The imposition of, but not the propensity for, social subordination impairs exploratory behaviors and general cognitive abilities

Behavioural Brain Research

Volumn 232, Issue 1, 2012, Pages 294-305

  Colas Zelin, Danielle ^a   Light, Kenneth R ^a   Kolata, Stefan ^a   Wass, Christopher ^a   Denman Brice, Alexander ^a   Rios, Christopher ^a   Szalk, Kris ^a   Matzel, Louis D ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Aggression; Cognition; General intelligence; Social status; Stress; Stress hormones; Subordination

Indexed keywords

CORTICOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY EQUILIBRIUM; COGNITION; CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; EXPLORATORY BEHAVIOR; FEAR; GRIP STRENGTH; INTELLIGENCE; LEARNING; MALE; MAZE TEST; MOUSE; NOCICEPTION; NONHUMAN; OLFACTORY DISCRIMINATION; PASSIVE AVOIDANCE; PRIORITY JOURNAL; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SOCIAL INTERACTION; TASK PERFORMANCE;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; COGNITION; CONDITIONING (PSYCHOLOGY); DISCRIMINATION (PSYCHOLOGY); DOMINANCE-SUBORDINATION; EXPLORATORY BEHAVIOR; FEAR; HAND STRENGTH; HOT TEMPERATURE; HYDROCORTISONE; MALE; MAZE LEARNING; MICE; ODORS; PAIN MEASUREMENT; POSTURAL BALANCE; PSYCHOMOTOR PERFORMANCE; SMELL; SOCIAL BEHAVIOR; SPACE PERCEPTION;

EID: 84860643947     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2012.04.017     Document Type: Article

References (95)

1. Shors T.J. Stressful experience and learning across the lifespan. Annual Review of Psychology 2006, 57:55-85.
2. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 2002, 78:578-595.
3. Roozendaal B. Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2003, 27(8):1213-1223.
4. Joëls M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends in Cognitive Sciences 2006, 10(4):152-158.
5. de Kloet E.R., Oitzl M.S., Joëls M. Stress and cognition: are corticosteroids good or bad guys?. Trends in Neurosciences 1999, 22(10):422-426.
6. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nature Reviews Neuroscience 2009, 10(6):434-445.
7. McEwen B.S., Sapolsky R.M. Stress and cognitive function. Current Opinion in Neurobiology 1995, 5(2):5-16.
8. Baumeister R.F., Twenge J.M., Nuss C.K. Effects of social exclusion on cognitive processes: anticipated aloneness reduces intelligent thought. Journal of Personality and Social Psychology 2002, 83(4):817-827.
9. Johnson G.M. Student alienation, academic achievement and WebCT use. Educational Technology & Society 2005, 8(2):179-189.
10. Schmader T., Johns M., Forbes C. An integrated process model of stereotype threat effects on performance. Psychological Review 2010, 115(2):336-356.
11. Hoover H., Oliver R., Hazler R.J. Bullying: perceptions of adolescent victims in the Midwestern USA. School Psychology International 1992, 13(1):5-16.
12. Olweus D. Aggressors and their victims: bullying at school. Disruptive behaviours in schools 1984, Wiley, New York.
13. Knox E., Conti-Ramsden G. Bullying risks of 11-year-old children with specific language impairment (SLI): does school placement matter?. International Journal of Language and Communication Disorders 2003, 38(1):1-12.
14. Perry D.G., Kusel S.J., Perry L.C. Victims of peer aggression. Developmental Psychology 1988, 24(6):807-814.
15. Horwood J., Salvi G., Thomas K., Duffy L., Gunnell D., Hollis C., et al. IQ and non-clinical psychotic symptoms in 12-year-olds: results from the ALSPAC birth Cohort. The British Journal of Psychiatry 2008, 193:185-191.
16. Alzoubi K.H., Abdul-Razzak K.K., Khabour O.F., Al-Tuweiq G.M., Alzubi M.A., Alkadhi K.A. Adverse effect of combination of chronic psychosocial stress and high fat diet on hippocampus-dependent memory in rats. Behavioural Brain Research 2009, 204(1):117-123.
