Decreased reward sensitivity in rats from the fischer344 strain compared to wistar rats is paralleled by differences in endocannabinoid signaling

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Brand, Theresa ^a   Spanagel, Rainer ^a   Schneider, Miriam ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; AMIDASE; FATTY-ACID AMIDE HYDROLASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME PHOSPHORYLATION; FISCHER 344 RAT; FOOD INTAKE; HIPPOCAMPUS; LOCOMOTION; MALE; MILK; NONHUMAN; NUCLEUS ACCUMBENS; PALATABLE FOOD REWARD; PLEASURE; PREFRONTAL CORTEX; PROTEIN EXPRESSION; RAT; REWARD; SIGNAL TRANSDUCTION; STARTLE REFLEX; STRAIN DIFFERENCE; WESTERN BLOTTING; WISTAR RAT; ANIMAL; BRAIN LEVEL; METABOLISM; PHYSIOLOGY; SPECIES DIFFERENCE;

RATTUS; RATTUS NORVEGICUS;

AMIDOHYDROLASES; ANIMALS; BRAIN CHEMISTRY; ENDOCANNABINOIDS; HIPPOCAMPUS; RATS; RATS, INBRED F344; RATS, WISTAR; RECEPTOR, CANNABINOID, CB1; REWARD; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84856742758     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031169     Document Type: Article

References (71)

