The decision to fight or flee - insights into underlying mechanism in crickets

Frontiers in Neuroscience

Volumn , Issue AUG, 2012, Pages

  Stevenson, Paul A ^a   Rillich, Jan ^b  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Aggression; Assessment; Biogenic amines; Decision making; Experience dependent plasticity; Motivation; Octopamine insects

Indexed keywords

ADRENALIN; NEUROPEPTIDE; NORADRENALIN; OCTOPAMINE;

AGGRESSION; ANIMAL BEHAVIOR; ANTENNA (ORGAN); CRICKET; DECISION MAKING; FIGHTING; FLIGHT; MOTOR ACTIVITY; NONHUMAN; ORTHOPTERA; REVIEW;

EID: 84866352739     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00118     Document Type: Review

References (95)

1. Adamo, S. A., Linn, C. E., and Hoy, R. R. (1995). The role of neurohormonal octopamine during "fight or flight" behavior in the field cricket Gryllus bimaculatus. J. Exp. Biol. 198, 1691-1700.
2. Alekseyenko, O. V., Lee, C., and Kravitz, E. A. (2010). Targeted manipulation of serotonergic seurotransmission affects the escalation of aggression in adult male Drosophila melanogaster. PLoS ONE 5, e10806. doi:10.1371/journal.pone.0010806
3. Alexander, R. D. (1961). Aggressiveness, territoriality, and sexual behavior in field crickets (Orthoptera: Gryllidae). Behavior 17, 130-223.
4. Anstey, M. L., Rogers, S. M., Ott, S. R., Burrows, M., and Simpson, S. J. (2009). Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323, 627-630.
5. Baba, Y., Tsukada, A., and Comer, C. M. (2010). Collision avoidance in running insects: antennal guidance in cockroaches. J. Exp. Biol. 213, 2294-2302.
6. Baier, A., Wittek, B., and Brembs, B. (2002). Drosophila as a new model organism for the neurobiology of aggression? J. Exp. Biol. 205, 1233-1240.
7. Barron, A. B., Maleszka, R., Helliwell, P. G., and Robinson, G. E. (2009). Effects of cocaine on honey bee dance behavior. J. Exp. Biol. 212, 163-168.
8. Barron, A. B., Sovik, E., and Cornish, J. (2010). The roles of dopamine and related compounds in rewardseeking behavior across animals phyla. Front. Behav. Neurosci. 4:163. doi:10.3389/fnbeh.2010.00163
9. Baudoux, S., Duch, C., and Morris, O. T. (1998). Coupling of efferent neuromodulatory neurons to rhythmical leg motor activity in the locust. J. Neurophysiol. 79, 361-370.
10. Bradbury, W. J., and Vehrencamp, L. (1998). Principles of Animal Communication. Sunderland, MA: Sinauer, 771-782.
11. Bräunig, P., and Pflüger, H. J. (2001). The unpaired median neurons of insects. Adv. Insect Physiol. 28, 185-266.
12. Briffa, M., and Elwood, R. W. (2005). Rapid change in energy status in fighting animals: causes and effects of strategic decisions. Anim. Behav. 70, 119-124.
13. Buhl, E., Schildberger, K., and Stevenson, P. A. (2008). A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J. Exp. Biol. 211, 2346-2357.
14. Bullerjahn, A., Mentel, T., Pflüger, H. J., and Stevenson, P. A. (2006). Nitric oxide: a co-modulator of efferent peptidergic neurosecretory cells including a unique octopaminergic neuron innervating locust heart. Cell Tissue Res. 325, 345-360.
15. Carre, J. M., and Putnam, S. K. (2010). Watching a previous victory produces an increase in testosterone among elite hockey players. Psychoneuroendocrinology 35, 475-479
16. Cattaert, D., Delbecque, J. P., Edwards, D. H., and Issa, F. A. (2010). Social interactions determine postural network sensitivity to 5-HT. J. Neurosci. 30, 5603-5616.
17. Certel, S. J., Leung, A., Lin, C. Y., Perez, P., Chiang, A. S., and Kravitz, E. A. (2010). Octopamine neuromodulatory effects on a social behavior decisionmaking network in Drosophila males. PLoS ONE 5, e13248. doi:10.1371/journal.pone.0013248
18. Certel, S. J., Savella, M. G., Schlegel, D. C., and Kravitz, E. A. (2007). Modulation of Drosophila male behavioral choice. Proc. Natl. Acad. Sci. U.S.A. 104, 4706-4711.
19. Chan, Y. B., and Kravitz, E. (2007). Specific subgroups of FruM neurons control sexually dimorphic patterns of aggression in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 104, 9577-9582.
20. Craft, L. L., and Perna, F. M. (2004). The benefits of exercise for the clinically depressed. J. Clin. Psychiatry 6, 104-111.
