Persistent conditioned place preference to aggression experience in adult male sexually-experienced CD-1 mice

Genes, Brain and Behavior

Volumn 16, Issue 1, 2017, Pages 44-55

  Golden, S A ^a   Aleyasin, H ^b   Heins, R ^a   Flanigan, M ^b   Heshmati, M ^b   Takahashi, A ^b,c   Russo, S J ^b   Shaham, Y ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Aggression; CD 1; conditioned place preference; D1 Cre; D2 Cre; food self administration; mice; punishment; reward

Indexed keywords

ADULT; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL FOOD; ARTICLE; C57BL 6 MOUSE; CD-1 MOUSE; CONTROLLED STUDY; FEMALE; FOOTSHOCK; HYBRID MOUSE STRAIN; MALE; MOUSE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PUNISHMENT; RESIDENT-INTRUDER TEST; ANIMAL; C57BL MOUSE; CONDITIONING; HYBRIDIZATION; PHENOTYPE; REINFORCEMENT; SEXUAL BEHAVIOR; SPATIAL BEHAVIOR;

AGGRESSION; ANIMALS; CONDITIONING (PSYCHOLOGY); HYBRIDIZATION, GENETIC; MALE; MICE; MICE, INBRED C57BL; PHENOTYPE; REINFORCEMENT (PSYCHOLOGY); SEXUAL BEHAVIOR, ANIMAL; SPATIAL BEHAVIOR;

EID: 84982227548     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12310     Document Type: Article

References (63)

