High on food: the interaction between the neural circuits for feeding and for reward

Jing-Jing Liu, Diptendu Mukherjee, Doron Haritan, Bogna Ignatowska-Jankowska, Ji Liu, Ami Citri, Zhiping P. Pang

PDF(1901 KB)
PDF(1901 KB)
Front. Biol. ›› 2015, Vol. 10 ›› Issue (2) : 165-176. DOI: 10.1007/s11515-015-1348-0
REVIEW
REVIEW

High on food: the interaction between the neural circuits for feeding and for reward

Author information +
History +

Abstract

Hunger, mostly initiated by a deficiency in energy, induces food seeking and intake. However, the drive toward food is not only regulated by physiological needs, but is motivated by the pleasure derived from ingestion of food, in particular palatable foods. Therefore, feeding is viewed as an adaptive motivated behavior that involves integrated communication between homeostatic feeding circuits and reward circuits. The initiation and termination of a feeding episode are instructed by a variety of neuronal signals, and maladaptive plasticity in almost any component of the network may lead to the development of pathological eating disorders. In this review we will summarize the latest understanding of how the feeding circuits and reward circuits in the brain interact. We will emphasize communication between the hypothalamus and the mesolimbic dopamine system and highlight complexities, discrepancies, open questions and future directions for the field.

Keywords

feeding / neural circuitry, hedonic, reward, mesolimbic system, dopamine, hypothalamus

Cite this article

Download citation ▾
Jing-Jing Liu, Diptendu Mukherjee, Doron Haritan, Bogna Ignatowska-Jankowska, Ji Liu, Ami Citri, Zhiping P. Pang. High on food: the interaction between the neural circuits for feeding and for reward. Front. Biol., 2015, 10(2): 165‒176 https://doi.org/10.1007/s11515-015-1348-0