17. Fitchett A.E., Collins S.A., Barnard C.J., Cassaday H.J. Subordinate male mice show long-lasting differences in spatial learning that persist when housed alone. Neurobiology of Learning and Memory 2005, 84(3):247-251.
18. Krugers H.J., Douma B.R., Andringa G., Bohus B., Korf J., Luiten P.G. Exposure to chronic psychosocial stress and corticosterone in the rat: effects on spatial discrimination learning and hippocampal protein kinase Cgamma immunoreactivity. Hippocampus 1997, 7(4):427-436.
19. Ohl F., Fuchs E. Memory performance in tree shrews: effects of stressful experiences. Neuroscience and Biobehavioral Reviews 1998, 23(2):319-323.
20. Ohl F., Fuchs E. Differential effects of chronic stress on memory processes in the tree shrew. Cognitive Brain Research 1999, 7:1379-1387.
21. Kvist B. Learning in mice selectively bred for high and low aggressiveness. Psychological Reports 1989, 64(1):127-130.
22. Bodnoff S.R., Humphreys A.G., Lehman J.C., Diamond D.M., Rose G.M., Meaney M.J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. Journal of Neuroscience 1995, 15(1):61-69.
23. Touyarot K., Venero C., Sandi C. Spatial learning impairment induced by chronic stress is related to individual differences in novelty reactivity: search for neurobiological correlates. Psychoneuroendocrinology 2004, 29(2):290-305.
24. Francia N., Cirulli F., Chiarotti F., Antonelli A., Aloe L., Alleva E. Spatial memory deficits in middle-aged mice correlate with lower exploratory activity and a subordinate status: role of hippocampal neurotrophins?. European Journal of Neuroscience 2006, 23(3):711-728.
25. Barnard C.J., Luo N. Acquisition of dominance status affects maze learning in mice. Behavioural Processes 2002, 60(1):53-59.
26. Fitchett A.E., Barnard C.J., Cassaday H.J. Corticosterone differences rather than social housing predict performance of T-maze alternation in male CD-1 mice. Animal Welfare 2009, 18(1):21-31.
27. Buwalda B., Kole M.H., Veenema A.H., Huininga M., de Boer S.F., Korte S.M., et al. Long-term effects of social stress on brain and behavior: a focus on hippocampal functioning. Neuroscience and Biobehavioral Reviews 2005, 29(1):83-97.
28. Bartolomucci A., de Biurrun G., Czéh B., van Kampen M., Fuchs E. Selective enhancement of spatial learning under chronic psychosocial stress. European Journal of Neuroscience 2002, 15(11):1863-1866.
29. Moragrega I., Carrasco M.C., Vicens P., Redolat R. Spatial learning in male mice with different levels of aggressiveness: effects of housing conditions and nicotine administration. Behavioural Brain Research 2003, 147(1-2):1-8.
30. Spritzer M.D., Meikle D.B., Solomon N.G. The relationship between dominance rank and spatial ability among male meadow voles (Microtus pennsylvanicus). Journal of Comparative Psychology 2004, 118(3):332-339.
31. Kolata S., Light K., Matzel L.D. Domain specific and domain general learning factors are expressed in genetically heterogeneous CD-1 mice. Intelligence 2008, 36(6):619-629.
32. Plomin R. Genetics and general cognitive ability. Nature 1999, 402:C25-C29.
33. Kolata S., Light K., Grossman H.C., Hale G., Matzel L.D. Selective attention is a primary determinant of the relationship between working memory and general learning ability in outbred mice. Learning and Memory 2007, 14(1):22-28.
34. Kolata S., Light K., Townsend D.A., Hale G., Grossman H.C., Matzel L.D. Neurobiology of Learning and Memory 2005, 84(3):241-246.
35. Light K.R., Kolata S., Wass C., Denman-Brice A., Zagalsky R., Matzel L.D. Working memory training promotes general cognitive abilities in genetically heterogeneous mice. Current Biology 2010, 20(8):777-782.