1. Bagg HJ, (1920) Individual differences and family resemblance in animal behavior. Archives of psychology ed New York The Science Press.
2. Yilmazer-Hanke DM, (2008) Morphological correlates of emotional and cognitive behaviour: insights from studies on inbred and outbred rodent strains and their crosses. Behav Pharmacol 19: 403-434.
3. Rodgers RJ, Cole JC, (1993) Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice. Physiol Behav 54: 729-736.
4. Rex A, Sondern U, Voigt JP, Franck S, Fink H, (1996) Strain differences in fear-motivated behavior of rats. Pharmacol Biochem Behav 54: 107-111.
5. Ramos A, Berton O, Mormede P, Chaouloff F, (1997) A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85: 57-69.
6. Griebel G, Belzung C, Perrault G, Sanger DJ, (2000) Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychopharmacology (Berl) 148: 164-170.
7. Shepard JD, Myers DA, (2008) Strain differences in anxiety-like behavior: association with corticotropin-releasing factor. Behav Brain Res 186: 239-245.
8. Shoaib M, Spanagel R, Stohr T, Shippenberg TS, (1995) Strain differences in the rewarding and dopamine-releasing effects of morphine in rats. Psychopharmacology (Berl) 117: 240-247.
9. Suzuki T, Koike Y, Yanaura S, George FR, Meisch RA, (1987) Genetic differences in the development of physical dependence on pentobarbital in four inbred strains of rats. Jpn J Pharmacol 45: 479-486.
10. Kosten TA, Miserendino MJ, Haile CN, DeCaprio JL, Jatlow PI, et al. (1997) Acquisition and maintenance of intravenous cocaine self-administration in Lewis and Fischer inbred rat strains. Brain Res 778: 418-429.
11. Bolanos CA, Barrot M, Berton O, Wallace-Black D, Nestler EJ, (2003) Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54: 1317-1329.
12. Palm S, Roman E, Nylander I, (2011) Differences in voluntary ethanol consumption in Wistar rats from five different suppliers. Alcohol 45: 607-614.
13. Freeman KB, Kearns DN, Kohut SJ, Riley AL, (2009) Strain differences in patterns of drug-intake during prolonged access to cocaine self-administration. Behav Neurosci 123: 156-164.
14. Gosnell BA, Krahn DD, (1993) Morphine-induced feeding: a comparison of the Lewis and Fischer 344 inbred rat strains. Pharmacol Biochem Behav 44: 919-924.
15. Kearns DN, Gomez-Serrano MA, Weiss SJ, Riley AL, (2006) A comparison of Lewis and Fischer rat strains on autoshaping (sign-tracking), discrimination reversal learning and negative auto-maintenance. Behav Brain Res 169: 193-200.
16. Solinas M, Goldberg SR, Piomelli D, (2008) The endocannabinoid system in brain reward processes. Br J Pharmacol 154: 369-383.
17. Cota D, Tschop MH, Horvath TL, Levine AS, (2006) Cannabinoids, opioids and eating behavior: the molecular face of hedonism? Brain Res Rev 51: 85-107.
18. Kirkham TC, (2009) Cannabinoids and appetite: food craving and food pleasure. Int Rev Psychiatry 21: 163-171.
19. Maldonado R, Valverde O, Berrendero F, (2006) Involvement of the endocannabinoid system in drug addiction. Trends Neurosci 29: 225-232.
20. Arnold JC, Topple AN, Mallet PE, Hunt GE, McGregor IS, (2001) The distribution of cannabinoid-induced Fos expression in rat brain: differences between the Lewis and Wistar strain. Brain Res 921: 240-255.
21. Arnold JC, Dielenberg RA, McGregor IS, (2010) Cannabinoids increase conditioned ultrasonic vocalisations and cat odour avoidance in rats: strain differences in drug-induced anxiety. Life Sci 87: 572-578.
22. Gardner EL, Paredes W, Smith D, Donner A, Milling C, et al. (1988) Facilitation of brain stimulation reward by delta 9-tetrahydrocannabinol. Psychopharmacology (Berl) 96: 142-144.
23. Lepore M, Vorel SR, Lowinson J, Gardner EL, (1995) Conditioned place preference induced by delta 9-tetrahydrocannabinol: comparison with cocaine, morphine, and food reward. Life Sci 56: 2073-2080.
24. Deiana S, Fattore L, Spano MS, Cossu G, Porcu E, et al. (2007) Strain and schedule-dependent differences in the acquisition, maintenance and extinction of intravenous cannabinoid self-administration in rats. Neuropharmacology 52: 646-654.
25. Stohr T, Schulte WD, Weiner I, Feldon J, (1998) Rat strain differences in open-field behavior and the locomotor stimulating and rewarding effects of amphetamine. Pharmacol Biochem Behav 59: 813-818.
26. Bert B, Fink H, Huston JP, Voits M, (2002) Fischer 344 and wistar rats differ in anxiety and habituation but not in water maze performance. Neurobiol Learn Mem 78: 11-22.
27. Rex A, Voigt JP, Fink H, (1999) Behavioral and neurochemical differences between Fischer 344 and Harlan-Wistar rats raised identically. Behav Genet 29: 187-192.
28. Schneider M, Spanagel R, (2008) Appetitive odor-cue conditioning attenuates the acoustic startle response in rats. Behav Brain Res 189: 226-230.
29. Schneider M, Heise V, Spanagel R, (2010) Differential involvement of the opioid receptor antagonist naloxone in motivational and hedonic aspects of reward. Behav Brain Res 208: 466-472.
30. Friemel CM, Spanagel R, Schneider M, (2010) Reward sensitivity for a palatable food reward peaks during pubertal developmental in rats. Front Behav Neurosci 4: 39.
31. Tordoff MG, Alarcon LK, Lawler MP, (2008) Preferences of 14 rat strains for 17 taste compounds. Physiol Behav 95: 308-332.
32. Koch M, Schmid A, Schnitzler HU, (2000) Role of the nucleus accumbens dopamine D1 and D2 receptors in instrumental and Pavlovian paradigms of conditioned reward. Psychopharmacology 152: 67-73.
33. Arnone M, Maruani J, Chaperon F, Thiebot M, Poncelet M, et al. (1997) Selective inhibition of sucrose and ethanol intake by SR 1411716, an antagonist of central cannabinoid (CB1) receptors. Psychopharmacology 132: 104-106.
34. McLaughlin PJ, Winston KM, Limebeer CL, Parker LA, Makriyannis A, et al. (2005) The cannabinoid CB1 antagonist AM 251 produces food avoidance and behaviors associated with nausea but does not impair feeding efficiency in rats. Psychopharmacology (Berl) 180: 286-293.
35. McLaughlin PJ, Qian L, Wood JT, Wisniecki A, Winston KM, et al. (2006) Suppression of food intake and food-reinforced behavior produced by the novel CB1 receptor antagonist/inverse agonist AM 1387. Pharmacol Biochem Behav 83: 396-402.
36. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM, (1998) Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83: 393-411.
37. Egertova M, Giang DK, Cravatt BF, Elphick MR, (1998) A new perspective on cannabinoid signalling: complementary localization of fatty acid amide hydrolase and the CB1 receptor in rat brain. Proc Biol Sci 265: 2081-2085.
38. Bouaboula M, Poinot-Chazel C, Bourrie B, Canat X, Calandra B, et al. (1995) Activation of mitogen-activated protein kinases by stimulation of the central cannabinoid receptor CB1. Biochem J 312 (Pt 2): 637-641.
39. Wartmann M, Campbell D, Subramanian A, Burstein SH, Davis RJ, (1995) The MAP kinase signal transduction pathway is activated by the endogenous cannabinoid anandamide. FEBS Lett 359: 133-136.
40. Derkinderen P, Valjent E, Toutant M, Corvol JC, Enslen H, et al. (2003) Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. J Neurosci 23: 2371-2382.
41. Pertwee RG, (2005) Inverse agonism and neutral antagonism at cannabinoid CB1 receptors. Life Sci 76: 1307-1324.
42. Bergman J, Delatte MS, Paronis CA, Vemuri K, Thakur GA, et al. (2008) Some effects of CB1 antagonists with inverse agonist and neutral biochemical properties. Physiol Behav 93: 666-670.
43. Lange JH, Kruse CG, (2005) Keynote review: Medicinal chemistry strategies to CB1 cannabinoid receptor antagonists. Drug Discov Today 10: 693-702.
44. Gardner EL, (2005) Endocannabinoid signaling system and brain reward: Emphasis on dopamine. Pharmacol Biochem Behav 81: 263-284.
45. Tzschentke T, (2000) The medial prefrontal cortex as a part of the brain reward system. Amino Acids 19: 219.
46. Tracy AL, Jarrard LE, Davidson TL, (2001) The hippocampus and motivation revisited: appetite and activity. Behav Brain Res 127: 13-23.
47. Harrold JA, Elliott JC, King PJ, Widdowson PS, Williams G, (2002) Down-regulation of cannabinoid-1 (CB-1) receptors in specific extrahypothalamic regions of rats with dietary obesity: a role for endogenous cannabinoids in driving appetite for palatable food? Brain Res 952: 232-238.
48. Fattore L, Vigano D, Fadda P, Rubino T, Fratta W, et al. (2007) Bidirectional regulation of mu-opioid and CB1-cannabinoid receptor in rats self-administering heroin or WIN 55,212-2. Eur J Neurosci 25: 2191-2200.
49. Schmelzeis MC, Mittleman G, (1996) The hippocampus and reward: effects of hippocampal lesions on progressive-ratio responding. Behav Neurosci 110: 1049-1066.
50. Mittleman G, Whishaw IQ, Jones GH, Koch M, Robbins TW, (1990) Cortical, hippocampal, and striatal mediation of schedule-induced behaviors. Behav Neurosci 104: 399-409.
51. Zhang PW, Ishiguro H, Ohtsuki T, Hess J, Carillo F, et al. (2004) Human cannabinoid receptor 1: 5′ exons, candidate regulatory regions, polymorphisms, haplotypes and association with polysubstance abuse. Mol Psychiatry 9: 916-931.
52. Zuo L, Kranzler HR, Luo X, Covault J, Gelernter J, (2007) CNR1 variation modulates risk for drug and alcohol dependence. Biol Psychiatry 62: 616-626.
53. Zuo L, Kranzler HR, Luo X, Yang BZ, Weiss R, et al. (2009) Interaction between two independent CNR1 variants increases risk for cocaine dependence in European Americans: a replication study in family-based sample and population-based sample. Neuropsychopharmacology 34: 1504-1513.
54. Benyamina A, Kebir O, Blecha L, Reynaud M, Krebs MO, (2010) CNR1 gene polymorphisms in addictive disorders: a systematic review and a meta-analysis. Addict Biol.
55. Filbey FM, Schacht JP, Myers US, Chavez RS, Hutchison KE, (2010) Individual and additive effects of the CNR1 and FAAH genes on brain response to marijuana cues. Neuropsychopharmacology 35: 967-975.
56. Di Marzo V, Goparaju SK, Wang L, Liu J, Batkai S, et al. (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410: 822-825.
57. Sanchis-Segura C, Cline BH, Marsicano G, Lutz B, Spanagel R, (2004) Reduced sensitivity to reward in CB1 knockout mice. Psychopharmacology (Berl) 176: 223-232.
58. Poncelet M, Maruani J, Calassi R, Soubrie P, (2003) Overeating, alcohol and sucrose consumption decrease in CB1 receptor deleted mice. Neurosci Lett 343: 216-218.
59. Thanos PK, Dimitrakakis ES, Rice O, Gifford A, Volkow ND, (2005) Ethanol self-administration and ethanol conditioned place preference are reduced in mice lacking cannabinoid CB1 receptors. Behav Brain Res 164: 206-213.
60. Merritt LL, Martin BR, Walters C, Lichtman AH, Damaj MI, (2008) The endogenous cannabinoid system modulates nicotine reward and dependence. J Pharmacol Exp Ther 326: 483-492.
61. Ward SJ, Walker EA, (2009) Sex and cannabinoid CB1 genotype differentiate palatable food and cocaine self-administration behaviors in mice. Behav Pharmacol 20: 605-613.
62. 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.
63. Salamone JD, Correa M, Farrar A, Mingote SM, (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191: 461-482.
64. Berridge KC, (1996) Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20: 1-25.
65. Kelley AE, Bakshi VP, Haber SN, Steininger TL, Will MJ, et al. (2002) Opioid modulation of taste hedonics within the ventral striatum. Physiol Behav 76: 365-377.
66. 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.
67. Solinas M, Goldberg SR, (2005) Motivational effects of cannabinoids and opioids on food reinforcement depend on simultaneous activation of cannabinoid and opioid systems. Neuropsychopharmacology 30: 2035-2045.
68. Tanda G, Munzar P, Goldberg SR, (2000) Self-administration behavior is maintained by the psychoactive ingredient of marijuana in squirrel monkeys. Nat Neurosci 3: 1073-1074.
69. 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.
70. Lupica CR, Riegel AC, (2005) Endocannabinoid release from midbrain dopamine neurons: a potential substrate for cannabinoid receptor antagonist treatment of addiction. Neuropharmacology 48: 1105-1116.
71. Lopez-Moreno JA, Lopez-Jimenez A, Gorriti MA, de Fonseca FR, (2010) Functional interactions between endogenous cannabinoid and opioid systems: focus on alcohol, genetics and drug-addicted behaviors. Curr Drug Targets 11: 406-428.