References

[1]
Anand B K, Brobeck J R (1951). Localization of a “feeding center” in the hypothalamus of the rat. Proc Soc Exp Biol Med, 77(2): 323–324
CrossRef Pubmed Google scholar
[2]
Atasoy D, Aponte Y, Su H H, Sternson S M (2008) A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci, 28: 7025–7030
[3]
Atasoy D, Betley J N, Su H H, Sternson S M (2012). Deconstruction of a neural circuit for hunger. Nature, 488(7410): 172–177
CrossRef Pubmed Google scholar
[4]
Atrens D M, Williams M P, Brady C J, Hunt G E (1982). Energy balance and hypothalamic self-stimulation. Behav Brain Res, 5(2): 131–142
CrossRef Pubmed Google scholar
[5]
Avena N M, Rada P, Hoebel B G (2008). Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev, 32(1): 20–39
CrossRef Pubmed Google scholar
[6]
Baicy K, London E D, Monterosso J, Wong M L, Delibasi T, Sharma A, Licinio J (2007). Leptin replacement alters brain response to food cues in genetically leptin-deficient adults. Proc Natl Acad Sci USA, 104(46): 18276–18279
CrossRef Pubmed Google scholar
[7]
Belgardt B F, Okamura T, Brüning J C (2009). Hormone and glucose signalling in POMC and AgRP neurons. J Physiol, 587(Pt 22): 5305–5314
CrossRef Pubmed Google scholar
[8]
Berridge K C (2009). ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders. Physiol Behav, 97(5): 537–550
CrossRef Pubmed Google scholar
[9]
Betley J N, Cao Z F, Ritola K D, Sternson S M (2013). Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell, 155(6): 1337–1350
CrossRef Pubmed Google scholar
[10]
Bittencourt J C, Presse F, Arias C, Peto C, Vaughan J, Nahon J L, Vale W, Sawchenko P E (1992). The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol, 319(2): 218–245
CrossRef Pubmed Google scholar
[11]
Blouet C, Schwartz G J (2010). Hypothalamic nutrient sensing in the control of energy homeostasis. Behav Brain Res, 209(1): 1–12
CrossRef Pubmed Google scholar
[12]
Borgland S L, Ungless M A, Bonci A (2010). Convergent actions of orexin/hypocretin and CRF on dopamine neurons: Emerging players in addiction. Brain Res, 1314: 139–144
CrossRef Pubmed Google scholar
[13]
Boules M, Cusack B, Zhao L, Fauq A, McCormick D J, Richelson E (2000). A novel neurotensin peptide analog given extracranially decreases food intake and weight in rodents. Brain Res, 865(1): 35–44
CrossRef Pubmed Google scholar
[14]
Cardinal R N, Parkinson J A, Hall J, Everitt B J (2002). Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev, 26(3): 321–352
CrossRef Pubmed Google scholar
[15]
Carroll M E, France C P, Meisch R A (1979). Food deprivation increases oral and intravenous drug intake in rats. Science, 205(4403): 319–321
CrossRef Pubmed Google scholar
[16]
Chung S, Hopf F W, Nagasaki H, Li C Y, Belluzzi J D, Bonci A, Civelli O (2009). The melanin-concentrating hormone system modulates cocaine reward. Proc Natl Acad Sci USA, 106(16): 6772–6777
CrossRef Pubmed Google scholar
[17]
Ciriello J, McMurray J C, Babic T, de Oliveira C V (2003). Collateral axonal projections from hypothalamic hypocretin neurons to cardiovascular sites in nucleus ambiguus and nucleus tractus solitarius. Brain Res, 991(1–2): 133–141
CrossRef Pubmed Google scholar
[18]
Citri A, Malenka R C (2008). Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology, 33(1): 18–41
CrossRef Pubmed Google scholar
[19]
Coll A P, Farooqi I S, O’Rahilly S (2007). The hormonal control of food intake. Cell, 129(2): 251–262
CrossRef Pubmed Google scholar
[20]
Coons E E, Cruce J A (1968). Lateral hypothalamus: food current intensity in maintaining self-stimulation of hunger. Science, 159(3819): 1117–1119
CrossRef Pubmed Google scholar
[21]
Cota D, Barrera J G, Seeley R J (2006). Leptin in energy balance and reward: two faces of the same coin? Neuron, 51(6): 678–680
CrossRef Pubmed Google scholar
[22]