36. Kolata S., Light K., Wass C.D., Colas-Zelin D., Roy D., Matzel L.D. A dopaminergic gene cluster in the prefrontal cortex predicts performance indicative of general intelligence in genetically heterogeneous mice. PLoS ONE 2010, 5(November (11)):e14036.
37. Matzel L.D., Kolata S. Selective attention, working memory, and animal intelligence. Neuroscience and Biobehavioral Reviews 2010, 34(January (1)):23-30.
38. Hardy M.P., Sottas C.M., Ge R., McKittrick C.R., Tamashiro K.L., McEwen B.S., et al. Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biology of Reproduction 2002, 67(6):1750-1755.
39. Monder C., Sakai R.R., Miroff Y., Blanchard D.C., Blanchard R.J. Reciprocal changes in plasma corticosterone and testosterone in stressed male rats maintained in a visible burrow system: evidence for a mediating role of testicular 11 beta-hydroxysteroid dehydrogenase. Endocrinology 1994, 134(3):1193-1198.
40. Dong Q., Salva A., Sottas C.M., Niu E., Holmes M., Hardy M.P. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. Journal of Andrology 2004, 25(6):973-981.
41. Blanchard D.C., Sakai R.R., McEwen B., Weiss S.M., Blanchard R.J. Subordination stress: behavioral, brain, and neuroendocrine correlates. Behavioural Brain Research 1993, 58(1-2):113-121.
42. Blanchard D.C., Spencer R.L., Weiss S.M., Blanchard R.J., McEwen B., Sakai R.R. Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates. Psychoneuroendocrinology 1995, 20(2):117-134.
43. Veenema A.H., Meijer O.C., de Kloet E.R., Koolhaas J.M., Bohus B.G. Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Hormones and Behavior 2003, 43(1):197-204.
44. von Holst D. Social stress in tree shrews: problems, results and goals. Journal of Comparative Physiology 1977, 120:71-86.
45. Nock B.L., Leshner A.I. Hormonal mediation of the effects of defeat on agonistic responding in mice. Physiology and Behavior 1976, 17(1):111-119.
46. Coe C., Mendoza S., Levine S. Social stastus constrains the stress response in the squirrel monkey. Physiology and Behavior 1979, 23(4):633-638.
47. Sapolsky R.M. Individual differences in cortisol secretory patterns in the wild baboon: role of negative feedback sensitivity. Endocrinology 1983, 113(6):2263-2267.
48. Bronson F.H. Establishment of social rank among grouped male mice: relative effects on circulating FSH, LH, and corticosterone. Physiology and Behavior 1973, 10(5):947-951.
49. Ely D.L., Henry J.P. Neuroendocrine response patterns in dominant and subordinate mice?. Hormones and Behavior 1978, 10(2):156-169.
50. Wirth M.M., Welsh K.M., Schultheiss O.C. Salivary cortisol changes in humans after winning or losing a dominance contest depend on implicit power motivation. Hormones and Behavior 2006, 49(3):346-352.
51. Blanchard D.C., McKittrick C.R., Hardy M.P., Blanchard R.J. Effects of social stress on hormones, brain and behavior. Hormones, brain and behavior 2002, vol. 1:735-772. Academic Press, San Diego.
52. Ruis M.A.W., te Brake J.H.A., Buwalda B., de Boer S.F., Meerlo P., Korte S.M., et al. Housing familiar male wildtype rats together reduces the long-term adverse behavioural and physiological effects of social defeat. Psychoneuroendocrinology 1999, 24:285-300.
53. Menzaghi F., Heinrichs S.C., Vargas-Cortes M., Goldstein G., Koob G.F. IRI-514, a synthetic peptide analogue of thymopentin, reduces the behavioral response to social stress in rats. Physiology and Behavior 1996, 60(2). 397-401(5).
54. Heinrichs S.C., Menzaghi F., Pich E.M., Baldwin H.A., Rassnick S., Britton K.T., et al. Anti-stress action of a corticotropin-releasing factor antagonist on behavioral reactivity to stressors of varying type and intensity. Neuropsychopharmacology 1994, 111(3):179-186.
