerts, J., Huguet, G., Kadar, E., Hartung, H., Sharp, T., and Temel, Y. (2015) Electrical stimulation alleviates depressive-like behaviors of rats: investigation of brain targets and potential mechanisms Transl. Psychiatry 5, e535 10.1038/tp.2015.24
29. West, A. P. (1990) Neurobehavioral studies of forced swimming: the role of learning and memory in the forced swim test Prog. Neuro-Psychopharmacol. Biol. Psychiatry 14 (6) 863-77 10.1016/0278-5846(90)90073-P
30. de Kloet, E. R. and Molendijk, M. L. (2016) Coping with the Forced Swim Stressor: Towards Understanding an Adaptive Mechanism Neural Plast. 2016, 6503162 10.1155/2016/6503162
31. Molendijk, M. L. and de Kloet, E. R. (2015) Immobility in the forced swim test is adaptive and does not reflect depression Psychoneuroendocrinology 62, 389-91 10.1016/j.psyneuen.2015.08.028
32. Nestler, E. J. and Hyman, S. E. (2010) Animal models of neuropsychiatric disorders Nat. Neurosci. 13 (10) 1161-9 10.1038/nn.2647
33. Spratt, E. G., Nicholas, J. S., Brady, K. T., Carpenter, L. A., Hatcher, C. R., Meekins, K. A., Furlanetto, R. W., and Charles, J. M. (2012) Enhanced cortisol response to stress in children in autism Journal of autism and developmental disorders 42 (1) 75-81 10.1007/s10803-011-1214-0
34. Taylor, J. L. and Corbett, B. A. (2014) A review of rhythm and responsiveness of cortisol in individuals with autism spectrum disorders Psychoneuroendocrinology 49, 207-28 10.1016/j.psyneuen.2014.07.015
35. Garcia-Villamisar, D. and Rojahn, J. (2015) Comorbid psychopathology and stress mediate the relationship between autistic traits and repetitive behaviours in adults with autism J. Intellect Disabil Res. 59 (2) 116-24 10.1111/jir.12083
36. Guo, Y. P. and Commons, K. G. (2017) Serotonin neuron abnormalities in the BTBR mouse model of autism Autism Res. 10, 66 10.1002/aur.1665
37. Onaivi, E. S., Benno, R., Halpern, T., Mehanovic, M., Schanz, N., Sanders, C., Yan, X., Ishiguro, H., Liu, Q. R., Berzal, A. L., Viveros, M. P., and Ali, S. F. (2011) Consequences of cannabinoid and monoaminergic system disruption in a mouse model of autism spectrum disorders Curr. Neuropharmacol 9 (1) 209-14 10.2174/157015911795017047
38. Silverman, J. L., Yang, M., Turner, S. M., Katz, A. M., Bell, D. B., Koenig, J. I., and Crawley, J. N. (2010) Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism Neuroscience 171 (4) 1197-208 10.1016/j.neuroscience.2010.09.059
39. Uutela, M., Lindholm, J., Rantamaki, T., Umemori, J., Hunter, K., Voikar, V., and Castren, M. L. (2014) Distinctive behavioral and cellular responses to fluoxetine in the mouse model for Fragile X syndrome Front. Cell. Neurosci. 8, 150 10.3389/fncel.2014.00150
40. Ehlinger, D. G., Panzini, C., and Commons, K. G. Disrupted Cav1.2 L-type calcium channel function and expression alters behavior and ascending serotonin system activity. Program No. 32.16. Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience 2016.
41. Panzini, C. and Commons, K. G. Altered action of 5-HT2a receptor ligands in the 16p11.2 deletion syndrome mouse. Program No. 30.05. Neuroscience Meeting Planner. San Diego, CA: Society for Neuroscience 2016.