Davis C, Strachan S, Berkson M (2004). Sensitivity to reward: implications for overeating and overweight. Appetite, 42(2): 131–138
CrossRef Pubmed Google scholar
[23]
Dietrich M O, Horvath T L (2009). Feeding signals and brain circuitry. Eur J Neurosci, 30(9): 1688–1696
CrossRef Pubmed Google scholar
[24]
Domingos A I, Vaynshteyn J, Voss H U, Ren X, Gradinaru V, Zang F, Deisseroth K, de Araujo I E, Friedman J (2011). Leptin regulates the reward value of nutrient. Nat Neurosci, 14(12): 1562–1568
CrossRef Pubmed Google scholar
[25]
Dossat A M, Diaz R, Gallo L, Panagos A, Kay K, Williams D L (2013). Nucleus accumbens GLP-1 receptors influence meal size and palatability. Am J Physiol Endocrinol Metab, 304(12): E1314–E1320
CrossRef Pubmed Google scholar
[26]
Dossat A M, Lilly N, Kay K, Williams D L (2011). Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci, 31(41): 14453–14457
CrossRef Pubmed Google scholar
[27]
Dube M G, Kalra S P, Kalra P S (1999). Food intake elicited by central administration of orexins/hypocretins: identification of hypothalamic sites of action. Brain Res, 842(2): 473–477
CrossRef Pubmed Google scholar
[28]
Everson S A, Maty S C, Lynch J W, Kaplan G A (2002). Epidemiologic evidence for the relation between socioeconomic status and depression, obesity, and diabetes. J Psychosom Res, 53(4): 891–895
CrossRef Pubmed Google scholar
[29]
Fadel J, Deutch A Y (2002). Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience, 111(2): 379–387
CrossRef Pubmed Google scholar
[30]
Farooqi I S, Bullmore E, Keogh J, Gillard J, O’Rahilly S, Fletcher P C (2007). Leptin regulates striatal regions and human eating behavior. Science, 317(5843): 1355
CrossRef Pubmed Google scholar
[31]
Feifel D, Goldenberg J, Melendez G, Shilling P D (2010). The acute and subchronic effects of a brain-penetrating, neurotensin-1 receptor agonist on feeding, body weight and temperature. Neuropharmacology, 58(1): 195–198
CrossRef Pubmed Google scholar
[32]
Figlewicz D P (2003). Insulin, food intake, and reward. Semin Clin Neuropsychiatry, 8(2): 82–93
CrossRef Pubmed Google scholar
[33]
Frank R A, Preshaw R L, Stutz R M, Valenstein E S (1982). Lateral hypothalamic stimulation: stimulus-bound eating and self-deprivation. Physiol Behav, 29(1): 17–21
CrossRef Pubmed Google scholar
[34]
Fulton S, Pissios P, Manchon R P, Stiles L, Frank L, Pothos E N, Maratos-Flier E, Flier J S (2006). Leptin regulation of the mesoaccumbens dopamine pathway. Neuron, 51(6): 811–822
CrossRef Pubmed Google scholar
[35]
Fulton S, Woodside B, Shizgal P (2000). Modulation of brain reward circuitry by leptin. Science, 287(5450): 125–128
CrossRef Pubmed Google scholar
[36]
Geiger B M, Haburcak M, Avena N M, Moyer M C, Hoebel B G, Pothos E N (2009). Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience, 159(4): 1193–1199
CrossRef Pubmed Google scholar
[37]
Georgescu D, Sears R M, Hommel J D, Barrot M, Bolanos C A, Marsh D J, Bednarek M A, Bibb J A, Maratos-Flier E, Nestler E J, DiLeone R J (2005). The hypothalamic neuropeptide melanin-concentrating hormone acts in the nucleus accumbens to modulate feeding behavior and forced-swim performance. J Neurosci, 25: 2933–2940
[38]
Goforth P B, Leinninger G M, Patterson C M, Satin L S, Myers M G Jr. (2014) Leptin acts via lateral hypothalamic area neurotensin neurons to inhibit orexin neurons by multiple GABA-independent mechanisms. J Neurosci, 34: 11405–11415
[39]
Goldstone A P (2006). The hypothalamus, hormones, and hunger: alterations in human obesity and illness. Prog Brain Res, 153: 57–73
CrossRef Pubmed Google scholar
[40]
Gutierrez R, Lobo M K, Zhang F, de Lecea L (2011). Neural integration of reward, arousal, and feeding: recruitment of VTA, lateral hypothalamus, and ventral striatal neurons. IUBMB Life, 63(10): 824–830
CrossRef Pubmed Google scholar
[41]
Hahn J D, Swanson L W (2010). Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res Brain Res Rev, 64(1): 14–103
