Adolescent social instability stress increases aggression in a food competition task in adult male Long-Evans rats

Developmental Psychobiology

Volumn 56, Issue 7, 2014, Pages 1575-1588

  Cumming, Mark J ^a   Thompson, Madison A ^a   Mccormick, Cheryl M ^a  

^a BROCK UNIVERSITY   (Canada)

Author keywords

Adolescence; Aggression; Dominance; Early experiences; Rats; Social; Stress

Indexed keywords

AGE; AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; COMPETITIVE BEHAVIOR; FOOD; LONG EVANS RAT; MALE; MENTAL STRESS; PHYSIOLOGY; PSYCHOLOGY; RANDOMIZATION; RAT; SOCIAL DOMINANCE;

AGE FACTORS; AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; COMPETITIVE BEHAVIOR; DOMINANCE-SUBORDINATION; FOOD; MALE; RANDOM ALLOCATION; RATS; RATS, LONG-EVANS; STRESS, PSYCHOLOGICAL;

EID: 84907856597     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.21252     Document Type: Article

References (79)

1. Adams N., & Boice, R. (1989). Development of dominance in domestic rats in laboratory and seminatural environments. Behavioral Processes, 19, 127-142.
2. Albert, D. J., Dyson, E. M., Walsh, M. L., & Wong, R. (1988). Defensive aggression and testosterone-dependent intermale social aggression are each elicited by food competition. Physiology & Behavior, 43, 21-28.
3. Arakawa, H. (2006). Changes in the pattern of exploratory behavior associated with the development of social dominance relationships in male rats. Developmental Psychobiology, 48, 39-47.
4. Askew, A., Gonzalez, F. A., Stahl, J. M., & Karom, M. C. (2006). Food competition and social experience effects on V-1a receptor binding in the forebrain of male Long-Evans hooded rats. Hormones and Behavior, 49, 328-336.
5. Baarendse, P. J. J., Counotte, D. S., O'Donnell, P., & Vanderschuren, L. (2013). Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. Neuropsychopharmacology, 38, 1485-1494.
6. Baenninger, L. P. (1970). Social dominance orders in the rat: "spontaneous", food, and water competition. Journal of Comparative and Physiological Psychology, 71, 202-209.
7. Baik, J. H. (2013). Dopamine signalling in reward-related behaviours. Frontiers in Neural Circuits, 7, 1-16.
8. Barnum, C. J., Blandino, P., & Deak, T. (2008). Social status modulates basal IL-1 concentrations in the hypothalamus of pair-housed rats and influences certain features of stress reactivity. Brain. Behavior and Immunity, 22, 517-527.
9. Bell, H. C., Pellis, S. M., & Kolb, B. (2010). Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. Behavioural Brain Research, 207, 7-13.
10. Berdoy, M., Smith, P., & MacDonald, D. W. (1995). Stability of social status in wild rats: age and the role of settled dominance. Behaviour, 13(132), 193-212.
11. Berdoy, M. (1994). Making decisions in the wild: Constraints, conflicts and communication in foraging rats. In B. G. Galef, M. Mainardi, Jr., & P. Valssechi (Eds.), Behavioural aspects of feeding (pp. 289-313). Langhorn, PA: Harwood Academic Publishers.
12. Bianchi, M., Fone, K. F. C., Azmi, N., Heidbreder, C. A., Hagan, J. J., & Marsden, C. A. (2006). Isolation rearing induces recognition memory deficits accompanied by cytoskeletal alterations in rat hippocampus. European Journal of Neuroscience, 24, 2894-2902.
13. Blakemore, S. J. (2012). Development of the social brain in adolescence. Journal of the Royal Society of Medicine, 105, 111-116.
14. Blanchard, D. C., Sakai, R. R., McEwen, B., Weiss, S. M., & Blanchard, R. J. (1993). Subordination stress: Behavioral, brain, and neuroendocrine correlates. Behavioural Brain Research, 58, 113-121.
15. Blanchard, R. J., Hori, K., Tom, P., & Blanchard, D. C. (1988). Social dominance and individual aggressiveness. Aggressive Behavior, 14, 195-203.
16. Bulygina, V. V., Amstislavskaia, T. G., & Maslova, L. N. (2005). The effect of social isolation during juvenile period on the sexual arousal in adult rats. Ross Fiziol Zh Im I M Sechenova, 91, 1356-1365.
17. Buwalda, B., Geerdink, M., Vidal, J., & Koolhaas, J. M. (2011). Social behavior and social stress in adolescence: A focus on animal models. Neuroscience and Biobehavioral Reviews, 32, 1713-1721.
