Endocannabinoids in amygdala and nucleus accumbens mediate social play reward in adolescent rats

Journal of Neuroscience

Volumn 32, Issue 43, 2012, Pages 14899-14908

  Trezza, Viviana ^a,c   Damsteegt, Ruth ^a   Manduca, Antonia ^c   Petrosino, Stefania ^d   van Kerkhof, Linda W M ^a   Jeroen Pasterkamp, R ^a   Zhou, Yeping ^a   Campolongo, Patrizia ^e   Cuomo, Vincenzo ^e   Di Marzo, Vincenzo ^d   Vanderschuren, Louk J M J ^a,b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c ROMA TRE UNIVERSITY   (Italy)

^d CNR   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

2 ARACHIDONOYLGLYCEROL; ANANDAMIDE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; N OLEOYLETHANOLAMINE; PALMIDROL;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; HABITUATION; HIPPOCAMPUS; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SOCIAL BEHAVIOR; SOCIAL INTERACTION; WESTERN BLOTTING;

AMIDOHYDROLASES; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BENZAMIDES; CANNABINOID RECEPTOR AGONISTS; CARBAMATES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCANNABINOIDS; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; INTERPERSONAL RELATIONS; MALE; NUCLEUS ACCUMBENS; PHOSPHOLIPASE D; PHOSPHORYLATION; PIPERIDINES; PLAY AND PLAYTHINGS; PYRAZOLES; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; REWARD;

EID: 84867803397     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0114-12.2012     Document Type: Article

References (78)

