Ghrelin acts as an interface between physiological state and phasic dopamine signaling

Journal of Neuroscience

Volumn 34, Issue 14, 2014, Pages 4905-4913

  Cone, Jackson J ^a   McCutcheon, James E ^a   Roitman, Mitchell F ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Feeding; Mesolimbic; Nucleus accumbens; Obesity; Reward; Voltammetry

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; ANGIOTENSIN II; DOPAMINE; GHRELIN; OREXIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC RESTRICTION; CANNULA; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DIET RESTRICTION; ELECTROCHEMISTRY; FOOD INTAKE; IMMUNOHISTOCHEMISTRY; LATERAL HYPOTHALAMUS; MALE; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SURGICAL TECHNIQUE;

FEEDING; MESOLIMBIC; NUCLEUS ACCUMBENS; OBESITY; REWARD; VOLTAMMETRY;

ACTION POTENTIALS; ANIMALS; BENZOXAZOLES; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FASTING; FEEDING BEHAVIOR; GHRELIN; HYPOTHALAMIC AREA, LATERAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NEURAL PATHWAYS; NEUROPEPTIDES; NUCLEUS ACCUMBENS; OLIGOPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; UREA; VENTRAL TEGMENTAL AREA; WAKEFULNESS;

EID: 84899439447     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4404-13.2014     Document Type: Article

References (67)