42. Brielmaier, J., Matteson, P. G., Silverman, J. L., Senerth, J. M., Kelly, S., Genestine, M., Millonig, J. H., DiCicco-Bloom, E., and Crawley, J. N. (2012) Autism-relevant social abnormalities and cognitive deficits in engrailed-2 knockout mice PLoS One 7 (7) e40914 10.1371/journal.pone.0040914
43. Brielmaier, J., Senerth, J. M., Silverman, J. L., Matteson, P. G., Millonig, J. H., DiCicco-Bloom, E., and Crawley, J. N. (2014) Chronic desipramine treatment rescues depression-related, social and cognitive deficits in Engrailed-2 knockout mice Genes Brain Behav 13 (3) 286-298 10.1111/gbb.12115
44. Zaccaria, K. J., Lagace, D. C., Eisch, A. J., and McCasland, J. S. (2010) Resistance to change and vulnerability to stress: autistic-like features of GAP43-deficient mice Genes Brain Behav 9 (8) 985-96 10.1111/j.1601-183X.2010.00638.x
45. Aller, M. I., Pecoraro, V., Paternain, A. V., Canals, S., and Lerma, J. (2015) Increased Dosage of High-Affinity Kainate Receptor Gene grik4 Alters Synaptic Transmission and Reproduces Autism Spectrum Disorders Features J. Neurosci. 35 (40) 13619-28 10.1523/JNEUROSCI.2217-15.2015
46. Jaehne, E. J., Klaric, T. S., Koblar, S. A., Baune, B. T., and Lewis, M. D. (2015) Effects of Npas4 deficiency on anxiety, depression-like, cognition and sociability behaviour Behav. Brain Res. 281, 276-82 10.1016/j.bbr.2014.12.044
47. Chandrasekhar, T. and Sikich, L. (2015) Challenges in the diagnosis and treatment of depression in autism spectrum disorders across the lifespan Dialogues Clin. Neurosci. 17 (2) 219-27
48. Woodbury-Smith, M. R., Boyd, K., and Szatmari, P. (2010) Autism spectrum disorders, schizophrenia and diagnostic confusion J. Psychiatry Neurosci. 35 (5) 360 10.1503/jpm.100130
49. Boyd, K., Woodbury-Smith, M., and Szatmari, P. (2011) Managing anxiety and depressive symptoms in adults with autism-spectrum disorders J. Psychiatry Neurosci. 36 (4) E35-6 10.1503/jpn.110040
50. Hurwitz, R., Blackmore, R., Hazell, P., Williams, K., and Woolfenden, S. (2012) Tricyclic antidepressants for autism spectrum disorders (ASD) in children and adolescents Cochrane Database Syst. Rev. 3) CD008372 10.1002/14651858.CD008372.pub2
51. Williams, K., Brignell, A., Randall, M., Silove, N., and Hazell, P. (2013) Selective serotonin reuptake inhibitors (SSRIs) for autism spectrum disorders (ASD) Cochrane Database Syst. Rev. 8) CD004677 10.1002/14651858.CD004677.pub3
52. Xu, G. P., Van Bockstaele, E., Reyes, B., Bethea, T., and Valentino, R. J. (2004) Chronic morphine sensitizes the brain norepinephrine system to corticotropin-releasing factor and stress J. Neurosci. 24 (38) 8193-7 10.1523/JNEUROSCI.1657-04.2004
53. Iniguez, S. D., Warren, B. L., Parise, E. M., Alcantara, L. F., Schuh, B., Maffeo, M. L., Manojlovic, Z., and Bolanos-Guzman, C. A. (2009) Nicotine exposure during adolescence induces a depression-like state in adulthood Neuropsychopharmacology 34 (6) 1609-24 10.1038/npp.2008.220
54. Stevenson, J. R., Schroeder, J. P., Nixon, K., Besheer, J., Crews, F. T., and Hodge, C. W. (2009) Abstinence following alcohol drinking produces depression-like behavior and reduced hippocampal neurogenesis in mice Neuropsychopharmacology 34 (5) 1209-22 10.1038/npp.2008.90
