An orexin hotspot in ventral pallidum amplifies hedonic 'liking' for sweetness

Neuropsychopharmacology

Volumn 38, Issue 9, 2013, Pages 1655-1664

  Ho, Chao Yi ^a   Berridge, Kent C ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

addiction; eating disorders; lateral hypothalamus; pleasure; reward; ventral pallidum

Indexed keywords

OREXIN; OREXIN A; SUCROSE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GLOBUS PALLIDUS; LATERAL HYPOTHALAMUS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; SWEETNESS; VENTRAL PALLIDUM;

AMYGDALA; ANIMALS; BRAIN MAPPING; GLOBUS PALLIDUS; HYPOTHALAMIC AREA, LATERAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICROINJECTIONS; NEURONS; NEUROPEPTIDES; QUININE; RATS; SUCROSE; TASTE PERCEPTION;

EID: 84880327583     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2013.62     Document Type: Article

References (58)

1. Aristotle (350BC) (2009). The Nicomachean ethics. Oxford University Press: Oxford, UK.
2. Aston-Jones G, Harris GC (2004). Brain substrates for increased drug seeking during protracted withdrawal. Neuropharmacology 47: 167-179. (Pubitemid 39298262)
3. Aston-Jones G, Smith RJ, Sartor GC, Moorman DE, Massi L, Tahsili-Fahadan P et al (2010). Lateral hypothalamic orexin/hypocretin neurons: a role in reward-seeking and addiction. Brain Res 1314: 74-90.
4. Baldo BA, Daniel RA, Berridge CW, Kelley AE (2003). Overlapping distributions of orexin/hypocretin-and dopamine-betahydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 464: 220-237. (Pubitemid 36976049)
5. Beaver J, Lawrence A, van Ditzhuijzen J, Davis M, Woods A, Calder A (2006). Individual differences in reward drive predict neural responses to images of food. J Neurosci 26: 5160-5166. (Pubitemid 44315297)
6. Berridge KC (2000). Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev 24: 173-198. (Pubitemid 30100443)
7. Berthoud H-R, Lenard NR, Shin AC (2011). Food reward, hyperphagia, and obesity. Am J Physiol 300: R1266-R1277.
8. Berthoud HR, Morrison C (2008). The brain, appetite, and obesity. Annu Rev Psychol 59: 55-92.
9. Borgland SL, Chang S-J, Bowers MS, Thompson JL, Vittoz N, Floresco SB et al (2009). Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci 29: 11215-11225.
10. Cabanac M (1971). Physiological role of pleasure. Science 173: 1103-1107.
11. Choi DL, Davis JF, Fitzgerald ME, Benoit SC (2010). The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience 167: 11-20.
12. España R, Calipari ES (2012). Hypocretin/orexin regulation of dopamine signaling: implications for reward and reinforcement mechanisms. Front Behav Neurosci 6: 54.
13. Gao Q, Horvath TL (2007). Neurobiology of feeding and energy expenditure. Annu Rev Neurosci 30: 367-398. (Pubitemid 47218761)
14. Gao Q, Horvath TL (2008). Neuronal control of energy homeostasis. FEBS Lett 582: 132-141. (Pubitemid 50014150)
15. Grill HJ, Norgren R (1978). The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143: 263-279. (Pubitemid 8277909)
16. Groenewegen HJ, Berendse HW, Haber SN (1993). Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 57: 113-142. (Pubitemid 23325638)
17. Groenewegen HJ, Wright CI, Beijer AV, Voorn P (1999). Convergence and segregation of ventral striatal inputs and outputs. Ann N Y Acad Sci 877: 49-63. (Pubitemid 29351850)
18. Haber SN, Knutson B (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35: 4-26.
19. Haber SN, Lynd-Balta E, Mitchell SJ (1993). The organization of the descending ventral pallidal projections in the monkey. J Comparative Neurol 329: 111-128. (Pubitemid 23078224)
20. Harris GC, Aston-Jones G (2006). Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29: 571-577. (Pubitemid 44416459)
21. Harris GC, Wimmer M, Aston-Jones G (2005). A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437: 556-559. (Pubitemid 41613553)
22. Heimer L, Van Hoesen GW, Trimble M, Zahm DS (2008). Anatomy of Neuropsychiatry: The New Anatomy of the Basal Forebrain and its Implications for Neuropsychiatric Illness. Elsevier: Academic Press: Amsterdam.
23. Ho C-Y (2010). The Ventral Pallidum as a Limbic Pleasure Generator. PhD Dissertation at The University of Michigan, Ann Arbor, MI, USA.
24. Jupp B, Krivdic B, Krstew E, Lawrence AJ (2011). The orexin(1) receptor antagonist SB-334867 dissociates the motivational properties of alcohol and sucrose in rats. Brain Res 1391: 54-59.
25. Kalivas PW, Nakamura M (1999). Neural systems for behavioral activation and reward. Cur Opin Neurobiol 9: 223-227. (Pubitemid 29201796)
26. Kelley AE, Baldo BA, Pratt WE (2005). A proposed hypothalamicthalamic- striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol 493: 72-85. (Pubitemid 41636189)
27. Kim AK, Brown RM, Lawrence AJ (2012). The role of orexins/hypocretins in alcohol use and abuse: an appetitive-reward relationship. Front Behav Neurosci 6: 78.
28. Kringelbach ML (2005). The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 6: 691-702. (Pubitemid 43160318)
