Memory of opponents is more potent than visual sign stimuli after social hierarchy has been established

Behavioural Brain Research

Volumn 183, Issue 1, 2007, Pages 31-42

  Korzan, Wayne J ^a   Höglund, Erik ^b   Watt, Michael J ^c   Forster, Gina L ^c   Øverli, Øyvind ^d   Lukkes, Jodi L ^c   Summers, Cliff H ^c,e  

^a STANFORD UNIVERSITY   (United States)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY OF SOUTH DAKOTA   (United States)

^d NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^e W O Farber Center for Civic Leadership   (United States)

Author keywords

Aggression; Anolis carolinensis; Dopamine; Eyespots; Lizard; Opponent; Recognition; Serotonin

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; MALE; MONOAMINERGIC SYSTEM; NONHUMAN; PRIORITY JOURNAL; SOCIAL DOMINANCE; SOCIAL STATUS; STIMULUS RESPONSE; VISUAL ACUITY; VISUAL MEMORY;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; CATECHOLAMINES; HIERARCHY, SOCIAL; HIPPOCAMPUS; LIZARDS; MALE; PIGMENTATION; RAPHE NUCLEI; RECOGNITION (PSYCHOLOGY); SEROTONIN; SOCIAL DOMINANCE; STATISTICS, NONPARAMETRIC; VISUAL PERCEPTION;

EID: 34547919603     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2007.05.021     Document Type: Article

References (88)