55. Belujon, P., Jakobowski, N. L., Dollish, H. K., and Grace, A. A. (2016) Withdrawal from Acute Amphetamine Induces an Amygdala-Driven Attenuation of Dopamine Neuron Activity: Reversal by Ketamine Neuropsychopharmacology 41 (2) 619-27 10.1038/npp.2015.191
56. McGregor, I. S., Gurtman, C. G., Morley, K. C., Clemens, K. J., Blokland, A., Li, K. M., Cornish, J. L., and Hunt, G. E. (2003) Increased anxiety and ″depressive″ symptoms months after MDMA (″ecstasy″) in rats: drug-induced hyperthermia does not predict long-term outcomes Psychopharmacology (Berl) 168 (4) 465-74 10.1007/s00213-003-1452-8
57. Bambico, F. R., Hattan, P. R., Garant, J. P., and Gobbi, G. (2012) Effect of delta-9-tetrahydrocannabinol on behavioral despair and on pre- and postsynaptic serotonergic transmission Prog. Neuro-Psychopharmacol. Biol. Psychiatry 38 (1) 88-96 10.1016/j.pnpbp.2012.02.006
58. Alves, C. J., Magalhaes, A., Summavielle, T., Melo, P., De Sousa, L., Tavares, M. A., and Monteiro, P. R. (2008) Hormonal, neurochemical, and behavioral response to a forced swim test in adolescent rats throughout cocaine withdrawal Ann. N. Y. Acad. Sci. 1139, 366-73 10.1196/annals.1432.047
59. Staub, D. R., Lunden, J. W., Cathel, A. M., Dolben, E. L., and Kirby, L. G. (2012) Morphine history sensitizes postsynaptic GABA receptors on dorsal raphe serotonin neurons in a stress-induced relapse model in rats Psychoneuroendocrinology 37 (6) 859-70 10.1016/j.psyneuen.2011.10.002
60. Hughes, J. R., Stead, L. F., Hartmann-Boyce, J., Cahill, K., and Lancaster, T. (2014) Antidepressants for smoking cessation Cochrane Database Syst. Rev. 1) CD000031 10.1002/14651858.CD000031.pub4
61. Slattery, D. A. and Cryan, J. F. (2012) Using the rat forced swim test to assess antidepressant-like activity in rodents Nat. Protoc. 7 (6) 1009-14 10.1038/nprot.2012.044
62. Hryhorczuk, C., Sharma, S., and Fulton, S. E. (2013) Metabolic disturbances connecting obesity and depression Front. Neurosci. 7, 177 10.3389/fnins.2013.00177
63. Martin-Aragon, S., Villar, A., and Benedi, J. (2016) Age-dependent effects of esculetin on mood-related behavior and cognition from stressed mice are associated with restoring brain antioxidant status Prog. Neuro-Psychopharmacol. Biol. Psychiatry 65, 1-16 10.1016/j.pnpbp.2015.08.007
64. Linthorst, A. C., Flachskamm, C., and Reul, J. M. (2008) Water temperature determines neurochemical and behavioural responses to forced swim stress: an in vivo microdialysis and biotelemetry study in rats Stress 11 (2) 88-100 10.1080/10253890701533231
65. Smith, B. L., Lyons, C. E., Correa, F. G., Benoit, S. C., Myers, B., Solomon, M. B., and Herman, J. P. (2017) Behavioral and physiological consequences of enrichment loss in rats Psychoneuroendocrinology 77, 37-46 10.1016/j.psyneuen.2016.11.040
66. Steru, L., Chermat, R., Thierry, B., and Simon, P. (1985) The tail suspension test: a new method for screening antidepressants in mice Psychopharmacology (Berl) 85 (3) 367-70 10.1007/BF00428203
67. Porter, K. R. (1957) The Submicroscopic Morphology of Protoplasm. In The Harvey Lectures (Dingle, J. H., Ed.), pp 175-228, Academic Press, New York, London.