1. Abizaid A, Liu ZW, Andrews ZB, Shanabrough M, Borok E, Elsworth JD, Roth RH, Sleeman MW, Picciotto MR, Tschöp MH, Gao XB, Horvath TL (2006) Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J Clin Invest 116: 3229-3239.CrossRef Medline
2. Ahn S, Phillips AG (1999) Dopaminergic correlates of sensory-specific satiety in the medial prefrontal cortex and nucleus accumbens of the rat. J Neurosci 19:RC29. Medline
3. Alhadeff AL, Rupprecht LE, Hayes MR (2012) GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 153:647-658.CrossRef Medline
4. Baldo BA, Sadeghian K, Basso AM, Kelley AE (2002) Effects of selective dopamine D1 or D2 receptor blockade within nucleus accumbens subregions on ingestive behavior and associated motor activity. Behav Brain Res 137:165-177.CrossRef Medline
5. Banks WA, Tschöp M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport a Cross the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302:822-827.CrossRef Medline
6. Bassareo V, Di Chiara G (1999) Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89:637-641.CrossRef Medline
7. Beeler JA, Daw N, Frazier CR, Zhuang X (2010) Tonic dopamine modulates exploitation of reward learning. Front Behav Neurosci 4:170.CrossRef Medline
8. Beeler JA, McCutcheon JE, Cao ZF, Murakami M, Alexander E, Roitman MF, Zhuang X (2012) Taste uncoupled from nutrition fails to sustain the reinforcing properties of food. Eur J Neurosci 36:2533-2546.CrossRef Medline
9. Berthoud HR, Münzberg H (2011) The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol Behav 104:29-39.CrossRef Medline
10. Borgland SL, Taha SA, Sarti F, Fields HL, Bonci A (2006) Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49:589-601.CrossRef Medline
11. Branch SY, Goertz RB, Sharpe AL, Pierce J, Roy S, Ko D, Paladini CA, Beckstead MJ (2013) Food restriction increases glutamate receptormediated burst firing of dopamine neurons. J Neurosci 33:13861-13872.CrossRef Medline
12. Brown HD, McCutcheon JE, Cone JJ, Ragozzino ME, Roitman MF (2011) Primary food reward and reward-predictive stimuli evoke different patterns of phasic dopamine signaling throughout the striatum. Eur J Neurosci 34:1997-2006.CrossRef Medline
13. Cabral A, Fernandez G, Perello M (2013) Analysis of brain nuclei accessible to ghrelin present in the cerebrospinal fluid. Neuroscience 253:406-415.CrossRef Medline
14. Cone JJ, Chartoff EH, Potter DN, Ebner SR, Roitman MF (2013) Prolonged high fat diet reduces dopamine reuptake without altering DAT gene expression. PLoS One 8:e58251.CrossRef Medline
15. Cummings DE, Frayo RS, Marmonier C, Aubert R, Chapelot D (2004) Plasma ghrelin levels and hunger scores in humans initiating meals voluntarily without time- and food-related cues. Am J Physiol Endocrinol Metab 287:E297-304.CrossRef Medline
16. Day JJ, Roitman MF, Wightman RM, Carelli RM (2007) Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat Neurosci 10:1020-1028.CrossRef Medline
17. Day JJ, Jones JL, Wightman RM, Carelli RM (2010) Phasic nucleus accumbens dopamine release encodes effort- and delay-related costs. Biol Psychiatry 68:306-309.CrossRef Medline
18. Di Ciano P, Cardinal RN, Cowell RA, Little SJ, Everitt BJ (2001) Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of pavlovian approach behavior. J Neurosci 21:9471-9477. Medline
19. Drewnowski A, Specter SE (2004) Poverty and obesity: the role of energy density and energy costs. Am J Clin Nutr 79:6-16. Medline
20. España RA, Oleson EB, Locke JL, Brookshire BR, Roberts DC, Jones SR (2010) The hypocretin-orexin system regulates cocaine selfadministration via actions on the mesolimbic dopamine system. Eur J Neurosci 31:336-348.CrossRef Medline
21. España RA, Melchior JR, Roberts DC, Jones SR (2011) Hypocretin 1/orexin A in the ventral tegmental area enhances dopamine responses to cocaine and promotes cocaine self-administration. Psychopharmacology 214: 415-426.CrossRef Medline
22. Fadel J, Deutch AY (2002) Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111:379-387.CrossRef Medline
23. Gan JO, Walton ME, Phillips PE (2010) Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine. Nat Neurosci 13:25-27.CrossRef Medline
24. Gore BB, Zweifel LS (2013) Genetic reconstruction of dopamine d1 receptor signaling in the nucleus accumbens facilitates natural and drug reward responses. J Neurosci 33:8640-8649.CrossRef Medline
25. Heien ML, Johnson MA, Wightman RM (2004) Resolving neurotransmitters detected by fast-scan cyclic voltammetry. Anal Chem 76:5697-5704.CrossRef Medline
26. Hernandez L, Hoebel BG (1988) Feeding and hypothalamic stimulation increase dopamine turnover in the accumbens. Physiol Behav 44:599-606.CrossRef Medline
27. Hommel JD, Trinko R, Sears RM, Georgescu D, Liu ZW, Gao XB, Thurmon JJ, Marinelli M, DiLeone RJ (2006) Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 51:801-810.CrossRef Medline
28. Ikemoto S (2010) Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neurosci Biobehav Rev 35:129-150.CrossRef Medline
29. Jerlhag E (2008) Systemic administration of ghrelin induces conditioned place preference and stimulates accumbal dopamine. Addict Biol 13:358-363.CrossRef Medline
30. Jerlhag E, Egecioglu E, Dickson SL, Andersson M, Svensson L, Engel JA (2006a) Ghrelin stimulates locomotor activity and accumbal dopamine-overflow via central cholinergic systems in mice: implications for its involvement in brain reward. Addict Biol 11:45-54.CrossRef Medline
31. Jerlhag E, Egecioglu E, Dickson SL, Douhan A, Svensson L, Engel JA (2007) Ghrelin administration into tegmental areas stimulates locomotor activity and increases extracellular concentration of dopamine in the nucleus accumbens. Addict Biol 12:6-16.CrossRef Medline
32. Kanoski SE, Fortin SM, Ricks KM, Grill HJ (2013) Ghrelin signaling in the ventral hippocampus stimulates learned and motivational aspects of feeding via PI3K-Akt signaling. Biol Psychiatry 73:915-923.CrossRef Medline
