Dopamine in the nucleus accumbens modulates the memory of social defeat in Syrian hamsters (Mesocricetus auratus)

Behavioural Brain Research

Volumn 286, Issue , 2015, Pages 22-28

  Gray, C L ^a   Norvelle, A ^b   Larkin, T ^b   Huhman, K L ^b  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Aggression; Conditioned defeat; Fear learning; Social stress

Indexed keywords

DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; FLUPENTIXOL; SODIUM CHLORIDE; DOPAMINE RECEPTOR BLOCKING AGENT;

ADULT; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; CONDITIONING; CONTROLLED STUDY; DEFENSIVE BEHAVIOR; DOPAMINE BRAIN LEVEL; EXPERIMENTAL STUDY; MALE; MEMORY; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; SOCIAL BEHAVIOR; SOCIAL STRESS; SUBMISSIVE BEHAVIOR; SYRIAN HAMSTER; TRAINING; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; FEAR; INDWELLING CATHETER; MESOCRICETUS; METABOLISM; PHYSIOLOGY; SOCIAL DOMINANCE;

AGGRESSION; ANIMALS; CATHETERS, INDWELLING; CONDITIONING (PSYCHOLOGY); DOMINANCE-SUBORDINATION; DOPAMINE; DOPAMINE ANTAGONISTS; FEAR; FLUPENTHIXOL; MALE; MEMORY; MESOCRICETUS; NUCLEUS ACCUMBENS; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2;

EID: 84925597431     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2015.02.030     Document Type: Article

References (67)