18. Buwalda, B., Stubbendorff, C., Zickert, N., & Koolhaas, J. M. (2013). Adolescent social stress does not necessarily lead to a compromised adaptive capacity during adulthood: a study on the consequences of social stress in rats. Neuroscience, 249, 258-270.
19. Calcagnetti D. J., & Schechter, M. D. (1992). Place conditioning reveals the rewarding aspect of social-interaction in juvenile rats. Physiology & Behavior, 51, 667-672.
20. Chase I. D., & Seitz, K. (2011). Self-Structuring Properties of Dominance Hierarchies: A New Perspective. Advances in Genetics, 75, 51-81.
21. Cook, C. J. (1999) Patterns of weaning and adult responses to stress. Physiology & Behavior, 67, 803-808.
22. Cordero M. I., & Sandi, C. (2007). Stress amplifies memory for social hierarchy. Frontiers in Neuroscience, 1, 175-184.
23. Davis, J. F., Krause, E. G., Melhorn, S. J., Sakai, R. R., & Benoit, S. C. (2009). Dominant rats are natural risk takers and display increased motivation for food reward. Neuroscience, 162, 23-30.
24. de Jong, J. G., van der Vegt, B. J., Buwalda, B., & Koolhaas, J. M. (2005). Social environment determines the long-term effects of social defeat. Physiology & Behavior, 84, 87-95.
25. Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2004). Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Developmental Psychobiology, 45, 153-162.
26. Drews, C. (1993) The concept and definition of dominance in animal behaviour. Behaviour, 125, 283-313.
27. Einon D. F., & Morgan, M. J. (1977). A critical period for social isolation in the rat. Developmental Psychobiology, 10, 123-132.
28. File S. E., & Seth, P. (2003). A review of 25 years of the social interaction test. European Journal of Pharmacology, 463, 35-53.
29. Fone K. C., & Porkness, M. V. (2008). Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neuroscience and Biobehavioral Reviews, 32, 1087-1102.
30. González Jatuff, A. S., Berástegui, M., Rodríguez, C. I., & Rodríguez Echandía, E. L. (1999). Permanent and transient effects of repeated preweaning stress on social and sexual behaviors of rats. Stress, 3, 97-106.
31. Green, M. R., Barnes, B., & McCormick, C. M. (2013). Social instability stress in adolescence increases anxiety and reduces social interactions in adulthood in male Long-Evans rats. Developmental Psychobiology, 55, 849-859.
32. Green M. R., & McCormick, C. M. (2013a). Effects of social instability stress in adolescence on long-term, not short-term, spatial memory performance. Behavioural Brain Research, 256, 165-171.
33. Green M. R., & McCormick, C. M. (2013b). Effects of stressors in adolescence on learning and memory in rodent models. Hormones and Behavior, 64, 364-379.
34. Hall, F. S. (1998). Social deprivation of neonatal, adolescent, and adult rats has distinct neurochemical and behavioral consequences. Critical Reviews in Neurobiology, 12, 129-162.
35. Hillman K. L., & Bilkey, D. K. (2012). Neural encoding of competitive effort in the anterior cingulate cortex. Nature Neuroscience, 15, 1290-1297.
36. Hol, T., Van Den Berg, C. L., van Ree, J. M., & Spruijt, B. M. (1999). Isolation during the play period in infancy decreases adult social interactions in rats. Behavioural Brain Research, 100, 91-97.
37. Hoshaw, B. A., Evans, J. C., Mueller, B., Valentino, R. J., & Lucki, I. (2006). Social competition in rats: Cell proliferation and behavior. Behavioural Brain Research, 175, 343-351.
38. Ismail, N., Garas, P., & Blaustein, J. D. (2011). Long-term effects of pubertal stressors on female sexual receptivity and estrogen receptor-α expression in cd-1 female mice. Hormones and Behavior, 59, 565-571.
39. Kozorovitskiy Y., & Gould, E. (2004). Dominance hierarchy influences adult neurogenesis in the dentate gyrus. Journal of Neuroscience, 24, 6755-6759.
40. Laroche, J., Gasbarro, L., Herman, J. P., & Blaustein, J. D. (2009a). Enduring influences of peripubertal/adolescent stressors on behavioral response to estradiol and progesterone in adult female mice. Neuroendocrinology, 150, 3717-3725.