55. Heinrichs S.C., Pich E.M., Miczek K.A., Britton K.T., Koob G.F. Corticotropin-releasing factor antagonist reduces emotionality in socially defeated rats via direct neurotropic action. Brain Research 1992, 581(2):190-197.
56. Berton O., Aguerre S., Sarrieau A., Mormede P., Chaouloff F. Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats?. Neuroscience 1998, 82(1):147-159.
57. Berton O., Durand M., Aguerre S., Mormède P., Chaouloff F. Behavioral, neuroendocrine and serotonergic consequences of single social defeat and repeated fluoxetine pretreatment in the Lewis rat strain. Neuroscience 1999, 92(1):327-341.
58. Avgustinovich D.F., Gorbach O.V., Kudryavtseva N.N. Comparative analysis of anxiety-like behavior in partition and plus-maze tests after agonistic interactions in mice. Physiology and Behavior 1997, 61(1):37-43.
59. Rodgers R.J., Cole J.C. Anxiety enhancement in the murine elevated plus maze by immediate prior exposure to social stressors. Physiology and Behavior 1993, 53(2):383-388.
60. Haller J., Halász J. Mild social stress abolishes the effects of isolation on anxiety and chlordiazepoxide reactivity. Psychopharmacology 1999, 144(4):311-315.
61. Peres R.C., Leite J.R. The influence of competitive status (winner/loser) on the behavior of male rats in three models of anxiety. Aggressive Behavior 2002, 28:164-171.
62. Kudryavtseva N.N., Bakshtanovskaya I.V., Koryakina L.A. Social model of depression in mice of C57BL/6J strain. Pharmacology Biochemistry and Behavior 1991, 38(2):315-320.
63. Kudryavtseva N.N., Madorskaya I.A., Bakshtanovskaya I.V. Social success and voluntary ethanol consumption in mice of C57BL/6J and CBA/Lac strains. Physiology and Behavior 1991, 50(1):143-146.
64. Zook J.M., Adams D.B. Competitive fighting in the rat. Journal of Comparative and Physiological Psychology 1975, 88(1):418-423.
65. Schneider R., Hoffmann H.J., Schicknick H., Moutier R. Genetic analysis of isolation-induced aggression. I. Comparison between closely related inbred mouse strains. Behavioral and Neural Biology 1992, 57:198-204.
66. Grant E.C., Mackintosh J.H. A comparison of the social postures of some common laboratory rodents. Behaviour 1963, 21(3-4):246-259.
67. Clark L.H., Schein M.W. Activities associated with conflict behavior in mice. Animal Behaviour 1966, 14(1):44-49.
68. Burg R.D., Slotnick B.M. Response of colony mice to intruders with different fighting experience. Aggressive Behavior 1983, 9(1):49-58.
69. Miczek K.A., Maxson S.C., Fish E.W., Faccidomo S. Aggressive behavioral phenotypes in mice. Behavioural Brain Research 2001, 125(1-2):167-181.
70. Ginsburg B., Allee W.C. Some effects of conditioning on social dominance and subordination in inbred strains of mice. Physiological Zoology 1942, 15(4):485-550.
71. Miczek K.A., O'Donnell J.M. Intruder-evoked aggression in isolated and nonisolated mice: effects of psychomotor stimulants and L-dopa. Psychopharmacology 1978, 57(1):47-55.
72. Miczek K.A., Thompson M.L., Shuster L. Opioid-like analgesia in defeated mice. Science 1982, 215(4539):1520-1522.
73. Miczek K.A. Aggressive and social stress responses in genetically modified mice: from horizontal to vertical strategy. Psychopharmacology 1999, 147(1):17-19.
74. Blanchard R.J., Takahashi L.K., Fukunaga K.K., Blanchard D.C. Functions of the vibrissae in the defensive and aggressive behavior of the rat. Aggressive Behavior 1977, 3:231-240.
75. Blanchard D.C., Blanchard R.J., Lee E.M., Nakamura S. Defensive behaviors in rats following septal and septal-amygdala lesions. Journal of Comparative and Physiological Psychology 1979, 93(April (2)):378-390.