33. Koch M, Schmid A, Schnitzler HU (2000) Role of nucleus accumbens dopamine D 1 and D 2 receptors in instrumental and Pavlovian paradigms of conditioned reward. Psychopharmacology 152:67-73.CrossRef Medline
34. Koob GF, Riley SJ, Smith SC, Robbins TW (1978) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. J Comp Physiol Psychol 92:917-927.CrossRef Medline
35. Korotkova TM, Sergeeva OA, Eriksson KS, Haas HL, Brown RE (2003) Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci 23:7-11.
36. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773.CrossRef Medline
37. Mahler SV, Aston-Jones GS (2012) Fos activation of selective afferents to ventral tegmental area during cue-induced reinstatement of cocaine seeking in rats. J Neurosci 32:13309-13326.CrossRef Medline
38. Malik S, McGlone F, Bedrossian D, Dagher A (2008) Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 7:400-409.CrossRef Medline
39. Margules DL, Olds J (1962) Identical "feeding" and "rewarding" systems in the lateral hypothalamus of rats. Science 135:374-375.CrossRef Medline
40. McCutcheon JE, Conrad KL, Carr SB, Ford KA, McGehee DS, Marinelli M (2012) Dopamine neurons in the ventral tegmental area fire faster in adolescent rats than in adults. J Neurophysiol 108:1620-1630.CrossRef Medline
41. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194-198.CrossRef Medline
42. Olszewski PK, Li D, Grace MK, Billington CJ, Kotz CM, Levine AS (2003) Neural basis of orexigenic effects of ghrelin acting within lateral hypothalamus. Peptides 24:597-602.CrossRef Medline
43. Owesson-White CA, Roitman MF, Sombers LA, Belle AM, Keithley RB, Peele JL, Carelli RM, Wightman RM (2012) Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens. J Neurochem 121:252-262.CrossRef Medline
44. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edition. London: Elsevier Academic.
45. Perello M, Sakata I, Birnbaum S, Chuang JC, Osborne-Lawrence S, Rovinsky SA, Woloszyn J, Yanagisawa M, Lutter M, Zigman JM (2010) Ghrelin increases the rewarding value of high-fat diet in an orexin-dependent manner. Biol Psychiatry 67:880-886.CrossRef Medline
46. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015. Medline
47. Phillips PE, Robinson DL, Stuber GD, Carelli RM, Wightman RM (2003) Real-time measurements of phasic changes in extracellular dopamine concentration in freely moving rats by fast-scan cyclic voltammetry. Methods Mol Med 79:443-464. Medline
48. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24:1265-1271.CrossRef Medline
49. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76:470-485.CrossRef Medline
50. Salamone JD, Steinpreis RE, McCullough LD, Smith P, Grebel D, Mahan K (1991) Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology 104:515-521.CrossRef Medline
51. Sinkala E, McCutcheon JE, Schuck MJ, Schmidt E, Roitman MF, Eddington DT (2012) Electrode calibration with a microfluidic flow cell for fastscan cyclic voltammetry. Lab Chip 12:2403-2408.CrossRef Medline
52. Skibicka KP, Shirazi RH, Rabasa-Papio C, Alvarez-Crespo M, Neuber C, Vogel H, Dickson SL (2013) Divergent circuitry underlying food reward and intake effects of ghrelin: dopaminergic VTA-accumbens projection mediates ghrelin's effect on food reward but not food intake. Neuropharmacology 73:274-283.CrossRef Medline
53. Smith-Roe SL, Kelley AE (2000) Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20:7737-7742. Medline
54. Sombers LA, Beyene M, Carelli RM, Wightman RM (2009) Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci 29:1735-1742.CrossRef Medline
55. Steinberg EE, Keiflin R, Boivin JR, Witten IB, Deisseroth K, Janak PH (2013) A causal link between prediction errors, dopamine neurons and learning. Nat Neurosci 16:966-973.CrossRef Medline
56. Stuber GD, Klanker M, de Ridder B, Bowers MS, Joosten RN, Feenstra MG, Bonci A (2008) Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 321:1690-1692.CrossRef Medline
57. Sugam JA, Day JJ, Wightman RM, Carelli RM (2012) Phasic nucleus accumbens dopamine encodes risk-based decision-making behavior. Biol Psychiatry 71:199-205.CrossRef Medline
58. Taber MT, Fibiger HC (1997) Feeding-evoked dopamine release in the nucleus, accumbens: regulation by glutamatergic mechanisms. Neuroscience 76:1105-1112.CrossRef Medline
59. Toshinai K, Date Y, Murakami N, Shimada M, Mondal MS, Shimbara T, Guan JL, Wang QP, Funahashi H, Sakurai T, Shioda S, Matsukura S, Kangawa K, Nakazato M (2003) Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology 144:1506-1512.CrossRef Medline
60. Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L, Deisseroth K (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:1080-1084.CrossRef Medline
61. Tschöp M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908-913.CrossRef Medline
62. Wanat MJ, Kuhnen CM, Phillips PE (2010) Delays conferred by escalating costs modulate dopamine release to rewards but not their predictors. J Neurosci 30:12020-12027.CrossRef Medline
63. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N (2012) Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858-873.CrossRef Medline
64. Wilson C, Nomikos GG, Collu M, Fibiger HC (1995) Dopaminergic correlates of motivated behavior: importance of drive. J Neurosci 15:5169-5178. Medline
65. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA, Brodsky M, Yizhar O, Cho SL, Gong S, Ramakrishnan C, Stuber GD, Tye KM, Janak PH, Deisseroth K (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:721-733.CrossRef Medline
66. Zigman JM, Jones JE, Lee CE, Saper CB, Elmquist JK (2006) Expression of ghrelin receptor mRNA in the rat and the mouse brain. J Comp Neurol 494:528-548.CrossRef Medline
67. Zweifel LS, Parker JG, Lobb CJ, Rainwater A, Wall VZ, Fadok JP, Darvas M, Kim MJ, Mizumori SJ, Paladini CA, Phillips PE, Palmiter RD (2009) Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc Natl Acad Sci U S A 106:7281-7288.CrossRef Medline.