41. Laroche, J., Gasbarro, L., Herman, J. P., & Blaustein, J. D. (2009b). Reduced behavioral response to gonadal hormones in mice shipped during the peripubertal/adolescent period. Endocrinology, 150, 2351-2358.
42. Lore R. K., & Stipo-Flaherty, A. (1984). Postweaning social experience and adult aggression in rats. Physiology & Behavior, 33, 571-574.
43. Lukkes, J. L., Mokin, M. V., Scholl, J. L., & Forster, G. L. (2009). Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Hormones and Behavior, 55(1), 248-256.
44. Maaswinkel, H., Gispen, W., & Spruijt, B. (1997). Executive function of the hippocampus in social behavior in the rat. Behavioral Neuroscience, 111, 777-784.
45. Malatynska E., & Knapp, R. J. (2005). Dominant-submissive behavior as models of mania and depression. Neuroscience and Biobehavioral Reviews, 29, 715-737.
46. Malatynska, E., Pinhasov, A., Crooke, J. J., Smith-Swintosky, V. L., & Brenneman, D. E. (2007). Reduction of dominant or submissive behaviors as models for antimanic or antidepressant drug testing: Technical considerations. Journal of Neuroscience Methods, 165, 175-182.
47. Marquez, C., Poirier, G. L., Cordero, M. I., Larsen, M. H., Groner, A., Marquis, J., Sandi, C. (2013). Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Translational Psychiatry, 3, e216, 1-12.
48. Masur J., & Benedito, A. M. C. (1974). Winning among rats in a food competition situation as a sex-related behavior. Behavioural Biology, 10, 533-540.
49. Mathews, I. Z., Kelly, H., & McCormick, C. M. (2011). Low doses of amphetamine lead to immediate and lasting locomotor sensitization in adolescent, not adult, male rats. Pharmacology, Biochemistry, & Behavior, 97, 640-647.
50. Mathews, I. Z., Mills, R. G., & McCormick, C. M. (2008). Chronic social stress in adolescence influenced both amphetamine conditioned place preference and locomotor sensitization. Developmental Psychobiology, 50, 451-459.
51. McCormick, C. M. (2010). An animal model of social instability stress in adolescence and risk for drugs of abuse. Physiology & Behavior, 99, 194-203.
52. McCormick C. M., & Green, M. R. (2013). From the stressed adolescent to the anxious and depressed adult: investigations in rodent models. Neuroscience, 249, 242-257.
53. McCormick, C. M., Green, M. R., Cameron, N. M., Nixon, F., Levy, M. J., & Clark, R. A. (2013). Deficits in male sexual behavior in adulthood after social instability stress in adolescence in rats. Hormones and Behavior, 63, 5-12.
54. McCormick, C. M., Hodges, T. E., & Simone, J. J. (2014). Peer pressures: social instability stress in adolescence and social deficits in adulthood in an animal model. Developmental Cognitive Neuroscience, Epub ahead of print.
55. McCormick, C. M., Merrick, A., Secen, J., & Helmreich, D. L. (2007). Social instability in adolescence alters the central and peripheral hypothalamic-pituitary-adrenal responses to a repeated homotypic stressor in male and female rats. Journal of Neuroendocrinology, 19, 116-126.
56. McCormick, C. M., Nixon, F., Thomas, C., Lowie, B., & Dyck, J. (2010). Hippocampal cell proliferation and spatial memory performance after social instability stress in adolescence in female rats. Behavioural Brain Research, 208, 23-29.
57. McCormick, C. M., Robarts, D., Gleason, E., & Kelsey, J. E. (2004). Stress during adolescence enhances locomotor sensitization to nicotine in adulthood in female, but not male, rats. Hormones and Behavior, 46, 458-466.
58. McCormick, C. M., Robarts, D., Kopeikina, K., & Kelsey, J. E. (2005). Long-lasting, sex-and age-specific effects of social stress on corticosterone responses to restraint and locomotor responses to psychostimulants in rats. Hormones and Behavior, 48, 64-74.
59. McCormick, C. M., Thomas, C. M., Sheridan, C. S., Nixon, F., Flynn, J. A., & Mathews, I. Z. (2012). Social instability stress in adolescent male rats alters hippocampal neurogenesis and produces a deficit in spatial location memory in adulthood. Hippocampus, 22, 1300-1312.