76. Animal play: evolutionary, comparative, and ecological perspectives. Structure-function interface in the analysis of play fighting 1998, 115-140. Cambridge University Press, New York, NY, USA. S.M. Pellis, V.C. Pellis, M. Bekoff, J.A. Byers (Eds.).
77. Sara S.J., Roullet P., Przybyslawski J. Consolidation of memory for odor-reward association: β-adrenergic receptor involvement in late phase. Learning and Memory 1999, 6:88-96.
78. Morris R.G.M. Pavlovian conditioned inhibition of fear during shuttlebox avoidance behavior. Learning and Motivation 1974, 5:424-447.
79. Bolles R.C. Avoidance and escape learning: simultaneous acquisition of different responses. Journal of Comparative and Physiological Psychology 1969, 68(3):355-358.
80. Matzel L.D., Townsend D.A., Grossman H., Han Y.R., Hale G., Zappulla M., et al. Exploration in outbred mice covaries with general learning abilities irrespective of stress reactivity, emotionality, and physical attributes. Neurobiology of Learning and Memory 2006, 86(2):228-240.
81. Kolata S., Wu J., Light K., Schachner M., Matzel L.D. Impaired working memory duration but normal learning abilities found in mice that are conditionally deficient in the close homolog of L1. Journal of Neuroscience 2008, 28(50):13505-13510.
82. Blanchard R.J., Wall P.M., Blanchard D.C. Problems in the study of rodent aggression. Hormones and Behavior 2003, 44(3):161-170.
83. Benton D. Is the concept of dominance useful in understanding rodent behavior?. Aggressive Behavior 1982, 8(2):104-107.
84. Uhrich J. The social hierarchy in albino mice. Journal of Comparative Psychology 1938, 25(2):373-413.
85. Brain P.F., Hui S.E. Variability in patterns of intra-specific biting attack in commonly used genetic lines of laboratory mice. Scandinavian Journal of Laboratory Animal Science 2003, 3(30):113-127.
86. Grossman H.C., Hale G., Light K., Kolata S., Townsend D.A., Goldfarb Y., et al. Pharmacological modulation of stress reactivity dissociates general learning ability from the propensity for exploration. Behavioral Neuroscience 2007, 121(5):949-964.
87. Light K.R., Kolata S., Hale G., Grossman H., Matzel L.D. Up-regulation of exploratory tendencies does not enhance general learning abilities in juvenile or young-adult outbred mice. Neurobiology of Learning and Memory 2008, 90(2):317-329.
88. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory drive. Journal of Comparative and Physiological Psychology 1955, 48(4):192-194.
89. Whimbey.A.E., Denenberg V.H. Two independent behavioral dimensions in open field performance. Journal of Comparative and Physiological Psychology 1967, 63(3):500-504.
90. Von Frijtag J.C., Kamal A., Reijmers L.G., Schrama L.H., van den Bos R., Spruijt B.M. Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats?. Neuroscience Letters 2001, 309(3):153-156.
91. Magariños A.M., McEwen B.S., Flügge G., Fuchs E. Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. Journal of Neuroscience 1996, 16(10):3534-3540.
92. McKittrick C.R., Magariños A.M., Blanchard D.C., Blanchard R.J., McEwen B.S., Sakai R.R. Chronic social stress reduces dendritic arbors in CA3 of hippocampus and decreases binding to serotonin transporter sites. Synapse 2000, 36(2):85-94.
93. Czéh B., Michaelis T., Watanabe T., Frahms J., De Biurrun G., Van Kampen M., et al. Stress-induced changes in cerebral metabolites, hippocampal volume, and cell proliferation are prevented by antidepressant treatment with tianeptine. Proceedings of the National Academy of Sciences of the United States of America 2001, 98(22):12796-12801.
94. Gould E., Tanapat P., McEwen B.S., Flügge G., Fuchs E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(6):3168-3171.
95. Matzel L.D., Light K.R., Wass C., Colas-Zelin D., Denman-Brice A., Waddel A.C., et al. Longitudinal attentional engagement rescues mice from age-related cognitive declines and cognitive inflexibility. Learning and Memory 2011, 18(April (5)):345-356.