Frustrative reward omission increases aggressive behaviour of inferior fighters

Proceedings of the Royal Society B: Biological Sciences

Volumn 281, Issue 1784, 2014, Pages

  Vindas, Marco A ^a,b   Johansen, Ida B ^b   Vela Avitua, Sergio ^a   Nørstrud, Karoline Sletbak ^b   Aalgaard, Marion ^c   Braastad, Bjarne O ^a   Höglund, Erik ^d   Øverli, Øyvind ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

^d Nordsocentret   (Denmark)

Author keywords

Aggression; Dyadic contests; Emotions; Frustration; Serotonin; Trace conditioning

Indexed keywords

AGGRESSION; BIOCHEMISTRY; BODY SIZE; COGNITION; CONSPECIFIC; CONTEST COMPETITION; HORMONE; PHYSIOLOGICAL RESPONSE; RESOURCE USE; SALMONID;

ANATOMY AND HISTOLOGY; ANIMAL; EVOLUTION; FOSSIL; PERCIFORMES;

ANATOMY AND HISTOLOGY; ANIMALS; BIOLOGICAL EVOLUTION; FOSSILS; PERCIFORMES;

EID: 84902668574     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2014.0300     Document Type: Article

References (68)

1. Huntingford FA, Turner AK. 1987 Animal conflict. New York, NY: Chapman and Hall.
2. Dugatkin LA, Biederman L. 1991 Balancing asymmetries in resource holding power and resource value in the pumpkinseed sunfish. Anim. Behav. 42, 691-692. (doi:10.1016/S0003-3472(05)80253-2)
3. Enquist M, Leimar O, Ljungberg T, Mallner Y, Segerdahl N. 1990 A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala. Anim. Behav. 40, 1-14. (doi:10.1016/S0003-3472(05)80660-8)
4. Hsu Y, Early RL, Wolf LL. 2011 Aggressive behaviour in fish: integrating information about contest costs. In Fish cognition and behavior, 2nd edn (eds C Brown, K Laland, J Krause), pp. 108-134. Oxford, UK: Wiley-Blackwell.
5. Hsu Y, Lee S-P, Chen M-H, Yang S-Y, Cheng K-C. 2008 Switching assessment strategy during a contest: fighting in killifish Kryptolebias marmoratus. Anim. Behav. 75, 1641-1649. (doi:10.1016/j.anbehav.2007.10.017)
6. Taylor PW, Elwood RW. 2003 The mismeasure of animal contests. Anim. Behav. 65, 1195-1202. (doi:10.1006/anbe.2003.2169)
7. Dugatkin LA, Ohlsen SR. 1990 Contrasting asymmetries in value expectation and resource holding power: effects on attack behaviour and dominance in the pumpkinseed sunfish, Lepomis gibbosus. Anim. Behav. 39, 802-804. (doi:10.1016/ S0003-3472(05)80394-X)
8. Briffa M, Elwood RW. 2009 Difficulties remain in distinguishing between mutual and self-assessment in animal contests. Anim. Behav. 77, 759-762. (doi:10.1016/j.anbehav.2008.11.010)
9. Couppis MH, Kennedy CH. 2008 The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacology 197, 449-456. (doi:10.1007/ s00213-007-1054-y)
10. Nelson RJ, Trainor BC. 2007 Neural mechanisms of aggression. Nat. Rev. Neurosci. 8, 536-546. (doi:10. 1038/nrn2174)
11. Morrison WG. 1996 Instincts as reflex choice: does loss of temper have strategic value? J. Econ. Behav. Organ. 31, 335-356. (doi:10.1016/S0167-2681(96)00878-5)
12. Cristol DA. 1992 Food deprivation influences dominance status in dark-eyed juncos, Junco hyemalis. Anim. Behav. 43, 117-124. (doi:10.1016/ S0003-3472(05)80077-6)
13. Grant JWA, Girard IL, Breau C, Weir LK. 2002 Influence of food abundance on competitive aggression in juvenile convict cichlids. Anim. Behav. 63, 323-330. (doi:10.1006/anbe.2001.1891)
14. Amsel A. 1958 The role of frustrative nonreward in noncontinuous reward situations. Psychol. Bull. 55, 102-119. (doi:10.1037/h0043125)