CrossRef Pubmed Google scholar
[42]
Hahn J D, Swanson L W (2012). Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat. J Comp Neurol, 520(9): 1831–1890
CrossRef Pubmed Google scholar
[43]
Håkansson M, de Lecea L, Sutcliffe J G, Yanagisawa M, Meister B (1999). Leptin receptor- and STAT3-immunoreactivities in hypocretin/orexin neurones of the lateral hypothalamus. J Neuroendocrinol, 11(8): 653–663
CrossRef Pubmed Google scholar
[44]
Haltia L T, Rinne J O, Merisaari H, Maguire R P, Savontaus E, Helin S, Någren K, Kaasinen V (2007). Effects of intravenous glucose on dopaminergic function in the human brain in vivo. Synapse, 61(9): 748–756
CrossRef Pubmed Google scholar
[45]
Hansen S, Stanfield E J, Everitt B J (1981). The effects of lesions of lateral tegmental noradrenergic neurons on components of sexual behavior and pseudopregnancy in female rats. Neuroscience, 6(6): 1105–1117
CrossRef Pubmed Google scholar
[46]
Harthoorn L F, Sañé A, Nethe M, Van Heerikhuize J J (2005). Multi-transcriptional profiling of melanin-concentrating hormone and orexin-containing neurons. Cell Mol Neurobiol, 25(8): 1209–1223
CrossRef Pubmed Google scholar
[47]
Hoebel B G, Teitelbaum P (1962). Hypothalamic control of feeding and self-stimulation. Science, 135(3501): 375–377
CrossRef Pubmed Google scholar
[48]
Hommel J D, Trinko R, Sears R M, Georgescu D, Liu Z W, Gao X B, Thurmon J J, Marinelli M, DiLeone R J (2006). Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron, 51(6): 801–810
CrossRef Pubmed Google scholar
[49]
Horjales-Araujo E, Hellysaz A, Broberger C (2014). Lateral hypothalamic thyrotropin-releasing hormone neurons: distribution and relationship to histochemically defined cell populations in the rat. Neuroscience, 277: 87–102
CrossRef Pubmed Google scholar
[50]
Horvath T L (2005). The hardship of obesity: a soft-wired hypothalamus. Nat Neurosci, 8(5): 561–565
CrossRef Pubmed Google scholar
[51]
Ishiwari K, Weber S M, Mingote S, Correa M, Salamone J D (2004). Accumbens dopamine and the regulation of effort in food-seeking behavior: modulation of work output by different ratio or force requirements. Behav Brain Res, 151(1–2): 83–91
CrossRef Pubmed Google scholar
[52]
Jennings J H, Rizzi G, Stamatakis A M, Ung R L, Stuber G D (2013). The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science, 341(6153): 1517–1521
CrossRef Pubmed Google scholar
[53]
Jerlhag E, Janson A C, Waters S, Engel J A (2012). Concomitant release of ventral tegmental acetylcholine and accumbal dopamine by ghrelin in rats. PLoS ONE, 7(11): e49557
CrossRef Pubmed Google scholar
[54]
Johnson P M, Kenny P J (2010). Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats (vol 13, pg 635, 2010). Nat Neurosci, 13: 1033–1033
CrossRef Google scholar
[55]
Karnani M M, Szabó G, Erdélyi F, Burdakov D (2013). Lateral hypothalamic GAD65 neurons are spontaneously firing and distinct from orexin- and melanin-concentrating hormone neurons. J Physiol, 591(Pt 4): 933–953
CrossRef Pubmed Google scholar
[56]
Kauer J A, Malenka R C (2007). Synaptic plasticity and addiction. Nat Rev Neurosci, 8(11): 844–858
CrossRef Pubmed Google scholar
[57]
Kelley A E (2004). Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev, 27(8): 765–776
CrossRef Pubmed Google scholar
[58]
Kelley A E, Baldo B A, Pratt W E (2005a). A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol, 493(1): 72–85
CrossRef Pubmed Google scholar
[59]
Kelley A E, Baldo B A, Pratt W E, Will M J (2005b). Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav, 86(5): 773–795
CrossRef Pubmed Google scholar
[60]
Kelley A E, Bless E P, Swanson C J (1996). Investigation of the effects of opiate antagonists infused into the nucleus accumbens on feeding and sucrose drinking in rats. J Pharmacol Exp Ther, 278(3): 1499–1507
Pubmed
[61]