29. Kupchik YM, Kalivas PW (2012). The rostral subcommissural ventral pallidum is a mix of ventral pallidal neurons and neurons from adjacent areas: an electrophysiological study. Brain Structure Function (doi:10.1007/s00429-012- 0471-9).
30. 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. (Pubitemid 47587687)
31. Mahler SV, Smith RJ, Moorman DE, Sartor GC, Aston-Jones G (2012). Multiple roles for orexin/hypocretin in addiction. Prog Brain Res 198: 79-121.
32. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M et al (2001). Differential expression of orexin receptors 1 and 2 in the rat brain. J Comparative Neurol 435: 6-25. (Pubitemid 32448719)
33. Napier TC, Mickiewicz AL (2010). The role of the ventral pallidum in psychiatric disorders. Neuropsychopharmacology 35: 337-337.
34. Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates 4th edn. Academic Press: New York.
35. Peciña S, Berridge KC (2005). Hedonic hot spot in nucleus accumbens shell: Where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25: 11777-11786. (Pubitemid 43098470)
36. Richard JM, Berridge KC (2011). Nucleus accumbens dopamine/glutamate interaction switches modes to generate desire versus dread: d1 alone for appetitive eating but D1 and D2 together for fear. J Neurosci 31: 12866-12879.
37. Robinson MJF, Berridge KC. in press (2013). Instant transformation of learned repulsion into motivational 'wanting'. Curr Biol 23: 282-289.
38. Shimura T, Imaoka H, Yamamoto T (2006). Neurochemical modulation of ingestive behavior in the ventral pallidum. Eur J Neurosci 23: 1596-1604.
39. Smith KS, Berridge KC (2005). The ventral pallidum and hedonic reward: neurochemical maps of sucrose 'liking' and food intake. J Neurosci 25: 8637-8649. (Pubitemid 41362040)
40. Smith KS, Berridge KC (2007). Opioid limbic circuit for reward: interaction between hedonic hotspots of nucleus accumbens and ventral pallidum. J Neurosci 27: 1594-1605. (Pubitemid 46280077)
41. Smith KS, Berridge KC, Aldridge JW (2011). Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc Natl Acad Sci USA 108: E255-E264.
42. Smith KS, Mahler SV, Pecina S, Berridge KC (2010a). Hedonic Hotspots: Generating Sensory Pleasure in the Brain. In: Kringelbach MLBerridge KC eds. Pleasures of the Brain. Oxford University Press: Oxford, UK, pp 27-49.
43. Smith KS, Tindell AJ, Aldridge JW, Berridge KC (2009). Ventral pallidum roles in reward and motivation. Behav Brain Res 196: 155-167.
44. Smith RJ, Tahsili-Fahadan P, Aston-Jones G (2010b). Orexin/hypocretin is necessary for context-driven cocaine-seeking. Neuropharmacology 58: 179-184.
45. Steiner JE (1973). The gustofacial response: observation on normal and anencephalic newborn infants. Symposium on Oral Sensation and Perception 4: 254-278.
46. Steiner JE, Glaser D, Hawilo ME, Berridge KC (2001). Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. Neurosci Biobehav Rev 25: 53-74. (Pubitemid 32098341)
47. Stoeckel LE, Weller RE, Cook EW 3rd, Twieg DB, Knowlton RC, Cox JE (2008). Widespread reward-system activation in obese women in response to pictures of high-calorie foods. Neuroimage 41: 636-647.
48. Stratford TR, Wirtshafter D (2012). Lateral hypothalamic involvement in feeding elicited from the ventral pallidum. Eur J Neurosci 37: 648-653.
49. Thompson JL, Borgland SL (2011). A role for hypocretin/orexin in motivation. Behav Brain Res 217: 446-453.
50. Thompson RH, Swanson LW (2010). Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci USA 107: 15235-15239.
51. Thorpe AJ, Kotz CM (2005). Orexin A in the nucleus accumbens stimulates feeding and locomotor activity. Brain Res 1050: 156-162. (Pubitemid 40922729)
52. Tindell AJ, Smith KS, Berridge KC, Aldridge JW (2009). Dynamic computation of incentive salience: 'wanting' what was never 'liked'. J Neurosci 29: 12220-12228.
53. Tindell AJ, Smith KS, Pecina S, Berridge KC, Aldridge JW (2006). Ventral pallidum firing codes hedonic reward: when a bad taste turns good. J Neurophysiol 96: 2399-2409. (Pubitemid 44785893)
54. Valenstein ES, Cox VC, Kakolewski JW (1970). Reexamination of the role of the hypothalamus in motivation. Psychol Rev 77: 16-31.
55. Wassum KM, Ostlund SB, Maidment NT, Balleine BW (2009). Distinct opioid circuits determine the palatability and the desirability of rewarding events. Proc Natl Acad Sci 106: 12512-12517.
56. Zahm DS, Parsley KP, Schwartz ZM, Cheng AY (2013). On lateral septum-like characteristics of outputs from the accumbal hedonic 'hotspot' of Peciña and Berridge with commentary on the transitional nature of basal forebrain 'boundaries'. J Comp Neurol 521: 50-68.
57. Zahm DS, Williams E, Wohltmann C (1996). Ventral striatopallidothalamic projection: IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. J Comp Neurol 364: 340-362. (Pubitemid 26035157)
58. Zheng H, Patterson L, Berthoud H (2007). Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 27: 11075-11082. (Pubitemid 47574162)