1. Balleine BW, Killcross S (2006) Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 29:272-279.
2. Barbano MF, Cador M (2007) Opioids for hedonic experience and dopamine to get ready for it. Psychopharmacology (Berl) 191:497-506.
3. Baxter MG, Murray EA (2002) The amygdala and reward. Nat Rev Neurosci 3:563-573.
4. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369.
5. Berridge KC, Ho CY, Richard JM, DiFeliceantonio AG (2010) The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 1350:43-64.
6. Caillé S, Alvarez-Jaimes L, Polis I, Stouffer DG, Parsons LH (2007) Specific alterations of extracellular endocannabinoid levels in the nucleus accumbens by ethanol, heroin, and cocaine self-administration. J Neurosci 27: 3695-3702.
7. Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51: 667-672.
8. Campolongo P, Roozendaal B, Trezza V, Hauer D, Schelling G, McGaugh JL, Cuomo V (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci U S A 106:4888-4893.
9. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321-352.
10. Chakrabarti B, Baron-Cohen S (2011) Variation in the human cannabinoid receptor CNR1 gene modulates gaze duration for happy faces. Mol Autism 2:10.
11. Chakrabarti B, Kent L, Suckling J, Bullmore E, Baron-Cohen S (2006) Variations in the human cannabinoid receptor (CNR1) gene modulate striatal responses to happy faces. Eur J Neurosci 23:1944-1948.
12. Cota D, Steiner MA, Marsicano G, Cervino C, Herman JP, Grübler Y, Stalla J, Pasquali R, Lutz B, Stalla GK, Pagotto U (2007) Requirement of cannabinoid receptor type 1 for the basal modulation of hypothalamicpituitary- adrenal axis function. Endocrinology 148:1574-1581.
13. Daigle TL, Kwok ML, Mackie K (2008) Regulation of CB1 cannabinoid receptor internalization by a promiscuous phosphorylation-dependent mechanism. J Neurochem 106:70-82.
14. De Petrocellis L, di Marzo V (2009) An introduction to the endocannabinoid system: from the early to the latest concepts. Best Pract Res Clin Endocrinol Metab 23:1-15.
15. di Marzo V (2006) A brief history of cannabinoid and endocannabinoid pharmacology as inspired by the work of British scientists. Trends Pharmacol Sci 27:134-140.
16. di Marzo V (2008) Targeting the endocannabinoid system: to enhance or reduce? Nat Rev Drug Discov 7:438-455.
17. di Marzo V, Ligresti A, Cristino L (2009) The endocannabinoid system as a link between homoeostatic and hedonic pathways involved in energy balance regulation. Int J Obes (Lond) 33 [Suppl 2]:S18-S24.
18. Douglas LA, Varlinskaya EI, Spear LP (2004) Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153-162.
19. Falk JL (1958) The grooming behavior of the chimpanzee as a reinforcer. J Exp Anal Behav 1:83-85.
20. Fattore L, Melis M, Fadda P, Pistis M, Fratta W (2010) The endocannabinoid system and nondrug rewarding behaviours. Exp Neurol 224:23-36.
21. Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017-1066.
22. Garcia DE, Brown S, Hille B, Mackie K (1998) Protein kinase C disrupts cannabinoid actions by phosphorylation of the CB1 cannabinoid receptor. J Neurosci 18:2834-2841.
23. Gardner EL (2005) Endocannabinoid signaling system and brain reward: emphasis on dopamine. Pharmacol Biochem Behav 81:263-284.
24. Guidali C, Viganò D, Petrosino S, Zamberletti E, Realini N, Binelli G, Rubino T, di Marzo V, Parolaro D (2011) Cannabinoid CB1 receptor antagonism prevents neurochemical and behavioural deficits induced by chronic phencyclidine. Int J Neuropsychopharmacol 14:17-28.
25. Hill MN, McLaughlin RJ, Bingham B, Shrestha L, Lee TT, Gray JM, Hillard CJ, Gorzalka BB, Viau V (2010) Endogenous cannabinoid signaling is essential for stress adaptation. Proc Natl Acad Sci U S A 107:9406-9411.
26. Humphreys AP, Einon DF (1981) Play as a reinforcer for maze-learning in juvenile rats. Anim Behav 29:259-270.
27. Ikemoto S (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56:27-78.
28. Ikemoto S, Panksepp J (1992) The effects of early social isolation on the motivation for social play in juvenile rats. Dev Psychobiol 25:261-274.
29. Karst H, Berger S, Erdmann G, Schütz G, Joëls M (2010) Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci U S A 107:14449-14454.
30. Kathuria S, Gaetani S, Fegley D, Valiño F, Duranti A, Tontini A, Mor M, Tarzia G, La Rana G, Calignano A, Giustino A, Tattoli M, Palmery M, Cuomo V, Piomelli D (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat Med 9:76-81.
31. Katona I, Rancz EA, Acsady L, Ledent C, Mackie K, Hajos N, Freund TF (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:9506-9518.
32. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27:765-776.
33. Laviolette SR, Grace AA (2006) The roles of cannabinoid and dopamine receptor systems in neural emotional learning circuits: implications for schizophrenia and addiction. Cell Mol Life Sci 63:1597-1613.
34. Leweke FM, Koethe D (2008) Cannabis and psychiatric disorders: it is not only addiction. Addict Biol 13:264-275.
35. Lutz B (2009) Endocannabinoid signals in the control of emotion. Curr Opin Pharmacol 9:46-52.
36. Mahler SV, Smith KS, Berridge KC (2007) Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances 'liking' of a sweet reward. Neuropsychopharmacology 32: 2267-2278.
37. Marco EM, García-Gutiérrez MS, Bermúdez-Silva FJ, Moreira FA, Guimarães F, Manzanares J, Viveros MP (2011) Endocannabinoid system and psychiatry: in search of a neurobiological basis for detrimental and potential therapeutic effects. Front Behav Neurosci 5:63.
38. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgänsberger W, di Marzo V, Lutz B (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418:530-534.
39. Mason WA, Saxon SV, Sharpe LG (1963) Preferential responses of young chimpanzees to food and social rewards. Psychol Rec 13:341-345.