Kempadoo K A, Tourino C, Cho S L, Magnani F, Leinninger G M, Stuber G D, Zhang F, Myers M G, Deisseroth K, de Lecea L, Bonci A (2013) Hypothalamic neurotensin projections promote reward by enhancing glutamate transmission in the VTA. J Neurosci, 33: 7618–7626
[62]
Kenny P J (2011a). Common cellular and molecular mechanisms in obesity and drug addiction. Nat Rev Neurosci, 12(11): 638–651
CrossRef Pubmed Google scholar
[63]
Kenny P J (2011b). Reward mechanisms in obesity: new insights and future directions. Neuron, 69(4): 664–679
CrossRef Pubmed Google scholar
[64]
Kokkotou E G, Tritos N A, Mastaitis J W, Slieker L, Maratos-Flier E (2001). Melanin-concentrating hormone receptor is a target of leptin action in the mouse brain. Endocrinology, 142(2): 680–686
CrossRef Pubmed Google scholar
[65]
Krilowicz B L, Szymusiak R, McGinty D (1994). Regulation of posterior lateral hypothalamic arousal related neuronal discharge by preoptic anterior hypothalamic warming. Brain Res, 668(1–2): 30–38
CrossRef Pubmed Google scholar
[66]
Lalonde R, Qian S (2007). Exploratory activity, motor coordination, and spatial learning in Mchr1 knockout mice. Behav Brain Res, 178(2): 293–304
CrossRef Pubmed Google scholar
[67]
Land B B, Narayanan N S, Liu R J, Gianessi C A, Brayton C E, Grimaldi D M, Sarhan M, Guarnieri D J, Deisseroth K, Aghajanian G K, DiLeone R J (2014). Medial prefrontal D1 dopamine neurons control food intake. Nat Neurosci, 17(2): 248–253
CrossRef Pubmed Google scholar
[68]
Leinninger G M, Jo Y H, Leshan R L, Louis G W, Yang H, Barrera J G, Wilson H, Opland D M, Faouzi M A, Gong Y, Jones J C, Rhodes C J, Chua S Jr, Diano S, Horvath T L, Seeley R J, Becker J B, Münzberg H, Myers M G Jr (2009). Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab, 10(2): 89–98
CrossRef Pubmed Google scholar
[69]
Leinninger G M, Opland D M, Jo Y H, Faouzi M, Christensen L, Cappellucci L A, Rhodes C J, Gnegy M E, Becker J B, Pothos E N, Seasholtz A F, Thompson R C, Myers M G Jr (2011). Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab, 14(3): 313–323
CrossRef Pubmed Google scholar
[70]
Lim B K, Huang K W, Grueter B A, Rothwell P E, Malenka R C (2012). Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature, 487(7406): 183–189
CrossRef Pubmed Google scholar
[71]
Lu X Y, Bagnol D, Burke S, Akil H, Watson S J (2000). Differential distribution and regulation of OX1 and OX2 orexin/hypocretin receptor messenger RNA in the brain upon fasting. Horm Behav, 37(4): 335–344
CrossRef Pubmed Google scholar
[72]
Ludwig D S, Tritos N A, Mastaitis J W, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier J S, Maratos-Flier E (2001). Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest, 107(3): 379–386
CrossRef Pubmed Google scholar
[73]
Lutter M, Nestler E J (2009). Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr, 139(3): 629–632
CrossRef Pubmed Google scholar
[74]
Marsh D J, Weingarth D T, Novi D E, Chen H Y, Trumbauer M E, Chen A S, Guan X M, Jiang M M, Feng Y, Camacho R E, Shen Z, Frazier E G, Yu H, Metzger J M, Kuca S J, Shearman L P, Gopal-Truter S, MacNeil D J, Strack A M, MacIntyre D E, Van der Ploeg L H, Qian S (2002). Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA, 99(5): 3240–3245
CrossRef Pubmed Google scholar
[75]
McCarty C A, Kosterman R, Mason W A, McCauley E, Hawkins J D, Herrenkohl T I, Lengua L J (2009). Longitudinal associations among depression, obesity and alcohol use disorders in young adulthood. Gen Hosp Psychiatry, 31(5): 442–450
CrossRef Pubmed Google scholar
[76]
Meister B (2007). Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav, 92(1–2): 263–271
CrossRef Pubmed Google scholar
[77]
Menatti A R, Weeks J W, Levinson C A, McGowan M M (2013). Exploring the relationship between social anxiety and bulimic symptoms: mediational effects of perfectionism among females. Cognit Ther Res, 37(5): 914–922
