Insulin induces long-term depression of ventral tegmental area dopamine neurons via endocannabinoids

Nature Neuroscience

Volumn 16, Issue 3, 2013, Pages 300-308

  Labouèbe, Gwenaël ^a,b   Liu, Shuai ^a,c   Dias, Carine ^a   Zou, Haiyan ^a   Wong, Jovi C Y ^a   Karunakaran, Subashini ^a   Clee, Susanne M ^a   Phillips, Anthony G ^a   Boutrel, Benjamin ^b   Borgland, Stephanie L ^a,c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCANNABINOID; GLUTAMIC ACID; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTICIPATION; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; FEEDING; HUNGER; LIPID DIET; LONG TERM DEPRESSION; MALE; MOUSE; NONHUMAN; OBESITY; PLACE PREFERENCE; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; REWARD; SATIETY; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CYTOLOGY; DRUG EFFECT; FAT INTAKE; FEEDING BEHAVIOR; LEARNING; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; DIETARY FATS; DOPAMINERGIC NEURONS; ENDOCANNABINOIDS; FEEDING BEHAVIOR; GLUTAMIC ACID; INSULIN; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTIC TRANSMISSION; TOR SERINE-THREONINE KINASES; VENTRAL TEGMENTAL AREA;

MLCS; MLOWN;

EID: 84875906445     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3321     Document Type: Article

References (57)