21. Cromarty, S. I., Mello, J., and KassSimon, G. (1999). Time in residence affects escape and agonistic behavior in adult male American lobsters. Biol. Bull. 196, 105-112.
22. Darwin, C. (1859). The Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. London: John Murray.
23. de Boer,S. F.,and Koolhaas,J. M. (2005). 5-HT1A and 5-HT1B receptor agonists and aggression:a pharmacological challenge of the serotonin deficiency hypothesis. Eur. J. Pharmacol. 526, 125-139.
24. Dierick, H. A., and Greenspan, R. J. (2007). Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39, 678-682.
25. Dixon, K. A., and Cade, W. H. (1986). Some factors influencing male maleaggression in the field cricket Gryllus integer (time of day, age, weight and sexual maturity). Anim. Behav. 34, 340-346.
26. Duch, C., Mentel, T., and Pflüger, H. J. (1999). Distribution and activation of different types of octopaminergic DUM neurons in the locust. J. Comp. Neurol. 403, 119-134.
27. Dyakonova, V., Schurmann, F. W., and Sakharov, D. A. (2002). Effects of opiate ligands on intraspecific aggression in crickets. Peptides 23, 835-841.
28. Dyakonova, V. E., and Krushinskii, A. L. (2006). Effects of an NO synthase inhibitor on aggressive and sexual behavior in male crickets. Neurosci. Behav. Physiol. 36, 565-571.
29. Dyakonova, V. E., Schurmann, F., and Sakharov, D. A. (1999). Effects of serotonergic and opioidergic drugs on escape behaviors and social status of male crickets. Naturwissenschaften 86, 435-437.
30. Edwards, A. C., Zwarts, L., Yamamoto, A., Callaerts, P., and Mackay, T. F. (2009). Mutations in many genes affect aggressive behavior in Drosophila melanogaster. BMC Biol. 7, 29. doi:10.1186/1741-7007-7-29
31. Edwards, D. H., and Spitzer, N. (2006). Social dominance and serotonin receptors in crayfish (review). Curr. Top. Dev. Biol. 74, 177-199.
32. Erber, J., Kloppenburg, P., and Scheidler, A. (1993). Neuromodulation by serotonin and octopamine in the honeybee: behavior, neuroanatomy and electrophysiology. Experientia 49, 1073-1083.
33. Evans, P. D. (1985). "Octopamine," in Comprehensive Insect Physiology Biochemistry and Pharmacology, eds G. A. Kerkut and L. I. Gilbert (Pergamon: Oxford), 499-530.
34. Fernandez, M. P., Chan, Y. B., Yew, J. Y., Billeter, J. C., Dreisewerd, K., Levine, J. D., and Kravitz, E. A. (2010). Pheromonal and behavioral cues trigger male-to-female aggression in Drosophila. PLoS Biol. 8, e1000541. doi:10.1371/journal.pbio.1000541
35. Ghosal, K., Gupta, M., and Killian, K. A. (2009). Agonistic behavior enhances adult neurogenesis in male Acheta domesticus crickets. J. Exp. Biol. 212, 2045-2056.
36. Ghosal, K., Naples, S. P., Rabe, A. R., and Killian, K. A. (2010). Agonistic behavior and electrical stimulation of the antennae induces FOSlike protein expression in the male cricket brain. Arch. Insect Biochem. Physiol. 74, 38-51.
37. Glimcher, P. W., Camerer, C. F., Fehr, E., and Poldrack, R. A. (eds). (2009). Neuroeconomics: Decision Making and the Brain. New York: Academic Press.
38. Hack, M. A. (1997). The energetic costs of fighting in the house cricket, Acheta domesticus L. Behav. Ecol. 8, 28-36.
39. Hall, M. D., Mclaren, L., Brooks, R. C., and Lailvaux, S. P. (2010). Interactions among performance capacities predict male combat outcomes in the field cricket. Funct. Ecol. 24, 159-164.
40. Hammer, M. (1993). An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366, 59-63.
41. Hammer, M., and Menzel, R. (1995). Learning and memory in the honey bee. J. Neurosci. 15, 1617-1630.
42. Hofmann, H. A. (1996). The cultural history of Chinese fighting crickets: a contribution not only to the history of biology. Biol. Zent. Bl. 115, 206-213.
43. Hofmann, H. A., and Schildberger, K. (2001). Assessment of strength and willingness to fight during aggressive encounters in crickets. Anim. Behav. 62, 337-348.
44. Hofmann, H. A., and Stevenson, P. A. (2000). Flight restores fight in crickets. Nature 403, 613-613.
45. Hoyer, S. C., Eckart, A., Herrel, A., Zars, T., Fischer, S. A., Hardie, S. L., and Heisenberg, M. (2008). Octopamine in male aggression of Drosophila. Curr. Biol. 18, 159-167.