40. McLaughlin RJ, Gobbi G (2012) Cannabinoids and emotionality: a neuroanatomical perspective. Neuroscience 204:134-144.
41. Niesink RJM, Van Ree JM (1989) Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 28:411-418.
42. Normansell L, Panksepp J (1990) Effects of morphine and naloxone on play-rewarded spatial discrimination in juvenile rats. Dev Psychobiol 23:75-83.
43. Okamoto Y, Morishita J, Tsuboi K, Tonai T, Ueda N (2004) Molecular characterization of a phospholipase D generating anandamide and its congeners. J Biol Chem 279:5298-5305.
44. Orio L, Edwards S, George O, Parsons LH, Koob GF (2009) A role for the endocannabinoid system in the increased motivation for cocaine in extended-access conditions. J Neurosci 29:4846-4857.
45. Pacher P, Bátkai S, Kunos G (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58:389-462.
46. Panksepp J, Siviy S, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465-492.
47. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed 6. San Diego: Elsevier Academic.
48. Peciña S, Berridge KC (2005) Hedonic hot spot in nucleus accumbens shell: where do μ-opioids cause increased hedonic impact of sweetness? J Neurosci 25:11777-11786.
49. Pellis SM, Pellis V (2009) The playful brain: venturing to the limits of neuroscience. Oxford, UK: Oneworld Publications.
50. Phan KL, Angstadt M, Golden J, Onyewuenyi I, Popovska A, de Wit H (2008) Cannabinoid modulation of amygdala reactivity to social signals of threat in humans. J Neurosci 28:2313-2319.
51. Piomelli D (2003) The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4:873-884.
52. Rozen S, Skaletsky H (2000) Primer3 on theWWWfor general users and for biologist programmers. Methods Mol Biol 132:365-386.
53. Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5:34-41.
54. Shinohara Y, Inui T, Yamamoto T, Shimura T (2009) Cannabinoid in the nucleus accumbens enhances the intake of palatable solution. Neuroreport 20:1382-1385.
55. Simmons D, Self DW (2009) Role of mu- and delta-opioid receptors in the nucleus accumbens in cocaine-seeking behavior. Neuropsychopharmacology 34:1946-1957.
56. Siviy SM, Panksepp J (2011) In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 35:1821-1830.
57. Solinas M, Goldberg SR, Piomelli D (2008) The endocannabinoid system in brain reward processes. Br J Pharmacol 154:369-383.
58. Soria-Gómez E, Matias I, Rueda-Orozco PE, Cisneros M, Petrosino S, Navarro L, di Marzo V, Prospéro-García O (2007) Pharmacological enhancement of the endocannabinoid system in the nucleus accumbens shell stimulates food intake and increases c-Fos expression in the hypothalamus. Br J Pharmacol 151:1109-1116.
59. Spano MS, Fadda P, Fratta W, Fattore L (2010) Cannabinoid-opioid interactions in drug discrimination and self-administration: effect of maternal, postnatal, adolescent and adult exposure to the drugs. Curr Drug Targets 11:450-461.
60. Thiel KJ, Okun AC, Neisewander JL (2008) Social reward-conditioned place preference: a model revealing an interaction between cocaine and social context rewards in rats. Drug Alcohol Depend 96:202-212.
61. Thiel KJ, Sanabria F, Neisewander JL (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology (Berl) 204:391-402.
62. Trezza V, Vanderschuren LJMJ (2008a) Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl) 197:217-227.
63. Trezza V, Vanderschuren LJMJ (2008b) Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. Eur Neuropsychopharmacol 18:519-530.
64. Trezza V, Vanderschuren LJMJ (2009) Divergent effects of anandamide transporter inhibitors with different target selectivity on social play behavior in adolescent rats. J Pharmacol Exp Ther 328:343-350.
65. Trezza V, Damsteegt R, Vanderschuren LJMJ (2009) Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol 19:659-669.
66. Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463-469.
67. Trezza V, Damsteegt R, Achterberg EJM, Vanderschuren LJMJ (2011a) Nucleus accumbens μ-opioid receptors mediate social reward. J Neurosci 31:6362-6370.
68. Trezza V, Campolongo P, Vanderschuren LJMJ (2011b) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1:444-458.
69. Tsou K, Brown S, Sañudo-Peña MC, Mackie K, Walker JM (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
70. van der Stelt M, di Marzo V (2003) The endocannabinoid system in the basal ganglia and in the mesolimbic reward system: implications for neurological and psychiatric disorders. Eur J Pharmacol 480:133-150.
71. Vanderschuren LJMJ, Niesink RJM, Spruijt BM, Van Ree JM (1995) Effects of morphine on different aspects of social play in juvenile rats. Psychopharmacology 117:225-231.
72. Vanderschuren LJMJ, Niesink RJM, Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309-326.
73. Vanderschuren LJMJ, Trezza V, Griffioen-Roose S, Schiepers OJG, Van Leeuwen N, De Vries TJ, Schoffelmeer ANM (2008) Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 33:2946-2956.
74. Viveros MP, Marco EM, Llorente R, López-Gallardo M (2007) Endocannabinoid system and synaptic plasticity: implications for emotional responses. Neural Plast 2007:52908.
75. Voorn P, Vanderschuren LJMJ, Groenewegen HJ, Robbins TW, Pennartz CMA (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27:468-474.
76. Wotjak CT (2005) Role of endogenous cannabinoids in cognition and emotionality. Mini Rev Med Chem 5:659-670.
77. Zanettini C, Panlilio LV, Alicki M, Goldberg SR, Haller J, Yasar S (2011) Effects of endocannabinoid system modulation on cognitive and emotional behavior. Front Behav Neurosci 5:57.
78. Zhou Y, Adolfs Y, Pijnappel WW, Fuller SJ, Van der Schors RC, Li KW, Sugden PH, Smit AB, Hergovich A, Pasterkamp RJ (2011) MICAL-1 is a negative regulator of MST-NDR kinase signaling and apoptosis. Mol Cell Biol 31:3603-3615.