1. Andrews T.J., and Summers C.H. Aggression, and the acquisition and function of social dominance in female Anolis carolinensis. Behaviour 133 (1996) 1265-1279
2. Bartolomucci A., de Biurrun G., Czeh B., Van Kampen M., and Fuchs E. Selective enhancement of spatial learning under chronic psychosocial stress. Eur J Neurosci 15 (2002) 1863-1866
3. Cabib S., D'Amato F.R., Puglisi-Allegra S., and Maestripieri D. Behavioral and mesocorticolimbic dopamine responses to non aggressive social interactions depend on previous social experiences and on the opponent's sex. Behav Brain Res 112 (2000) 13-22
4. Crews D. Inter- and intraindividual variation in display patterns in the lizard, Anolis carolinensis. Herpetelogica 31 (1975) 37-47
5. Crews D. The hormonal control of behavior in a lizard. Sci Am 241 (1979) 180-187
6. Day L.B., Crews D., and Wilczynski W. Effects of medial and dorsal cortex lesions on spatial memory in lizards. Behav Brain Res 118 (2001) 27-42
7. de Villiers M.S., van Jaarsveld A.S., Meltzer D.G., and Richardson P.R. Social dynamics and the cortisol response to immobilization stress of the African wild dog, Lycaon pictus. Horm Behav 31 (1997) 3-14
8. Deckel A.W. Behavioral changes in Anolis carolinensis following injection with fluoxetine. Behav Brain Res 78 (1996) 175-182
9. Deckel A.W., and Fuqua L. Effects of serotonergic drugs on lateralized aggression and aggressive displays in Anolis carolinensis. Behav Brain Res 95 (1998) 227-232
10. Deckel A.W., and Jevitts E. Left vs. right-hemisphere regulation of aggressive behaviors in Anolis carolinensis: effects of eye-patching and fluoxetine administration. J Exp Zool 278 (1997) 9-21
11. Deckel A.W., Lillaney R., Ronan P.J., and Summers C.H. Lateralized effects of ethanol on aggression and serotonergic systems in Anolis carolinensis. Brain Res 807 (1998) 38-46
12. DeCourcy K.R., and Jenssen T.A. Structure and use of male territorial headbob signals by the lizard Anolis carolinensis. Anim Behav 47 (1994) 251-262
13. Edwards P.J. Plumage variation, territoriality and breeding displays of the golden plover Pluvialis apricaria in Southwest Scotland. Ibis 124 (1982) 88-95
14. Evans L.T. A study of social hierarchy in the lizard, Anolis carolinensis. J Genet Psychol 48 (1936) 88-111
15. Forster G.L., Watt M.J., Korzan W.J., Renner K.J., and Summers C.H. Opponent recognition in male green anoles, Anolis carolinensis. Anim Behav 69 (2005) 733-740
16. Goldman J.M., and Hadley M.E. In vitro demonstration of adrenergic receptors controlling melanophore responses of the lizard, Anolis carolinensis. J Pharmacol Exp Ther 166 (1969) 1-7
17. 2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29 (1998) 80-83
18. Greenberg B., and Noble G.K. Social behavior of the American chameleon (Anolis carolinensis). Physiol Zool 17 (1944) 392-439
19. Greenberg N. A neuroethological study of display behavior in the lizard, Anolis carolinensis (Reptilia, Lacertilia, Iguanidae). Am Zool 17 (1977) 191-201
20. Greenberg N. A forebrain atlas and stereotaxic technique for the lizard, Anolis carolinensis. J Morphol 174 (1982) 217-236
21. Greenberg N. Central and autonomic aspects of aggression and dominance in reptiles. In: Ewert J.P., Capranica R.R., and Ingle D.J. (Eds). Advances in vertebrate neuroethology (1983), Plenum, New York 1135-1143
22. Greenberg N. Ethological aspects of stress in a model lizard, Anolis carolinensis. Integ Comp Biol 42 (2002) 526-540
23. Greenberg N. Sociality, stress, and the corpus striatum of the green anolis lizard. Physiol Behav 79 (2003) 429-440
24. Greenberg N., and Crews D. Endocrine and behavioral responses to aggression and social dominance in the green anole lizard, Anolis carolinensis. Gen Comp Endocrinol 77 (1990) 246-255
25. Hadley M.E., and Goldman J.M. Physiological color changes in reptiles. Am Zool 9 (1969) 489-504
26. Höglund E., Kolm N., and Winberg S. Stress-induced changes in brain serotonergic activity, plasma cortisol and aggressive behavior in Arctic charr (Salvelinus alpinus) is counteracted by L-DOPA. Physiol Behav 74 (2001) 381-389
27. Höglund E., Korzan W.J., Watt M.J., Forster G.L., Summers T.R., Johannessen H.F., et al. Effects of L-DOPA on aggressive behavior and central monoaminergic activity in the lizard Anolis carolinensis, using a new method for drug delivery. Behav Brain Res 156 (2005) 53-64
28. Jenssen T.A., Greenberg N., and Hovde K.A. Behavioral profile of free-ranging lizards, Anolis carolinensis, across breeding and post-breeding seasons. Herp Monogr 9 (1995) 41-62
29. Jenssen T.A., Lovern M.B., and Congdon J.D. Field-testing the protandry-based mating system for the lizard, Anolis carolinensis: does the model organism have the right model?. Behav Ecol Sociobiol 50 (2001) 162-172
30. Jenssen T.A., and Nuñez S.C. Spatial and breeding relationships of the lizard, Anolis carolinensis: evidence of intrasexual selection. Behaviour 135 (1998) 1003