1. Gerozissis, K. Brain insulin, energy and glucose homeostasis; genes, environment and metabolic pathologies. Eur. J. Pharmacol. 585, 38-49 (2008).
2. Palmiter, R.D. Is dopamine a physiologically relevant mediator of feeding behavior? Trends Neurosci. 30, 375-381 (2007). (Pubitemid 47088716)
3. Bonci, A. & Malenka, R.C. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J. Neurosci. 19, 3723-3730 (1999). (Pubitemid 29222248)
4. Overton, P.G., Richards, C.D., Berry, M.S. & Clark, D. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuroreport 10, 221-226 (1999). (Pubitemid 29104790)
5. Borgland, S.L. et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J. Neurosci. 29, 11215-11225 (2009).
6. Borgland, S.L., Taha, S.A., Sarti, F., Fields, H.L. & Bonci, A. Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49, 589-601 (2006). (Pubitemid 43221893)
7. Abizaid, A. et al. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J. Clin. Invest. 116, 3229-3239 (2006). (Pubitemid 44878637)
8. Thompson, J.L. & Borgland, S.L. A role for hypocretin/orexin in motivation. Behav. Brain Res. 217, 446-453 (2011).
9. Baskin, D.G. et al. Insulin and leptin: dual adiposity signals to the brain for the regulation of food intake and body weight. Brain Res. 848, 114-123 (1999). (Pubitemid 30001660)
10. Woods, S.C., Seeley, R.J., Baskin, D.G. & Schwartz, M.W. Insulin and the blood-brain barrier. Curr. Pharm. Des. 9, 795-800 (2003). (Pubitemid 36367601)
11. Hommel, J.D. et al. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51, 801-810 (2006). (Pubitemid 44374908)
12. Fulton, S. et al. Leptin regulation of the mesoaccumbens dopamine pathway. Neuron 51, 811-822 (2006). (Pubitemid 44374918)
13. Figlewicz, D.P., Evans, S.B., Murphy, J., Hoen, M. & Baskin, D.G. Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res. 964, 107-115 (2003). (Pubitemid 36165075)
14. Figlewicz, D.P., Bennett, J.L., Naleid, A.M., Davis, C. & Grimm, J.W. Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol. Behav. 89, 611-616 (2006). (Pubitemid 44634584)
15. Figlewicz, D.P. et al. Intraventricular insulin and leptin reverse place preference conditioned with high-fat diet in rats. Behav. Neurosci. 118, 479-487 (2004). (Pubitemid 38685315)
16. Sipols, A.J., Bayer, J., Bennett, R. & Figlewicz, D.P. Intraventricular insulin decreases kappa opioid-mediated sucrose intake in rats. Peptides 23, 2181-2187 (2002). (Pubitemid 36092052)
17. Figlewicz, D.P., Bennett, J.L., Aliakbari, S., Zavosh, A. & Sipols, A.J. Insulin acts at different CNS sites to decrease acute sucrose intake and sucrose self-administration in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R388-R394 (2008).
18. Mebel, D.M., Wong, J.C., Dong, Y.J. & Borgland, S.L. Insulin in the ventral tegmental area reduces hedonic feeding and suppresses dopamine concentration via increased reuptake. Eur. J. Neurosci. 36, 2336-2346 (2012).
19. Bruijnzeel, A.W., Corrie, L.W., Rogers, J.A. & Yamada, H. Effects of insulin and leptin in the ventral tegmental area and arcuate hypothalamic nucleus on food intake and brain reward function in female rats. Behav. Brain Res. 219, 254-264 (2011).
20. Overton, P.G. & Clark, D. Burst firing in midbrain dopamine neurons. Brain Res. Brain Res. Rev. 25, 312-334 (1997). (Pubitemid 28070309)
21. Watabe-Uchida, M., Zhu, L., Ogawa, S.K., Vamanrao, A. & Uchida, N. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74, 858-873 (2012).
22. Wang, Y.T. & Linden, D.J. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25, 635-647 (2000).
23. Man, H.Y. et al. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25, 649-662 (2000).
24. Baltensperger, K. et al. Catalysis of serine and tyrosine autophosphorylation by the human insulin receptor. Proc. Natl. Acad. Sci. USA 89, 7885-7889 (1992).
25. Schäffer, L. et al. A novel high-affinity peptide antagonist to the insulin receptor. Biochem. Biophys. Res. Commun. 376, 380-383 (2008).
26. Vigneri, R., Squatrito, S. & Sciacca, L. Insulin and its analogs: actions via insulin and IGF receptors. Acta Diabetol. 47, 271-278 (2010).
27. Asnaghi, L., Bruno, P., Priulla, M. & Nicolin, A. mTOR: a protein kinase switching between life and death. Pharmacol. Res. 50, 545-549 (2004). (Pubitemid 39388965)
28. Mameli, M., Balland, B., Lujan, R. & Lüscher, C. Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science 317, 530-533 (2007). (Pubitemid 47196120)
29. Lee, S.H., Liu, L., Wang, Y.T. & Sheng, M. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36, 661-674 (2002). (Pubitemid 35346759)
30. Malinow, R. & Malenka, R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126 (2002). (Pubitemid 34748013)
31. Lüscher, C. et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649-658 (1999).
32. Kauer, J.A. & Malenka, R.C. Synaptic plasticity and addiction. Nat. Rev. Neurosci. 8, 844-858 (2007). (Pubitemid 350006216)
33. Katz, B. Quantal mechanism of neural transmitter release. Science 173, 123-126 (1971).
34. Melis, M. et al. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J. Neurosci. 24, 53-62 (2004). (Pubitemid 38181669)
35. Heifets, B.D. & Castillo, P.E. Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol. 71, 283-306 (2009).
36. Bisogno, T. et al. Brain regional distribution of endocannabinoids: implications for their biosynthesis and biological function. Biochem. Biophys. Res. Commun. 256, 377-380 (1999). (Pubitemid 29298893)
37. Blum, I.D., Waddington-Lamont, E., Rodrigues, T. & Abizaid, A. Isolating neural correlates of the pacemaker for food anticipation. PLoS ONE 7, e36117 (2012).
38. Ahn, S. & Phillips, A.G. Dopaminergic correlates of sensory-specific satiety in the medial prefrontal cortex and nucleus accumbens of the rat. J. Neurosci. 19, RC29 (1999).
39. Sanchis-Segura, C. & Spanagel, R. Behavioural assessment of drug reinforcement and addictive features in rodents: an overview. Addict. Biol. 11, 2-38 (2006). (Pubitemid 46696746)
40. Pan, B., Hillard, C.J. & Liu, Q.S. Endocannabinoid signaling mediates cocaine-induced inhibitory synaptic plasticity in midbrain dopamine neurons. J. Neurosci. 28, 1385-1397 (2008). (Pubitemid 351231531)
41. Henny, P. et al. Structural correlates of heterogeneous in vivo activity of midbrain dopaminergic neurons. Nat. Neurosci. 15, 613-619 (2012).
42. Grueter, B.A., Brasnjo, G. & Malenka, R.C. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Nat. Neurosci. 13, 1519-1525 (2010).
43. Gerdeman, G.L., Ronesi, J. & Lovinger, D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5, 446-451 (2002). (Pubitemid 34454250)
44. Ronesi, J., Gerdeman, G.L. & Lovinger, D.M. Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J. Neurosci. 24, 1673-1679 (2004). (Pubitemid 38240964)
45. Yin, H.H., Davis, M.I., Ronesi, J.A. & Lovinger, D.M. The role of protein synthesis in striatal long-term depression. J. Neurosci. 26, 11811-11820 (2006). (Pubitemid 44772091)
46. Massa, F. et al. Alterations in the hippocampal endocannabinoid system in diet-induced obese mice. J. Neurosci. 30, 6273-6281 (2010).
47. Lüscher, C. & Malenka, R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 69, 650-663 (2011).
48. Duckworth, W.C., Bennett, R.G. & Hammel, F.G. Insulin degradation: progress and potential. Endocr. Rev. 19, 608-624 (1998). (Pubitemid 28467714)
49. Tsai, H.C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084 (2009).
50. Stuber, G.D. et al. Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 321, 1690-1692 (2008).
51. Yoshizaki, T. et al. Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells. Neurosci. Lett. 363, 33-37 (2004). (Pubitemid 38659556)
52. Johnson, S.W. & North, R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. (Lond.) 450, 455-468 (1992).
53. Lacey, M.G., Mercuri, N.B. & North, R.A. Actions of cocaine on rat dopaminergic neurones in vitro. Br. J. Pharmacol. 99, 731-735 (1990). (Pubitemid 20111315)
54. Richardson, N.R. & Roberts, D.C. Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J. Neurosci. Methods 66, 1-11 (1996). (Pubitemid 26180064)
55. Schoffelmeer, A.N. et al. Insulin modulates cocaine-sensitive monoamine transporter function and impulsive behavior. J. Neurosci. 31, 1284-1291 (2011).
56. Paxinos, G. & Watson, C. The Rat Brain in Sterotaxic Coordinates (Academic, New York, 1997).
57. Brebner, K. et al. Nucleus accumbens long-term depression and the expression of behavioral sensitization. Science 310, 1340-1343 (2005). (Pubitemid 41698868)