CrossRef Pubmed Google scholar
[78]
Miller N E (1960). Motivational effects of brain stimulation and drugs. Fed Proc, 19: 846–854
Pubmed
[79]
Millington G W (2007). The role of proopiomelanocortin (POMC) neurones in feeding behaviour. Nutr Metab (Lond), 4(1): 18
CrossRef Pubmed Google scholar
[80]
Morrison S D, Mayer J (1957). Adipsia and aphagia in rats after lateral subthalamic lesions. Am J Physiol, 191(2): 248–254
Pubmed
[81]
Morton G J, Cummings D E, Baskin D G, Barsh G S, Schwartz M W (2006). Central nervous system control of food intake and body weight. Nature, 443(7109): 289–295
CrossRef Pubmed Google scholar
[82]
Morton G J, Meek T H, Schwartz M W (2014). Neurobiology of food intake in health and disease. Nat Rev Neurosci, 15(6): 367–378
CrossRef Pubmed Google scholar
[83]
Morton T D, Salovitz B (2006). Evolving a theoretical model of child safety in maltreating families. Child Abuse Negl, 30(12): 1317–1327
CrossRef Pubmed Google scholar
[84]
Murray S, Tulloch A, Gold M S, Avena N M (2014). Hormonal and neural mechanisms of food reward, eating behaviour and obesity. Nat Rev Endocrinol, 10(9): 540–552
CrossRef Pubmed Google scholar
[85]
Musselman D L, Betan E, Larsen H, Phillips L S (2003). Relationship of depression to diabetes types 1 and 2: epidemiology, biology, and treatment. Biol Psychiatry, 54(3): 317–329
CrossRef Pubmed Google scholar
[86]
Nahon J L, Presse F, Bittencourt J C, Sawchenko P E, Vale W (1989). The rat melanin-concentrating hormone messenger ribonucleic acid encodes multiple putative neuropeptides coexpressed in the dorsolateral hypothalamus. Endocrinology, 125(4): 2056–2065
CrossRef Pubmed Google scholar
[87]
Narayanan N S, Guarnieri D J, DiLeone R J (2010). Metabolic hormones, dopamine circuits, and feeding. Front Neuroendocrinol, 31(1): 104–112
CrossRef Pubmed Google scholar
[88]
Olds J, Milner P (1954). Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol, 47(6): 419–427
CrossRef Pubmed Google scholar
[89]
Pascoli V, Terrier J, Espallergues J, Valjent E, O’Connor E C, Lüscher C (2014). Contrasting forms of cocaine-evoked plasticity control components of relapse. Nature, 509(7501): 459–464
CrossRef Pubmed Google scholar
[90]
Peciña S, Berridge K C (1995). Central enhancement of taste pleasure by intraventricular morphine. Neurobiology (Bp), 3(3-4): 269–280
Pubmed
[91]
Peciña S, Berridge K C (2000). Opioid site in nucleus accumbens shell mediates eating and hedonic ‘liking’ for food: map based on microinjection Fos plumes. Brain Res, 863(1–2): 71–86
CrossRef Pubmed Google scholar
[92]
Petrovich G D, Holland P C, Gallagher M (2005) Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J Neurosci, 25: 8295–8302
[93]
Pfaffly J, Michaelides M, Wang G J, Pessin J E, Volkow N D, Thanos P K (2010). Leptin increases striatal dopamine D2 receptor binding in leptin-deficient obese (ob/ob) mice. Synapse, 64(7): 503–510
CrossRef Pubmed Google scholar
[94]
Qu D, Ludwig D S, Gammeltoft S, Piper M, Pelleymounter M A, Cullen M J, Mathes W F, Przypek R, Kanarek R, Maratos-Flier E (1996). A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature, 380(6571): 243–247
CrossRef Pubmed Google scholar
[95]
Rada P, Avena N M, Hoebel B G (2005). Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience, 134(3): 737–744
CrossRef Pubmed Google scholar
[96]
Rosin D L, Weston M C, Sevigny C P, Stornetta R L, Guyenet P G (2003). Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J Comp Neurol, 465(4): 593–603
CrossRef Pubmed Google scholar
[97]
Routtenberg A, Lindy J (1965). Effects of the availability of rewarding septal and hypothalamic stimulation on bar pressing for food under conditions of deprivation. J Comp Physiol Psychol, 60(2): 158–161
CrossRef Pubmed Google scholar
[98]
Sahu A, Carraway R E, Wang Y P (2001). Evidence that neurotensin mediates the central effect of leptin on food intake in rat. Brain Res, 888(2): 343–347