31. Jenssen T.A., Decourcy K.R., and Congdon J.D. Assessment in contests of male lizards (Anolis carolinensis): how should smaller males respond when size matters?. Anim Behav 69 (2005) 1325-1336
32. Kaplan J.R., Manuck S.B., Fontenot M.B., and Mann J.J. Central nervous system monoamine correlates of social dominance in cynomolgus monkeys (Macaca fascicularis). Neuropsychopharmacology 26 (2002) 431-443
33. Korzan W.J., Forster G.L., Watt M.J., and Summers C.H. Dopaminergic activity modulation via aggression, status and a visual social signal. Behav Neuorsci 120 (2006) 93-102
34. Korzan W.J., Øverli Ø., and Summers C.H. Future social rank: forecasting status in the green anole (Anolis carolinensis). Acta Ethologica 9 (2006) 48-57
35. Korzan W.J., and Summers C.H. Serotonergic response to social stress and artificial social sign stimuli during paired interactions between male Anolis carolinensis. Neuroscience 123 (2004) 835-845
36. Korzan WJ, Summers CH. Behavioral diversity and neurochemical plasticity: Selection of stress coping strategies that define social status. Brain Behav Evol 2007; 70, in press.
37. Korzan W.J., Summers T.R., Ronan P.J., Renner K.J., and Summers C.H. The role of monoaminergic nuclei during aggression and sympathetic social signaling. Brain Behav Evol 57 (2001) 317-327
38. Korzan W.J., Summers T.R., Ronan P.J., and Summers C.H. Visible sympathetic activity as a social signal in Anolis carolinensis: changes in aggression and plasma catecholamines. Horm Behav 38 (2000) 193-199
39. Korzan W.J., Summers T.R., and Summers C.H. Monoaminergic activities of limbic regions are elevated during aggression: influence of sympathetic social signaling. Brain Res 870 (2000) 170-178
40. Korzan W.J., Summers T.R., and Summers C.H. Manipulation of visual sympathetic sign stimulus modifies social status and plasma catecholamines. Gen Comp Endocrinol 128 (2002) 153-161
41. Larson E.T., and Summers C.H. Serotonin reverses dominant social status. Behav Brain Res 121 (2001) 95-102
42. Licht P. Regulation of the annual testis cycle by photoperiod and temperature in the lizard, Anolis carolinensis. Ecology 52 (1971) 240-252
43. Lin P.Y.T., Bulawa M.C., Wong P., Lin L., Scott J., and Blank C.L. The determination of catecholamines, indoleamines and related enzymatic activities using three micron liquid chromatography. J Liq Chromatogr 7 (1984) 509
44. Ling T., Forster G.L., Korzan W.J., Renner K.J., Summers C.H., and Watt M.J. Rapid neuroendocrine responses to restraint stress differ with social status. Soc Neurosci Abs 31 (2005) 57.8
45. Lopez K.H., Jones R.E., Seufert D.W., Rand M.S., and Dores R.M. Catecholaminergic cells and fibers in the brain of the lizard Anolis carolinensis identified by traditional as well as whole-mount immunohistochemistry. Cell Tissue Res 270 (1992) 319-337
46. Lovern M.B., McNabb F.M., and Jenssen T.A. Developmental effects of testosterone on behavior in male and female green anoles (Anolis carolinensis). Horm Behav 39 (2001) 131-143
47. Maaswinkel H., Baars A.M., Gispen W.H., and Spruijt B.M. Roles of the basolateral amygdala and hippocampus in social recognition in rats. Physiol Behav 60 (1996) 55-63
48. Matt K.S., Moore M.C., Knapp R., and Moore I.T. Sympathetic mediation of stress and aggressive competition: plasma catecholamines in free-living male tree lizards. Physiol Behav 61 (1997) 639-647
49. Matter J.M., Ronan P.J., and Summers C.H. Central monoamines in free-ranging lizards: differences associated with social roles and territoriality. Brain Behav Evol 51 (1998) 23-32
50. 2B in the lizard Anolis carolinensis. Neuroscience 128 (2004) 675-684
51. Morgan D., Grant K.A., Prioleau O.A., Nader S.H., Kaplan J.R., and Nader M.A. Predictors of social status in cynomolgus monkeys (Macaca fascicularis) after group formation. Am J Primatol 52 (2000) 115-131
52. Muske L.E., and Fernald R.D. Control of a teleost social signal. I. Neural basis for differential expression of a color pattern. J Comp Physiol [A] 160 (1987) 89-97
53. Muske L.E., and Fernald R.D. Control of a teleost social signal. II. Anatomical and physiological specializations of chromatophores. J Comp Physiol [A] 160 (1987) 99-107
54. Nuñez S.C., Jenssen T.A., and Ersland K. Female activity profile of a polygynous lizard (Anolis carolinensis): evidence of intersexual asymmetry. Behaviour 134 (1997) 205-223
55. Oliveira R.F., Hirschenhauser K., Carneiro L.A., and Canario A.V. Social modulation of androgen levels in male teleost fish. Comp Biochem Physiol B Biochem Mol Biol 132 (2002) 203-215
56. Oliveira R.F., Lopes M., Carneiro L.A., and Canario A.V. Watching fights raises fish hormone levels. Nature 409 (2001) 475
57. Oliveira R.F., McGregor P.K., and Latruffe C. Know thine enemy: fighting fish gather information from observing conspecific interactions. Proc R Soc Lond B Biol Sci 265 (1998) 1045-1049