15. Dantzer R, Arnone M, Mormede P. 1980 Effects of frustration on behaviour and plasma corticosteroid levels in pigs. Physiol. Behav. 24, 1-4. (doi:10. 1016/0031-9384(80)90005-0)
16. David JT, Cervantes MC, Trosky KA, Salinas JA, Delville Y. 2004 A neural network underlying individual differences in emotion and aggression in male golden hamsters. Neuroscience 126, 567-578. (doi:10.1016/j.neuroscience.2004.04.031)
17. de Almeida RMM, Miczek KA. 2002 Aggression escalated by social instigation or by discontinuation of reinforcement ('Frustration') in mice: inhibition by anpirtoline: a 5-HT1B receptor agonist. Neuropsychopharmacology 27, 171-181. (doi:10. 1016/S0893-133X(02)00291-9)
18. Duncan IJH, Wood-Gush DGM. 1971 Frustration and aggression in the domestic fowl. Anim. Behav. 19, 500-504. (doi:10.1016/S0003-3472(71)80104-5)
19. Zimmerman PH, Koene P. 1998 The effect of frustrative nonreward on vocalisations and behaviour in the laying hen, Gallus gallus domesticus. Behav. Process. 44, 73-79. (doi:10. 1016/S0376-6357(98)00035-7)
20. Brown C, Laland K, Krause J. 2011 Fish cognition and behaviour. In Fish cognition and behavior, 2nd edn (eds C Brown, K Laland, J Krause), pp. 1-9. Oxford, UK: Wiley-Blackwell.
21. Magnhagen C, Braithwaite VA, Forsgren E, Kapoor BG. 2008 Fish behaviour. Enfield, NH: Science Publishers.
22. Rose JD. 2007 Anthropomorphism and 'mental welfare' of fishes. Dis. Aquat. Org. 75, 139-154. (doi:10.3354/dao075139)
23. Huntingford FA, Adams C, Braithwaite VA, Kadri S, Pottinger TG, Sandøe P, Turnbull JF. 2006 Current issues in fish welfare. J. Fish Biol. 68, 332-372. (doi:10.1111/j.0022-1112.2006.001046.x)
24. Vindas MA, Folkedal O, Kristiansen TS, Stien LH, Braastad BO, Mayer I, Ø Øverli. 2012 Omission of expected reward agitates Atlantic salmon (Salmo salar). Anim. Cogn. 15, 903-911. (doi:10.1007/ s10071-012-0517-7)
25. Galhardo L, Vital J, Oliveira RF. 2011 The role of predictability in the stress response of a cichlid fish. Physiol. Behav. 102, 367-372. (doi:10.1016/j. physbeh.2010.11.035)
26. Sánchez JA, López-Olmeda JF, Blanco-Vives B, Sánchez-Vázquez FJ. 2009 Effects of feeding schedule on locomotor activity rhythms and stress response in sea bream. Physiol. Behav. 98, 125-129. (doi:10.1016/j.physbeh.2009.04.020)
27. Vindas MA et al. 2014 Coping with unpredictability: dopaminergic and neurotrophic responses to omission of expected reward in Atlantic salmon (Salmo salar L.). PLoS ONE 9, e85543. (doi:10.1371/ journal.pone.0085543)
28. Noakes DLG, Leatherland JF. 1977 Social dominance and interrenal cell activity in rainbow trout, Salmo gairdneri (Pisces, Salmonidae). Environ. Biol. Fish. 2, 131-136. (doi:10.1007/BF00005368)
29. Berejikian BA, Tezak EP, Riley SC, LaRae AL. 2001 Competitive ability and social behaviour of juvenile steelhead reared in enriched and conventional hatchery tanks and a stream environment. J. Fish. Biol 59, 1600-1613. (doi:10.1111/j.1095-8649.2001.tb00224.x)
30. Winberg S, Nilsson GE. 1993 Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish. Comp. Biochem. Physiol. 106C, 597-614.
31. Summers CH, Winberg S. 2006 Interactions between the neural regulation of stress and aggression. J. Exp. Biol. 209, 4581-4589. (doi:10.1242/ jeb.02565)
32. O'Connell LA, Hofmann HA. 2012 Evolution of a vertebrate social decision-making network. Science 336, 1154-1157. (doi:10.1126/science.1218889)
33. O'Connell LA, Hofmann HA. 2011 The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 519, 3599-3639. (doi:10.1002/cne.22735)