CrossRef Pubmed Google scholar
[99]
Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli R M, Tanaka H, Williams S C, Richardson J A, Kozlowski G P, Wilson S, Arch J R, Buckingham R E, Haynes A C, Carr S A, Annan R S, McNulty D E, Liu W S, Terrett J A, Elshourbagy N A, Bergsma D J, Yanagisawa M (1998). Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell, 92(4): 573–585
CrossRef Pubmed Google scholar
[100]
Salamone J D, Cousins M S, Bucher S (1994). Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav Brain Res, 65(2): 221–229
CrossRef Pubmed Google scholar
[101]
Sano H, Yokoi M (2007) Striatal medium spiny neurons terminate in a distinct region in the lateral hypothalamic area and do not directly innervate orexin/hypocretin- or melanin-concentrating hormone-containing neurons. J Neurosci, 27: 6948–6955
[102]
Saper C B, Chou T C, Elmquist J K (2002). The need to feed: homeostatic and hedonic control of eating. Neuron, 36(2): 199–211
CrossRef Pubmed Google scholar
[103]
Saper C B, Lu J, Chou T C, Gooley J (2005). The hypothalamic integrator for circadian rhythms. Trends Neurosci, 28(3): 152–157
CrossRef Pubmed Google scholar
[104]
Sears R M, Liu R J, Narayanan N S, Sharf R, Yeckel M F, Laubach M, Aghajanian GK, DiLeone R J (2010) Regulation of nucleus accumbens activity by the hypothalamic neuropeptide melanin-concentrating hormone. J Neurosci, 30: 8263–8273
[105]
Shimada M, Tritos N A, Lowell B B, Flier J S, Maratos-Flier E (1998). Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature, 396(6712): 670–674
CrossRef Pubmed Google scholar
[106]
Skibicka K P, Shirazi R H, Rabasa-Papio C, Alvarez-Crespo M, Neuber C, Vogel H, Dickson S L (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 Pubmed Google scholar
[107]
Skofitsch G, Jacobowitz D M, Zamir N (1985). Immunohistochemical localization of a melanin concentrating hormone-like peptide in the rat brain. Brain Res Bull, 15(6): 635–649
CrossRef Pubmed Google scholar
[108]
Small D M, Jones-Gotman M, Dagher A (2003). Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage, 19(4): 1709–1715
CrossRef Pubmed Google scholar
[109]
Spies G (1965). Food versus intracranial self-stimulation reinforcement in food-deprived rats. J Comp Physiol Psychol, 60(2): 153–157
CrossRef Pubmed Google scholar
[110]
Stanley B G, Willett V L 3rd, Donias H W, Ha L H, Spears L C (1993). The lateral hypothalamus: a primary site mediating excitatory amino acid-elicited eating. Brain Res, 630(1–2): 41–49
CrossRef Pubmed Google scholar
[111]
Sterling P, Eyer J (1988) Allostasis: a New Paradigm to Explain Arousal Pathology. John Wiley & Sons
[112]
Sternson S M (2013). Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron, 77(5): 810–824
CrossRef Pubmed Google scholar
[113]
Stratford T R, Kelley A E (1999). Evidence of a functional relationship between the nucleus accumbens shell and lateral hypothalamus subserving the control of feeding behavior. J Neurosci, 19(24): 11040–11048
Pubmed
[114]
Stuber G D, Evans S B, Higgins M S, Pu Y, Figlewicz D P (2002). Food restriction modulates amphetamine-conditioned place preference and nucleus accumbens dopamine release in the rat. Synapse, 46(2): 83–90
CrossRef Pubmed Google scholar
[115]
Stuber G D, Sparta D R, Stamatakis A M, van Leeuwen W A, Hardjoprajitno J E, Cho S, Tye K M, Kempadoo K A, Zhang F, Deisseroth K, Bonci A (2011). Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature, 475(7356): 377–380
CrossRef Pubmed Google scholar
[116]
Teitelbaum P, Stellar E (1954). Recovery from the failure to eat produced by hypothalamic lesions. Science, 120(3126): 894–895
CrossRef Pubmed Google scholar
[117]