1. de Almeida, R.M. & Miczek, K.A. (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.
2. Anderson, N.E. & Kiehl, K.A. (2014) Psychopathy and aggression: when paralimbic dysfunction leads to violence. Curr Top Behav Neurosci 17, 369–393.
3. Azrin, N.H. (1970) Punishment of elicited aggression. J Exp Anal Behav 14, 7–10.
4. Azrin, N.H., Hutchinson, R.R. & Hake, D.F. (1967) Attack, avoidance, and escape reactions to aversive shock. J Exp Anal Behav 10, 131–148.
5. Baenninger, R. & Grossman, J.C. (1969) Some effects of punishment on pain-elicited aggression. J Exp Anal Behav 12, 1017–1022.
6. Bandler, R.J. Jr. (1969) Facilitation of aggressive behaviour in rat by direct cholinergic stimulation of the hypothalamus. Nature 224, 1035–1036.
7. Beck, A., Heinz, A.J. & Heinz, A. (2014) Translational clinical neuroscience perspectives on the cognitive and neurobiological mechanisms underlying alcohol-related aggression. Curr Top Behav Neurosci 17, 443–474.
8. Bouton, M.E. & Schepers, S.T. (2015) Renewal after the punishment of free operant behavior. J Exp Psychol Anim Learn Cogn 41, 81–90.
9. Calu, D.J., Chen, Y.W., Kawa, A.B., Nair, S.G. & Shaham, Y. (2014) The use of the reinstatement model to study relapse to palatable food seeking during dieting. Neuropharmacology 76 Pt B, 395–406.
10. Caprioli, D., Venniro, M., Zeric, T., Li, X., Adhikary, S., Madangopal, R., Marchant, N.J., Lucantonio, F., Schoenbaum, G., Bossert, J.M. & Shaham, Y. (2015a) Effect of the novel positive allosteric modulator of metabotropic glutamate receptor 2 AZD8529 on incubation of methamphetamine craving after prolonged voluntary abstinence in a rat model. Biol Psychiatry 78, 463–473.
11. Caprioli, D., Zeric, T., Thorndike, E.B. & Venniro, M. (2015b) Persistent palatable food preference in rats with a history of limited and extended access to methamphetamine self-administration. Addict Biol 20, 913–926.
12. Couppis, M.H. & Kennedy, C.H. (2008) The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacology (Berl) 197, 449–456.
13. Da Vanzo, J.P., Daugherty, M., Ruckart, R. & Kang, L. (1966) Pharmacological and biochemical studies in isolation-induced fighting mice. Psychopharmacologia 9, 210–219.
14. Deroche-Gamonet, V., Belin, D. & Piazza, P.V. (2004) Evidence for addiction-like behavior in the rat. Science 305, 1014–1017.
15. Dolenc, B., Dernovsek, M.Z., Sprah, L., Tavcar, R., Perugi, G. & Akiskal, H.S. (2015) Relationship between affective temperaments and aggression in euthymic patients with bipolar mood disorder and major depressive disorder. J Affect Disord 174, 13–18.
16. Elbert, T., Weierstall, R. & Schauer, M. (2010) Fascination violence: on mind and brain of man hunters. Eur Arch Psychiatry Clin Neurosci 260 (Suppl 2), S100–S105.
17. van Erp, A.M. & Miczek, K.A. (2000) Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20, 9320–9325.
18. van Erp, A.M. & Miczek, K.A. (2007) Increased accumbal dopamine during daily alcohol consumption and subsequent aggressive behavior in rats. Psychopharmacology (Berl) 191, 679–688.
19. Evans, W.O. (1961) A new technique for the investigation of some analgesic drugs on a reflexive behavior in the rat. Psychopharrnacologia 2, 318–325.
20. Falkner, A.L., Grosenick, L., Davidson, T.J., Deisseroth, K. & Lin, D. (2016) Hypothalamic control of male aggression-seeking behavior. Nat Neurosci 19, 596–604.
21. Fish, E.W., De Bold, J.F. & Miczek, K.A. (2002) Aggressive behavior as a reinforcer in mice: activation by allopregnanolone. Psychopharmacology (Berl) 163, 459–466.
22. Glusman, M. & Roizin, L. (1960) Role of the hypothalamus in the organization of agonistic behavior in the cat. Trans Am Neurol Assoc 85, 177–181.
23. Golden, S.A., Covington, H.E. III, Berton, O. & Russo, S.J. (2011) A standardized protocol for repeated social defeat stress in mice. Nat Protoc 6, 1183–1191.
24. Golden, S.A., Heshmati, M., Flanigan, M., Christoffel, D.J., Guise, K., Pfau, M.L., Aleyasin, H., Menard, C., Zhang, H., Hodes, G.E., Bregman, D., Khibnik, L., Tai, J., Rebusi, N., Krawitz, B., Chaudhury, D., Walsh, J.J., Han, M.H., Shapiro, M.L. & Russo, S.J. (2016) Basal forebrain projections to the lateral habenula modulate aggression reward. Nature 534, 688–692.
25. Hill, A.P., Zuckerman, K.E., Hagen, A.D., Kriz, D.J., Duvall, S.W., van Santen, J., Nigg, J., Fair, D. & Fombonne, E. (2014) Aggressive behavior problems in children with autism spectrum disorders: prevalence and correlates in a large clinical sample. Res Autism Spectr Disord 8, 1121–1133.
26. Krasnova, I.N., Marchant, N.J., Ladenheim, B., McCoy, M.T., Panlilio, L.V., Bossert, J.M., Shaham, Y. & Cadet, J.L. (2014) Incubation of methamphetamine and palatable food craving after punishment-induced abstinence. Neuropsychopharmacology 39, 2008–2016.
27. Krishnan, V., Han, M.H., Graham, D.L. et al. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391–404.
28. Kudryavtseva, N.N., Bakshtanovskaya, I.V. & Koryakina, L.A. (1991) Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav 38, 315–320.
29. Kudryavtseva, N.N., Bondar, N.P. & Avgustinovich, D.F. (2004) Effects of repeated experience of aggression on the aggressive motivation and development of anxiety in male mice. Neurosci Behav Physiol 34, 721–730.
30. Kudryavtseva, N.N., Smagin, D.A., Kovalenko, I.L. & Vishnivetskaya, G.B. (2014) Repeated positive fighting experience in male inbred mice. Nat Protoc 9, 2705–2717.
31. Lenoir, M., Serre, F., Cantin, L. & Ahmed, S.H. (2007) Intense sweetness surpasses cocaine reward. PLoS One 2, e698.
32. Levine, L., Barsel, G.E. & Diakow, C.A. (1965) Interaction of aggressive and sexual behavior in male mice. Behaviour 25, 272–280.