1. Bonafons C., Jehel L., Coroller-Bequet A. Specificity of the links between workplace harassment and PTSD: primary results using court decisions, a pilot study in France. Int Arch Occup Environ Health 2009, 82:663-668.
2. van Oort F.V., Greaves-Lord K., Ormel J., Verhulst F.C., Huizink A.C. Risk indicators of anxiety throughout adolescence: the TRAILS study. Depress Anxiety 2011, 28:485-494.
3. van Winkel R., Stefanis N.C., Myin-Germeys I. Psychosocial stress and psychosis. A review of the neurobiological mechanisms and the evidence for gene-stress interaction. Schizophr Bull 2008, 34:1095-1105.
4. Lim C., Chong S.A., Keefe R.S. Psychosocial factors in the neurobiology of schizophrenia: a selective review. Ann Acad Med Singapore 2009, 38:402-406.
5. Carvalho S., Pinto-Gouveia J., Pimentel P., Maia D., Gilbert P., Mota-Pereira J. Entrapment and defeat perceptions in depressive symptomatology: through an evolutionary approach. Psychiatry 2013, 76:53-67.
6. Solomon M.B., Karom M.C., Huhman K.L. Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters. Horm Behav 2007, 52:211-219.
7. Jasnow A.M., Huhman K.L. Activation of GABA(A) receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters. Brain Res 2001, 920:142-150.
8. Jasnow A.M., Cooper M.A., Huhman K.L. N-methyl-D-aspartate receptors in the amygdala are necessary for the acquisition and expression of conditioned defeat. Neuroscience 2004, 123:625-634.
9. Jasnow A.M., Shi C., Israel J.E., Davis M., Huhman K.L. Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala. Behav Neurosci 2005, 119:1125-1130.
10. Markham C.M., Taylor S.L., Huhman K.L. Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters. Learn Mem 2010, 17:109-116.
11. Luckett C., Norvelle A., Huhman K. The role of the nucleus accumbens in the acquisition and expression of conditioned defeat. Behav Brain Res 2012, 227:208-214.
12. Rainnie D.G., Mania I., Mascagni F., McDonald A.J. Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 2006, 498:142-161.
13. Rainnie D.G., Asprodini E.K., Shinnick-Gallagher P. Inhibitory transmission in the basolateral amygdala. J Neurophysiol 1991, 66:999-1009.
14. Schotanus S.M., Chergui K. Dopamine D1 receptors and group I metabotropic glutamate receptors contribute to the induction of long-term potentiation in the nucleus accumbens. Neuropharmacology 2008, 54:837-844.
15. Benes F.M. The role of stress and dopamine-GABA interactions in the vulnerability for schizophrenia. J Psychiatr Res 1997, 31:257-275.
16. Glover D.A., Powers M.B., Bergman L., Smits J.A., Telch M.J., Stuber M. Urinary dopamine and turn bias in traumatized women with and without PTSD symptoms. Behav Brain Res 2003, 144:137-141.
17. Drury S.S., Theall K.P., Keats B.J., Scheeringa M. The role of the dopamine transporter (DAT) in the development of PTSD in preschool children. J Trauma Stress 2009, 22:534-539.
18. Oades R.D., Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 1987, 434:117-165.
19. Deutch A.Y., Tam S.Y., Roth R.H. Footshock and conditioned stress increase 3,4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not substantia nigra. Brain Res 1985, 333:143-146.
20. Anstrom K.K., Miczek K.A., Budygin E.A. Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 2009, 161:3-12.
21. Razzoli M., Andreoli M., Michielin F., Quarta D., Sokal D.M. Increased phasic activity of VTA dopamine neurons in mice 3 weeks after repeated social defeat. Behav Brain Res 2011, 218:253-257.
22. Rodaros D., Caruana D.A., Amir S., Stewart J. Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 2007, 150:8-13.
23. Wanat M.J., Hopf F.W., Stuber G.D., Phillips P.E., Bonci A. Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol (Lond) 2008, 586:2157-2170.
24. Chaudhury D., Walsh J.J., Friedman A.K., Juarez B., Ku S.M., Koo J.W., et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 2013, 493:532-536.
25. Tidey J.W., Miczek K.A. Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 1996, 721:140-149.
26. Horvitz J.C. Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum. Behav Brain Res 2002, 137:65-74.
27. Floresco S.B., Blaha C.D., Yang C.R., Phillips A.G. Modulation of hippocampal and amygdalar-evoked activity of nucleus accumbens neurons by dopamine: cellular mechanisms of input selection. J Neurosci 2001, 21:2851-2860.
28. Huhman K.L., Solomon M.B., Janicki M., Harmon A.C., Lin S.M., Israel J.E., et al. Conditioned defeat in male and female Syrian hamsters. Horm Behav 2003, 44:293-299.
29. Landau I.T. Light-dark rhythms in aggressive behavior of the male golden hamster. Physiol Behav 1975, 14:767-774.
30. Guarraci F.A., Frohardt R.J., Falls W.A., Kapp B.S. The effects of intra-amygdaloid infusions of a D2 dopamine receptor antagonist on Pavlovian fear conditioning. Behav Neurosci 2000, 114:647-651.
31. Greba Q., Gifkins A., Kokkinidis L. Inhibition of amygdaloid dopamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res 2001, 899:218-226.
32. Guarraci F.A., Frohardt R.J., Kapp B.S. Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 1999, 827:28-40.
33. Ito R., Hayen A. Opposing roles of nucleus accumbens core and shell dopamine in the modulation of limbic information processing. J Neurosci 2011, 31:6001-6007.
34. Morin L.P., Wood R.J. Atlas of the golden hamster brain 2001, Academic Press, San Diego.
35. McDonald M.M., Markham C.M., Norvelle A., Albers H.E., Huhman K.L. GABAA receptor activation in the lateral septum reduces the expression of conditioned defeat and increases aggression in Syrian hamsters. Brain Res 2012, 1439:27-33.
36. Bahi A., Dreyer J.L. Involvement of nucleus accumbens dopamine D1 receptors in ethanol drinking, ethanol-induced conditioned place preference, and ethanol-induced psychomotor sensitization in mice. Psychopharmacology (Berl) 2012, 222:141-153.