46. Hsu, Y., Earley, R. L., and Wolf, L. L. (2006). Modulation of aggressive behavior by fighting experience: mechanisms and contest outcomes. Biol. Rev. Camb. Philos. Soc. 81, 33-74.
47. Hsu,Y.Y.,Lee,I. H.,and Lu,C. K. (2009). Prior contest information: mechanisms underlying winner and loser effects. Behav. Ecol. Sociobiol. (Print) 63, 1247-1257.
48. Huber, F. (1960). Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirnes bei der Fortbewegung und der Lauterzeugung der Grillen. ZeitschriftfürvergleichendeTierphysiologie 44, 60-132.
49. Huber, F., Moore, T. E., and Loher, W. (1989). Cricket Behavior and Neurobiology. New York: Cornell University.
50. Hurd, P. L. (2006). Resource holding potential, subjective resource value, and game theoretical models of aggressiveness signaling. J. Theor. Biol. 241, 639-648.
51. Iwasaki, M., Delago, A., Nishino, H., and Aonuma, H. (2006). Effects of previous experience on the agonistic behavior of male crickets, Gryllus bimaculatus. Zool. Sci. 23, 863-872
52. Iwasaki, M., and Katagiri, C. (2008). Cuticular lipids and odors induce sex-specific behaviors in the male cricket Gryllus bimaculatus. Comp. Biochem. Physiol. A 149, 306-313.
53. Iwasaki, M., Nishino, H., Delago, A., and Aonuma, H. (2007). Effects of NO/cGMP signaling on behavioral changes in subordinate male crickets, Gryllus bimaculatus. Zool. Sci. 24, 860-868.
54. Johnson, O., Becnel, J., and Nichols, C. D. (2009). Serotonin 5-HT(2) and 5-HT(1A)-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158, 1292-1300.
55. Judge, K. A., and Bonanno, V. L. (2008). Male weaponry in a fighting cricket. PLoS ONE 3, e3980. doi:10.1371/journal.pone.0003980
56. Kemp, D. J., and Wiklund, C. (2004). Residency effects in animal contests. Proc. R. Soc. Lond. B Biol. Sci. 271, 1707-1711.
57. Khazraie, K., and Campan, M. (1999). The role of prior agonistic experience in dominance relationships in male crickets Gryllus bimaculatus (Orthoptera: Gryllidae). Behav. Process. 44, 341-348.
58. Killian, K. A., and Allen, J. R. (2008). Mating resets male cricket aggression. J. Insect Behav. 21, 535-548.
59. Kravitz, E. A., and Huber, R. (2003). Aggression in invertebrates. Curr. Opin. Neurobiol. 13, 736-743.
60. Maynard Smith, J., and Price, G. R. (1973). The logic of animal conflict. Nature 246, 15-18.
61. Mizunami, M., Unoki, S., Mori, Y., Hirashima, D., Hatano, A., and Matsumoto, Y. (2009). Roles of octopaminergic and dopaminergic neurons in appetitive and aversive memory recall in an insect. BMC Biol. 7, 46. doi:10.1186/1741-70077-46
62. Morris, O. T., Duch, C., and Stevenson, P. A. (1999). Differential activation of octopaminergic (DUM) neurons via proprioceptors responding to flight muscle contractions in the locust. J. Exp. Biol. 202, 3555-3564.
63. Murakami, S., and Itoh, M. T. (2001). Effects of aggression and wing removal on brain serotonin levels in male crickets, Gryllus bimaculatus. J. Insect Physiol. 47, 1309-1312.
64. Nelson, R. J. (2006). Biology of Aggression. Oxford: Oxford University Press.
65. Nelson, R. J., and Trainor, B. C. (2007). Neural mechanisms of aggression. Nat. Rev. Neurosci. 8, 536-546.
66. Nilsen, S. P., Chan, Y. B., Huber, R., and Kravitz, E. A. (2004). Genderselective patterns of aggressive behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 101, 12342-12347.
67. Nosil, P. (2002). Food fights in house crickets, Acheta domesticus, and the effects of body size and hunger level. Can. J. Zool. 80, 409-417.
68. O'Connell, L. A., and Hofmann, H. A. (2011). The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 519, 3599-3639.
69. Oliveira, R. F., Silva, A., and Canario, A. V. M. (2009). Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish. Proc. R. Soc. Lond. B Biol. Sci. 276, 2249-2256.
70. Parker, G. A. (1974). Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47, 223-243.
71. Payne,R. J. H. (1998). Gradually escalating fights and displays: the cumulative assessment model. Anim. Behav. 56, 651-662.
72. Pflüger, H., and Stevenson, P. A. (2005). Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct. Dev. 34, 379-396.