34. Nilsson J, Kristiansen TS, Fosseidengen JE, Stien LH, Fernö A, van den Bos R. 2010 Learning and anticipatory behaviour in a 'sit-and-wait' predator: the Atlantic halibut. Behav. Process. 83, 257-266. (doi:10.1016/j.beproc.2009.12.008)
35. Armstrong JL, Boldt JL, Cross AD, Moss JH, Davis ND, Myers KW, Walker RV, Beauchamp DA, Haldorson LJ. 2005 Distribution, size, and interannual, seasonal and diel food habits of northern Gulf of Alaska juvenile pink salmon, Oncorhynchus gorbuscha. Deep Sea Res. 52, 247-265. (doi:10.1016/j.dsr2.2004.09.019)
36. Brown C, Davidson T, Laland K. 2003 Environmental enrichment and prior experience of live prey improve foraging behaviour in hatchery-reared Atlantic salmon. J. Fish Biol. 63, 187-196. (doi:10. 1111/j.1095-8649.2003.00208.x)
37. Jacobsen JA, Hansen LP. 2001 Feeding habits of wild and escaped farmed Atlantic salmon, Salmo salar L, in the Northeast Atlantic. ICES J. Mar. Sci. 58, 916-933. (doi:10.1006/jmsc.2001.1084)
38. Schabetsberger R, Morgan CA, Brodeur RD, Potts CL, Peterson WT, Emmett RL. 2003 Prey selectivity and diel feeding chronology of juvenile chinook (Oncorhynchus tshawytscha) and coho (O. kisutch) salmon in the Columbia River plume. Fish Oceanogr. 12, 523-540. (doi:10.1046/j.1365-2419.2003.00231.x)
39. Sørensen C, Bohlin LC, Øverli Ø, Nilsson GE. 2011 Cortisol reduces cell proliferation in the telencephalon of rainbow trout (Oncorhynchus mykiss). Physiol. Behav. 102, 518-523. (doi:10. 1016/j.physbeh.2010.12.023)
40. Navas JM, Anglade I, Bailhache T, Pakdel F, Breton B, Jégo P, Kah O. 1995 Do gonadotrophin-releasing hormone neurons express estrogen receptors in the rainbow trout? A double immunohistochemical study. J. Comp. Neurol. 363, 461-474. (doi:10. 1002/cne.903630309)
41. Broglio C, Gómez A, Durán E, Salas C, Rodríguez F. 2011 Brain and cognition in teleost fish. In Fish cognition and behavior, 2nd edn (eds C Brown, K Laland, J Krause), pp. 325-358. Oxford, UK: Wiley-Blackwell.
42. Nilsson J, Kristiansen TS, Fosseidengen J, Fernö A, van den Bos R. 2008 Learning in cod (Gadus morhua): long trace interval retention. Anim. Cogn. 11, 215-222. (doi:10.1007/s10071-007-0103-6)
43. Nordgreen J, Janczak A, Hovland A, Ranheim B, Horsberg T. 2010 Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): what do they learn? Anim. Cogn. 13, 303-309. (doi:10.1007/ s10071-009-0267-3)
44. Piper WH. 1990 Site tenacity and dominance in wintering white-throated sparrows Zonotrichia albicollis (Passeriformes: Emberizidae). Ethology 85, 114-122. (doi:10.1111/j.1439-0310.1990. tb00391.x)
45. Winberg S, Øverli Ø, Lepage O. 2001 Suppression of aggression in rainbow trout (Oncorhynchus mykiss) by dietary L-tryptophan. J. Exp. Biol. 204, 3867-3876.
46. Höglund E, Bakke MJ, Øverli Ø, Winberg S, Nilsson GE. 2005 Suppression of aggressive behaviour in juvenile Atlantic cod (Gadus morhua) by l-tryptophan supplementation. Aquaculture 249, 525-531. (doi:10.1016/j.aquaculture.2005.04.028)
47. Andersson MÅ, Höglund E. 2012 Linking personality to larval energy reserves in rainbow trout (Oncorhynchus mykiss). PLoS ONE 7, e49247. (doi:10.1371/journal.pone.0049247)
48. Deckel AW, Fuqua L. 1998 Effects of serotonergic drugs on lateralized aggression and aggressive displays in Anolis carolinensis. Behav. Brain Res. 95, 227-232. (doi:10.1016/S0166-4328(98)00048-5)
49. Larson ET, Summers CH. 2001 Serotonin reverses dominant social status. Behav. Brain Res. 121, 95-102. (doi:10.1016/S0166-4328(00)00393-4)