60. Meng, Q. X., Li, N. X., Han, X. A., Shao, F., & Wang, W. W. (2010). Peri-adolescence isolation rearing alters social behavior and nociception in rats. Neuroscience Letters, 480, 25-29.
61. Morrissey, M. D., Mathews, I. Z., & McCormick, C. M. (2011). Enduring deficits in contextual and auditory fear conditioning after adolescent, not adult, social instability stress in male rats. Neurobiology of Learning and Memory, 95, 46-56.
62. Nelson, E. E., Leibenluft, E., McClure, E. B., & Pine, D. S. (2005). The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology. Psychological Medicine, 35, 163-174.
63. Olfe, J., Domanska, G., Schuett, C., & Kiank, C. (2010). Different stress-related phenotypes of balb/c mice from in-house or vendor: Alterations of the sympathetic and HPA axis responsiveness. BMC Physiology, 10, 2.
64. Pagani, J. H., Zhao, M., Cui, Z., Williams Avram, S. K., Dudek, S. M., & Young, W. S. (2014). Role of the vasopressin 1b receptor in rodent aggressive behavior and synaptic plasticity in hippocampal area CA2. Molecular Psychiatry, Epub ahead of print.
65. Parent, C. I., Del Corpo, A., Cameron, N. M., & Meaney, M. J. (2013). Maternal care associates with play dominance rank among adult female rats. Developmental Psychobiology, 55(7), 745-756.
66. Pellis, S. M., Field, E. F., Smith, L. K., & Field, V. C. (1997). Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neuroscience and Biobehavioral Reviews, 21, 105-120.
67. Pellis S. M., & Pellis, V. C. (1987). Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus Norvegicus. Aggressive Behavior, 13, 227-242.
68. Pellis S. M., & Pellis, V. C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Developmental Psychobiology, 23, 215-231.
69. Pellis S. M., & Pellis, V. C. (1991). Attack and defense during play fighting appear to be motivationally independant behaviors in muroid rodents. The Psychological Record, 41, 175-184.
70. Pellis S. M., & Pellis, V. C. (2007). Rough-and-tumble play and the development of the social brain. Current Directions in Psychological Science, 16, 95-98.
71. Sturman D. A., & Moghaddam, B. (2011). The neurobiology of adolescence: Changes in brain architecture, functional dynamics, and behavioral tendencies. Neuroscience and Biobehavioral Reviews, 35, 1704-1712.
72. Swanson H. H., & van de Poll, N. E. (1983). Effects of an isolated or enriched environment after handling on sexual maturation and behaviour in male and female rats. Journal of Reproduction and Fertility, 69, 165-171.
73. Trezza, V., Baarendse, P. J. J., & Vanderschuren, L. (2010). The pleasures of play: pharmacological insights into social reward mechanisms. Trends in Pharmacological Sciences, 31(10), 463-469.
74. van den Berg, C. L., Hol, T., Van Ree, J. M., Spruijt, B. M., Everts, H., & Koolhaas, J. M. (1999). Play is indispensable for an adequate development of coping with social challenges in the rat. Developmental Psychobiology, 34, 129-138.
75. van der Kooij, M. A., Fantin, M., Kraev, I., Korshunova, I., Grosse, J., Zanoletti, O, et al. (2014). Impaired hippocampal neuroligin-2 function by chronic stress or synthetic peptide treatment is linked to social deficits and increased aggression. Neuropsychopharmacology, 39(5), 1148-1158.
76. van der Kooij M. A., & Sandi, C. (2012). Social memories in rodents: Methods, mechanisms and modulation by stress. Neuroscience and Biobehavioral Reviews, 36, 1763-1772.
77. van Kerkhof, L. W. M., Damsteegt, R., Trezza, V., Voorn, P., & Vanderschuren, L. (2013). Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. Neuropsychopharmacology, 38, 1899-1909.
78. Veenit, V., Cordero, M. I., Tzanoulinou, S., & Sandi, C. (2013). Increased corticosterone in peripubertal rats leads to long-lasting alterations in social exploration and aggression. Frontiers in Behavioral Neuroscience, 7, 1-10.
79. Weiss, A., King, J. E., & Enns, R. M. (2002). Subjective well-being is heritable and genetically correlated with dominance in chimpanzees (Pan troglodytes). Journal of Personality and Social Psychology, 83, 1141-1149.