33. Lin, D., Boyle, M.P., Dollar, P., Lee, H., Lein, E.S., Perona, P. & Anderson, D.J. (2011) Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221–226.
34. Lipp, H.P. & Hunsperger, R.W. (1978) Threat, attack and flight elicited by electrical stimulation of the ventromedial hypothalamus of the marmoset monkey Callithrix jacchus. Brain Behav Evol 15, 260–293.
35. Macdonnell, M.F. & Flynn, J.P. (1964) Attack elicited by stimulation of the thalamus of cats. Science 144, 1249–1250.
36. Marchant, N.J., Khuc, T.N., Pickens, C.L., Bonci, A. & Shaham, Y. (2013) Context-induced relapse to alcohol seeking after punishment in a rat model. Biol Psychiatry 73, 256–262.
37. Marchant, N.J., Rabei, R., Kaganovsky, K., Caprioli, D., Bossert, J.M., Bonci, A. & Shaham, Y. (2014) A critical role of lateral hypothalamus in context-induced relapse to alcohol seeking after punishment-imposed abstinence. J Neurosci 34, 7447–7457.
38. Marchant, N.J., Campbell, E.J., Whitaker, L.R., Harvey, B.K., Kaganovsky, K., Adhikary, S., Hope, B.T., Heins, R.C., Prisinzano, T.E., Vardy, E., Bonci, A., Bossert, J.M. & Shaham, Y. (2016) Role of ventral subiculum in context-induced relapse to alcohol seeking after punishment-imposed abstinence. J Neurosci 36, 3281–3294.
39. Martinez, M., Guillen-Salazar, F., Salvador, A. & Simon, V.M. (1995) Successful intermale aggression and conditioned place preference in mice. Physiol Behav 58, 323–328.
40. May, M.E. (2011) Aggression as positive reinforcement in people with intellectual disabilities. Res Dev Disabil 32, 2214–2224.
41. May, M.E. & Kennedy, C.H. (2009) Aggression as positive reinforcement in mice under various ratio- and time-based reinforcement schedules. J Exp Anal Behav 91, 185–196.
42. Meisel, R.L. & Joppa, M.A. (1994) Conditioned place preference in female hamsters following aggressive or sexual encounters. Physiol Behav 56, 1115–1118.
43. Miczek, K.A. & O'Donnell, J.M. (1978) Intruder-evoked aggression in isolated and nonisolated mice: effects of psychomotor stimulants and L-dopa. Psychopharmacology (Berl) 57, 47–55.
44. Miczek, K.A., DeBold, J.F. & Thompson, M.L. (1984) Pharmacological, hormonal, and behavioral manipulations in analysis of aggressive behavior. Prog Clin Biol Res 167, 1–26.
45. Miles, S.R., Menefee, D.S., Wanner, J., Teten Tharp, A. & Kent, T.A. (2015) The relationship between emotion dysregulation and impulsive aggression in veterans with posttraumatic stress disorder symptoms. J Interpers Violence 31, 1795–1816. doi: 10.1177/0886260515570746.
46. Moran, J.K., Weierstall, R. & Elbert, T. (2014) Differences in brain circuitry for appetitive and reactive aggression as revealed by realistic auditory scripts. Front Behav Neurosci 8, 425.
47. Mucha, R.F., van der Kooy, D., O'Shaughnessy, M. & Bucenieks, P. (1982) Drug reinforcement studied by the use of place conditioning in rat. Brain Res 243, 91–105.
48. Mueller, D. & Stewart, J. (2000) Cocaine-induced conditioned place preference: reinstatement by priming injections of cocaine after extinction. Behav Brain Res 115, 39–47.
49. Mueller, D., Perdikaris, D. & Stewart, J. (2002) Persistence and drug-induced reinstatement of a morphine-induced conditioned place preference. Behav Brain Res 136, 389–397.
50. O'Kelly, L. & Steckle, L. (1939) A note on long enduring emotional responses in the rat. J Psychol 8, 125.
51. Oyegbile, T.O. & Marler, C.A. (2005) Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm Behav 48, 259–267.
52. Pelloux, Y., Everitt, B.J. & Dickinson, A. (2007) Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology (Berl) 194, 127–137.
53. Roberts, C.L. & Blase, K. (1971) Elicitation and punishment of intraspecies aggression by the same stimulus. J Exp Anal Behav 15, 193–196.
54. Silva, B.A., Mattucci, C., Krzywkowski, P., Murana, E., Illarionova, A., Grinevich, V., Canteras, N.S., Ragozzino, D. & Gross, C.T. (2013) Independent hypothalamic circuits for social and predator fear. Nat Neurosci 16, 1731–1733.
55. Stephens, D.N., Duka, T., Crombag, H.S., Cunningham, C.L., Heilig, M. & Crabbe, J.C. (2010) Reward sensitivity: issues of measurement, and achieving consilience between human and animal phenotypes. Addict Biol 15, 145–168.
56. Swanson, J.W., Swartz, M.S., Van Dorn, R.A., Elbogen, E.B., Wagner, H.R., Rosenheck, R.A., Stroup, T.S., McEvoy, J.P. & Lieberman, J.A. (2006) A national study of violent behavior in persons with schizophrenia. Arch Gen Psychiatry 63, 490–499.
57. Takahashi, A., Lee, R.X., Iwasato, T., Itohara, S., Arima, H., Bettler, B., Miczek, K.A. & Koide, T. (2015) Glutamate input in the dorsal raphe nucleus as a determinant of escalated aggression in male mice. J Neurosci 35, 6452–6463.
58. Tellegen, A. & Horn, J.M. (1972) Primary aggressive motivation in three inbred strains of mice. J Comp Physiol Psychol 78, 297–304.
59. Toth, M., Fuzesi, T., Halasz, J., Tulogdi, A. & Haller, J. (2010) Neural inputs of the hypothalamic “aggression area” in the rat. Behav Brain Res 215, 7–20.
60. Ulrich, R., Wolfe, M. & Dulaney, S. (1969) Punishment of shock-induced aggression. J Exp Anal Behav 12, 1009–1015.
61. Van der Kooy, D. (1987) Place conditioning: a simple and effective method for assessing the motivational properties of drugs. In Bozarth, M.A. (ed), Methods of Assessing the Reinforcing Properties of Abused Drugs. Springer-Verlag, New York, pp. 229–240.
62. Vernon, W. & Ulrich, R. (1966) Classical conditioning of pain-elicited aggression. Science 152, 668–669.
63. Wise, R.A. (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5, 483–494.