58. Orrell K.S., and Jenssen T.A. Heterosexual signalling by lizard Anolis carolinensis, with intersexual comparisons across contexts. Behaviour 140 (2003) 603-634
59. Øverli Ø., Korzan W.J., Larson E.T., Winberg S., Lepage O., Pottinger T.G., et al. Behavioral and neuroendocrine correlates of displaced aggression in trout. Horm Behav 45 (2004) 324-329
60. Øverli Ø., Pottinger T.G., Carrick T.R., Overli E., and Winberg S. Brain monoaminergic activity in rainbow trout selected for high and low stress responsiveness. Brain Behav Evol 57 (2001) 214-224
61. Packard M.G., and White N.M. Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists. Behav Neurosci 105 (1991) 295-306
62. Plavicki J., Yang E.-J., and Wilczynski W. Dominance status predicts response to nonsocial forced movement stress in the green anole lizard (Anolis carolinensis). Physiol Behav 80 (2004) 547-555
63. Rand A.S., Ryan M.J., and Wilczynski W. Signal redundancy and receiver permissiveness in acoustic mate recognition by the tungara frog, Physalaemus pustulosus. Am Zool 32 (1992) 81-90
64. Ruby D.E. Male breeding success and differential access to females in Anolis carolinensis. Herpetelogica 40 (1984) 272-280
65. Shannon N.J., Gunnet J.W., and Moore K.E. A comparison of biochemical indices of 5-hydroxytryptaminergic neuronal activity following electrical stimulation of the dorsal raphe nucleus. J Neurochem 47 (1986) 958-965
66. Stamps J.A., and Krishnan V.V. Territory acquisition in lizards. IV. Obtaining high status and exclusive home ranges. Anim Behav 55 (1998) 461-472
67. Sugerman R.A. Observer effects in Anolis sagrei. J Herpetol 24 (1990) 316-317
68. Summers C.H. Mechanisms for quick and variable responses. Brain Behav Evol 57 (2001) 283-292
69. Summers C.H. Social interaction over time, implications for stress responsiveness. Integ Comp Biol 42 (2002) 591-599
70. Summers C.H., Forster G.L., Korzan W.J., Watt M.J., Larson E.T., Overli O., et al. Dynamics and mechanics of social rank reversal. J Comp Physiol A 191 (2005) 241-252
71. Summers C.H., and Greenberg N. Somatic correlates of adrenergic activity during aggression in the lizard, Anolis carolinensis. Horm Behav 28 (1994) 29-40
72. Summers C.H., and Greenberg N. Activation of central biogenic amines following aggressive interaction in male lizards, Anolis carolinensis. Brain Behav Evol 45 (1995) 339-349
73. Summers C.H., Korzan W.J., Lukkes J.L., Øverli Ø., Höglund E., Watt M.J., et al. Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol Biochem Zool 78 (2005) 679-694
74. Summers C.H., Larson E.T., Ronan P.J., Hofmann P.M., Emerson A.J., and Renner K.J. Serotonergic responses to corticosterone and testosterone in the limbic system. Gen Comp Endocrinol 117 (2000) 151-159
75. Summers C.H., Larson E.T., Summers T.R., Renner K.J., and Greenberg N. Regional and temporal separation of serotonergic activity mediating social stress. Neuroscience 87 (1998) 489-496
76. Summers C.H., Summers T.R., Moore M.C., Korzan W.J., Woodley S.K., Ronan P.J., et al. Temporal patterns of limbic monoamine and plasma corticosterone response during social stress. Neuroscience 116 (2003) 553-563
77. Summers C.H., Watt M.J., Ling T.J., Forster G.L., Carpenter R.E., Korzan W.J., et al. Glucocorticoid interaction with aggression in non-mammalian vertebrates: reciprocal action. Eur J Pharmacol 526 (2005) 21-35
78. Summers C.H., and Winberg S. Interactions between the neural regulation of stress and aggression. J Exp Biol 209 (2006) 4581-4589
79. Summers T.R., Hunter A.L., and Summers C.H. Female social reproductive roles affect central monoamines. Brain Res 767 (1997) 272-278
80. Tokarz R.R. Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei). Anim Behav 33 (1985) 746-753
81. 2 receptors in complex maze learning and acetylcholine release in ventral hippocampus of rats. Neuroscience 103 (2001) 27-33
82. van der Vegt B.J., Lieuwes N., van de Wall E.H., Kato K., Moya-Albiol L., Martinez-Sanchis S., et al. Activation of serotonergic neurotransmission during the performance of aggressive behavior in rats. Behav Neurosci 117 (2003) 667-674
83. Vaughan G.L., and Greenberg N. Propranolol, a β-adrenergic antagonist, retards response to MSH in skin of Anolis carolinensis. Physiol Behav 40 (1987) 555-558
84. Winberg S., and Nilsson G.E. Induction of social dominance by L-dopa treatment in Arctic charr. Neuroreport 3 (1992) 243-246
85. Winberg S., and Nilsson G.E. Roles of brain monoamine transmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp Biochem Physiol 106C (1993) 597-614
86. Wingfield J.C., Lynn S., and Soma K.K. Avoiding the 'costs' of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol 57 (2001) 239-251
87. Yang E.J., and Wilczynski W. Social experience organizes parallel networks in sensory and limbic forebrain. Dev Neurobiol 67 (2007) 285-303
88. Yang E.-J., Phelps S.M., Crews D., and Wilczynski W. The effects of social experience on aggressive behavior in Anolis carolinensis. Ethology 107 (2001) 777-793