73. Raichlen, D. A., Foster, A. D., Gerdeman, G. L., Seillier,A., and Giuffrida, A. (2011). Wired to run: exerciseinduced endocannabinoid signaling in humans and cursorial mammals with implications for the 'runner's high'. J. Exp. Biol. 215, 1331-1336.
74. Rillich, J., Buhl, E., Schildberger, K., and Stevenson, P. A. (2009). Female crickets are driven to fight by the male courting and calling songs. Anim. Behav. 77, 737-742.
75. Rillich, J., Schildberger, K., and Stevenson, P. A. (2007). Assessment strategy of fighting crickets revealed by manipulating information exchange. Anim. Behav. 74, 823-836
76. Rillich, J., Schildberger, K., and Stevenson, P. A. (2011). Octopamine and occupancy an aminergic mechanism for intruder-resident aggression in crickets. Proc. R. Soc. Lond. B Biol. Sci. 278, 1873-1880.
77. Rillich, J., and Stevenson, P. A. (2011). Winning fights induces hyperaggression via the action of the biogenic amine octopamine in crickets. PLoS ONE 6, e28891. doi:10.1371/journal.pone.0028891
78. Robinson, E. J. H., Franks, N. R., Ellis, S., Okuda, S., and Marshall, J. A. R. (2011). A simple threshold rule is sufficient to explain sophisticated collective decisionmaking. Plos One 6, e19981. doi:10.1371/journal.pone.0019981
79. Rodriguez-Munoz, R., Bretman, A., and Tregenza, T. (2011). Guarding males protect females from predation in a wild insect. Curr. Biol. 21, 1716-1719.
80. Rutte, C., Taborsky, M., and Brinkhof, M. W. (2006). What sets the odds of winning and losing? Trends Ecol. Evol. 21, 16-21.
81. Schöneich, S., Schildberger, K., and Stevenson, P. A. (2011). Neuronal organization of a fast-mediating cephalo-thoracic pathway for antennal-tactile information in the cricket. J. Comp. Neurol. 519, 1677-1690.
82. Schröter, U., Malun, D., and Menzel, R. (2007). Innervation pattern of suboesophageal ventral unpaired median neurons in the honeybee brain. Cell Tissue Res. 327, 647-667
83. Schwärzel, M., Monastirioti, M., Scholz, H., Friggi-Grelin, F., Birman, S., and Heisenberg, M. (2003). Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J. Neurosci. 23, 10495-10502.
84. Simmons, L. W. (1986). Inter-male competition and mating success in the field cricket, Gryllus bimaculatus (de Geer). Anim. Behav. 34, 567-579.
85. Simpson, S. J., and Stevenson, P. A. (2012). Neuromodulation of Social Behavior in Insects, in Oxford Handbook of Molecular Psychology. Oxford: Oxford University Press.
86. Stevenson,P.A. (2011)." Neurochemical control of the decision to flight or flee in crickets," in Ninth Göttingen Meeting of the German Neuroscience Society, Goettingen, S20/26.
87. Stevenson, P. A., Dyakonova, V., Rillich, J., and Schildberger, K. (2005). Octopamine and experience-dependent modulation of aggression in crickets. J. Neurosci. 25, 1431-1441.
88. Stevenson, P. A., Hofmann, H. A., Schoch, K., and Schildberger, K. (2000). The fight and flight responses of crickets depleted of biogenic amines. J. Neurobiol. 43, 107-120.
89. Stevenson, P. A., and Sporhase Eichmann, U. (1995). Localization of octopaminergic neurons in insects. Comp. Biochem. Physiol. B 11, 203-215.
90. Tops, M., Russo, S., Boksem, M. A., and Tucker, D. M. (2009). Serotonin: modulator of a drive to withdraw. Brain Cogn. 71, 427-436.
91. Verlinden, H., Vleugels, R., Marchal, E., Badisco, L., Pflüger, H. J., Blenau, W., and Broeck, J. V. (2010). The role of octopamine in locusts and other arthropods. J. Insect Physiol. 56, 854-867.
92. Vrontou, E., Nilsen, S. P., Demir, E., Kravitz, E. A., and Dickson, B. J. (2006). Fruitless regulates aggression and dominance in Drosophila. Nat. Neurosci. 9, 1469-1471.
93. Wang, L., and Anderson, D. J. (2010). Identification of an aggressionpromoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231.
94. Yurkovic, A., Wang Basu, C., and Kravitz, E. A. (2006). Learning and memory associated with aggression in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 103, 17519-17524.
95. Zhou, C., Rao, Y., and Rau, Y. (2008). A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 11, 1059-1067.