Thanos P K, Michaelides M, Piyis Y K, Wang G J, Volkow N D (2008). Food restriction markedly increases dopamine D2 receptor (D2R) in a rat model of obesity as assessed with in-vivo muPET imaging ([11C] raclopride) and in-vitro ([3H] spiperone) autoradiography. Synapse, 62(1): 50–61
CrossRef Pubmed Google scholar
[118]
Tomasi D, Wang G J, Wang R, Caparelli E C, Logan J, Volkow N D (2014). Overlapping patterns of brain activation to food and cocaine cues in cocaine abusers: Association to striatal D2/D3 receptors. Hum Brain Mapp
Pubmed
[119]
Trifilieff P, Martinez D (2014). Imaging addiction: D2 receptors and dopamine signaling in the striatum as biomarkers for impulsivity. Neuropharmacology, 76(Pt B): 498–509
CrossRef Pubmed Google scholar
[120]
Trojniar W, Plucińska K, Ignatowska-Jankowska B, Jankowski M (2007). Damage to the nucleus accumbens shell but not core impairs ventral tegmental area stimulation-induced feeding. J Physiol Pharmacol, 58(Suppl 3): 63–71
Pubmed
[121]
Volkow N D, Wang G J, Baler R D (2011). Reward, dopamine and the control of food intake: implications for obesity. Trends Cogn Sci, 15(1): 37–46
CrossRef Pubmed Google scholar
[122]
Volkow N D, Wang G J, Fowler J S, Telang F (2008). Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci, 363(1507): 3191–3200
CrossRef Pubmed Google scholar
[123]
Volkow N D, Wang G J, Tomasi D, Baler R D (2013). Obesity and addiction: neurobiological overlaps. Obes Rev, 14(1): 2–18
CrossRef Pubmed Google scholar
[124]
Volkow N D, Wise R A (2005). How can drug addiction help us understand obesity? Nat Neurosci, 8(5): 555–560
CrossRef Pubmed Google scholar
[125]
Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell B B (2011). Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron, 71(1): 142–154
CrossRef Pubmed Google scholar
[126]
Wang G J, Volkow N D, Logan J, Pappas N R, Wong C T, Zhu W, Netusil N, Fowler J S (2001). Brain dopamine and obesity. Lancet, 357(9253): 354–357
CrossRef Pubmed Google scholar
[127]
Wang L, Shen M, Yu Y, Tao Y, Zheng P, Wang F, Ma L (2014). Optogenetic activation of GABAergic neurons in the nucleus accumbens decreases the activity of the ventral pallidum and the expression of cocaine-context-associated memory. Int J Neuropsychopharmacol, 17(5): 753–763
CrossRef Pubmed Google scholar
[128]
Willie J T, Chemelli R M, Sinton C M, Yanagisawa M (2001). To eat or to sleep? Orexin in the regulation of feeding and wakefulness. Annu Rev Neurosci, 24(1): 429–458
CrossRef Pubmed Google scholar
[129]
Wise R A (1974). Lateral hypothalamic electrical stimulation: does it make animals ‘hungry’? Brain Res, 67(2): 187–209
CrossRef Pubmed Google scholar
[130]
Wise R A (2006). Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci, 361(1471): 1149–1158
CrossRef Pubmed Google scholar
[131]
Yamanaka A, Beuckmann C T, Willie J T, Hara J, Tsujino N, Mieda M, Tominaga M, Yagami K, Sugiyama F, Goto K, Yanagisawa M, Sakurai T (2003). Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron, 38(5): 701–713
CrossRef Pubmed Google scholar
[132]
Zahm D S, Brog J S (1992). On the significance of subterritories in the “accumbens” part of the rat ventral striatum. Neuroscience, 50(4): 751–767
CrossRef Pubmed Google scholar
[133]
Zheng H, Corkern M, Stoyanova I, Patterson L M, Tian R, Berthoud H R (2003). Peptides that regulate food intake: appetite-inducing accumbens manipulation activates hypothalamic orexin neurons and inhibits POMC neurons. Am J Physiol Regul Integr Comp Physiol, 284(6): R1436–R1444
Pubmed

Acknowledgements

The authors want to thank the generous support from the US-Israel Binational Science Foundation (BSF; grant #2011266).
Jing-Jing Liu, Diptendu Mukherjee, Doron Haritan, Bogna Ignatowska-Jankowska, Ji Liu, Ami Citri and Zhiping P. Pang declare that they have no conflict of interests. This article does not contain any studies with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(1901 KB)

Accesses

Citations

Detail

Sections
Recommended

/