50. Ferris CF, Melloni Jr RH, Koppel G, Perry KW, Fuller RW, Delville Y. 1997 Vasopressin/serotonin interactions in the anterior hypothalamus control aggressive behavior in golden hamsters. J. Neurosci. 17, 4331-4340.
51. Ison M, Fachinelli C, Echandía ELR. 1996 Effect of the ICV injection of 5, 7-di-hydroxytryptamine on the aggressive behavior of dominant and submissive pigeons (Columba livia). Pharmacol. Biochem. Behav. 53, 951-955. (doi:10.1016/0091-3057(95)02005-5)
52. Summers CH. 1997 Central monoamines in freeranging lizards: differences associated with social roles and territoriality. Brain Behav. Evol. 51, 23-32.
53. Summers CH et al. 2005 Does serotonin influence aggression? Comparing regional activity before and during social interaction. Physiol. Biochem. Zool. 78, 679-694. (doi:10.1086/432139)
54. van Erp AMM, Miczek KA. 2000 Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J. Neurosci. 20, 9320-9325.
55. Winberg S, Nilsson GE, Olsén KH. 1992 Changes in brain serotonergic activity during hierarchic behavior in Arctic charr (Salvelinus alpinus L.) are socially induced. J. Comp. Physiol. 170A, 93-99.
56. Øverli Ø, Harris CA, Winberg S. 1999 Short-term effects of fights for social dominance and the establishment of dominant-subordinate relationships on brain monoamines and cortisol in rainbow trout. Brain Behav. Evol. 54, 263-275. (doi:10.1159/000006627)
57. Winberg S, Carter CG, Mccarthy ID, He ZY, Nilsson GE, Houlihan DF. 1993 Feeding rank and brain serotonergic activity in rainbow trout Oncorhyncus mykiss. J. Exp. Biol. 179, 197-211.
58. Singewald GM, Rjabokon A, Singewald N, Ebner K. 2011 The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacology 36, 793-804. (doi:10. 1038/npp.2010.213)
59. Luo AH, Tahsili-Fahadan P, Wise RA, Lupica CR, Aston-Jones G. 2011 Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 333, 353-357. (doi:10. 1126/science.1204622)
60. Goodson JL, Kingsbury MA. 2013 What's in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks. Horm. Behav. 64, 103-112. (doi:10.1016/j.yhbeh.2013.05.006)
61. Anstrom KK, Miczek KA, Budygin EA. 2009 Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161, 3-12. (doi:10.1016/j.neuroscience.2009.03.023)
62. Tidey JW, Miczek KA. 1996 Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res. 721, 140-149. (doi:10.1016/0006-8993(96) 00159-X)
63. Korzan WJ, Forster GL, Watt MJ, Summers CH. 2006 Dopaminergic activity modulation via aggression, status, and a visual social signal. Behav. Neurosci. 120, 93-102. (doi:10.1037/0735-7044.120.1.93)
64. McIntyre DC, Healy LM, Saari M. 1979 Intraspecies aggression and monoamine levels in rainbow trout (Salmo gairdneri) fingerlings. Behav. Neural Biol. 25, 90-98. (doi:10.1016/S0163-1047(79)90807-0)
65. Winberg S, Nilsson GE. 1992 Induction of social dominance by L-dopa treatment in Arctic charr. Neuroreport 3, 243-246. (doi:10.1097/00001756-199203000-00006)
66. Winberg S, Nilsson GE, Olsén K. 1991 Social rank and brain levels of monoamines and monoamine metabolites in Arctic charr, Salvelinus alpinus (L.). J. Comp. Physiol. 168A, 241-246.
67. Øverli Ø et al. 2004 Stress coping style predicts aggression and social dominance in rainbow trout. Horm. Behav. 45, 235-241. (doi:10.1016/j.yhbeh.2003.12.002)
68. Hess U, Thibault P. 2009 Darwin and emotion expression. Am. Psychol. 64, 120-128. (doi:10. 1037/a0013386)