37. Young E.A., Dreumont S.E., Cunningham C.L. Role of nucleus accumbens dopamine receptor subtypes in the learning and expression of alcohol-seeking behavior. Neurobiol Learn Mem 2014, 108:28-37.
38. McFarland K., Kalivas P.W. The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 2001, 21:8655-8663.
39. Bradfield L.A., McNally G.P. The role of nucleus accumbens shell in learning about neutral versus excitatory stimuli during Pavlovian fear conditioning. Learn Mem 2010, 17:337-343.
40. Schwienbacher I., Fendt M., Richardson R., Schnitzler H.U. Temporary inactivation of the nucleus accumbens disrupts acquisition and expression of fear-potentiated startle in rats. Brain Res 2004, 1027:87-93.
41. Fenu S., Bassareo V., Di Chiara G. A role for dopamine D1 receptors of the nucleus accumbens shell in conditioned taste aversion learning. J Neurosci 2001, 21:6897-6904.
42. Campi K.L., Greenberg G.D., Kapoor A., Ziegler T.E., Trainor B.C. Sex differences in effects of dopamine D1 receptors on social withdrawal. Neuropharmacology 2014, 77:208-216.
43. Friedman A.K., Walsh J.J., Juarez B., Ku S.M., Chaudhury D., Wang J., et al. Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science 2014, 344:313-319.
44. Radulovic J., Fischer A., Katerkamp U., Spiess J. Role of regional neurotransmitter receptors in corticotropin-releasing factor (CRF)-mediated modulation of fear conditioning. Neuropharmacology 2000, 39:707-710.
45. Kreibich A.S., Briand L., Cleck J.N., Ecke L., Rice K.C., Blendy J.A. Stress-induced potentiation of cocaine reward: a role for CRF R1 and CREB. Neuropsychopharmacology 2009, 34:2609-2617.
46. Simon H., Taghzouti K., Le Moal M. Deficits in spatial-memory tasks following lesions of septal dopaminergic terminals in the rat. Behav Brain Res 1986, 19:7-16.
47. Schwartzer J.J., Ricci L.A., Melloni R.H. Prior fighting experience increases aggression in Syrian hamsters: implications for a role of dopamine in the winner effect. Aggress Behav 2013, 39:290-300.
48. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.
49. Badrinarayan A., Wescott S.A., Vander Weele C.M., Saunders B.T., Couturier B.E., Maren S., et al. Aversive stimuli differentially modulate real-time dopamine transmission dynamics within the nucleus accumbens core and shell. J Neurosci 2012, 32:15779-15790.
50. Markham C.M., Huhman K.L. Is the medial amygdala part of the neural circuit modulating conditioned defeat in Syrian hamsters. Learn Mem 2008, 15:6-12.
51. Markham C.M., Norvelle A., Huhman K.L. Role of the bed nucleus of the stria terminalis in the acquisition and expression of conditioned defeat in Syrian hamsters. Behav Brain Res 2009, 198:69-73.
52. Alderson H.L., Parkinson J.A., Robbins T.W., Everitt B.J. The effects of excitotoxic lesions of the nucleus accumbens core or shell regions on intravenous heroin self-administration in rats. Psychopharmacology (Berl) 2001, 153:455-463.
53. Gruber A.J., Hussain R.J., O'Donnell P. The nucleus accumbens: a switchboard for goal-directed behaviors. PLoS ONE 2009, 4:e5062.
54. Meredith G.E., Totterdell S. Microcircuits in nucleus accumbens' shell and core involved in cognition and reward. Psychobiology 1999, 27:165-186.
55. Lobo M.K., Zaman S., Damez-Werno D.M., Koo J.W., Bagot R.C., Dinieri J.A., et al. DeltaFosB induction in striatal medium spiny neuron subtypes in response to chronic pharmacological, emotional, and optogenetic stimuli. J Neurosci 2013, 33:18381-18395.
56. Faure A., Reynolds S.M., Richard J.M., Berridge K.C. Mesolimbic dopamine in desire and dread: enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens. J Neurosci 2008, 28:7184-7192.
57. Richard J.M., Plawecki A.M., Berridge K.C. Nucleus accumbens GABAergic inhibition generates intense eating and fear that resists environmental retuning and needs no local dopamine. Eur J Neurosci 2013, 37:1789-1802.
58. Heimer L., Zahm D.S., Churchill L., Kalivas P.W., Wohltmann C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 1991, 41:89-125.
59. Jorgensen A. Pharmacokinetic studies in volunteers of intravenous and oral cis (Z)-flupentixol and intramuscular cis (Z)-flupentixol decanoate in Viscoleo. Eur J Clin Pharmacol 1980, 18:355-360.
60. Hyttel J., Arnt J., van den Berghe M. Selective dopamine D1 and D2 receptor antagonists. Psychopharmacol Ser 1989, 7:109-122.
61. Bourne J.A. SCH 23390: the first selective dopamine D1-like receptor antagonist. CNS Drug Rev 2001, 7:399-414.
62. Young L.T., Wong D.F., Goldman S., Minkin E., Chen C., Matsumura K., et al. Effects of endogenous dopamine on kinetics of [3H]N-methylspiperone and [3H]raclopride binding in the rat brain. Synapse 1991, 9:188-194.
63. Podda M.V., Riccardi E., D'Ascenzo M., Azzena G.B., Grassi C. Dopamine D1-like receptor activation depolarizes medium spiny neurons of the mouse nucleus accumbens by inhibiting inwardly rectifying K+ currents through a cAMP-dependent protein kinase A-independent mechanism. Neuroscience 2010, 167:678-690.
64. Wong S.T., Athos J., Figueroa X.A., Pineda V.V., Schaefer M.L., Chavkin C.C., et al. Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 1999, 23:787-798.
65. West A.R., Floresco S.B., Charara A., Rosenkranz J.A., Grace A.A. Electrophysiological interactions between striatal glutamatergic and dopaminergic systems. Ann NY Acad Sci 2003, 1003:53-74.
66. Camardese G., Di Giuda D., Di Nicola M., Cocciolillo F., Giordano A., Janiri L., et al. Imaging studies on dopamine transporter and depression: a review of literature and suggestions for future research. J Psychiatr Res 2014, 51C:7-18.
67. Corrigan F.M., Fisher J.J., Nutt D.J. Autonomic dysregulation and the Window of Tolerance model of the effects of complex emotional trauma. J Psychopharmacol (Oxf) 2011, 25:17-25.