Inhibitory Input from the Lateral Hypothalamus to the Ventral Tegmental Area Disinhibits Dopamine Neurons and Promotes Behavioral Activation

Neuron

Volumn 90, Issue 6, 2016, Pages 1286-1298

  Nieh, Edward H ^a   Vander Weele, Caitlin M ^a   Matthews, Gillian A ^a   Presbrey, Kara N ^a   Wichmann, Romy ^a   Leppla, Christopher A ^a   Izadmehr, Ehsan M ^a   Tye, Kay M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; 4 AMINOBUTYRIC ACID RECEPTOR;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIOR; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; FEMALE; GABAERGIC SYSTEM; GLUTAMATERGIC SYNAPSE; LATERAL HYPOTHALAMUS; MALE; MOTIVATION; MOUSE; NERVE TRACT; NONHUMAN; NUCLEUS ACCUMBENS; PHOTOACTIVATION; PLACE AVOIDANCE; PLACE PREFERENCE; PRIORITY JOURNAL; REINFORCEMENT; SOCIAL INTERACTION; VENTRAL TEGMENTUM; ANIMAL; ANIMAL BEHAVIOR; METABOLISM; NERVE CELL INHIBITION; PHYSIOLOGY; REWARD;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DOPAMINE; DOPAMINERGIC NEURONS; GABAERGIC NEURONS; HYPOTHALAMIC AREA, LATERAL; MICE; NEURAL INHIBITION; NUCLEUS ACCUMBENS; REWARD; VENTRAL TEGMENTAL AREA;

EID: 84970028600     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.04.035     Document Type: Article

References (80)

1. Albert D.J., Nanji N., Brayley K.N., Madryga F.J. Hyperreactivity as well as mouse killing is induced by electrical stimulation of the lateral hypothalamus in the rat. Behav. Neural Biol. 1979, 27:59-71.
2. Anand B.K., Brobeck J.R. Localization of a "feeding center" in the hypothalamus of the rat. Proc. Soc. Exp. Biol. Med. Soc. Exp. Biol. Med. N. Y. 1951, 77:323-324.
3. Andersson J.L., Nomikos G.G., Marcus M., Hertel P., Mathé J.M., Svensson T.H. Ritanserin potentiates the stimulatory effects of raclopride on neuronal activity and dopamine release selectivity in the mesolimbic dopaminergic system. Naunyn Schmiedebergs Arch. Pharmacol. 1995, 352:374-385.
4. Aragona B.J., Cleaveland N.A., Stuber G.D., Day J.J., Carelli R.M., Wightman R.M. Preferential enhancement of dopamine transmission within the nucleus accumbens shell by cocaine is attributable to a direct increase in phasic dopamine release events. J. Neurosci. 2008, 28:8821-8831.
5. Barbano M.F., Wang H.-L., Morales M., Wise R.A. Feeding and reward are differentially induced by activating GABAergic lateral hypothalamic projections to VTA. J. Neurosci. 2016, 36:2975-2985.
6. Berk M.L., Finkelstein J.A. Efferent connections of the lateral hypothalamic area of the rat: an autoradiographic investigation. Brain Res. Bull. 1982, 8:511-526.
7. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res. Brain Res. Rev. 1998, 28:309-369.
8. Berthoud H.-R., Münzberg H. The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol. Behav. 2011, 104:29-39.
9. Betley J.N., Xu S., Cao Z.F.H., Gong R., Magnus C.J., Yu Y., Sternson S.M. Neurons for hunger and thirst transmit a negative-valence teaching signal. Nature 2015, 521:180-185.
10. Bielajew C., Shizgal P. Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle. J. Neurosci. 1986, 6:919-929.
11. Black D.W., Moyer T. Clinical features and psychiatric comorbidity of subjects with pathological gambling behavior. Psychiatr. Serv. 1998, 49:1434-1439.
12. Bocklisch C., Pascoli V., Wong J.C.Y., House D.R.C., Yvon C., de Roo M., Tan K.R., Lüscher C. Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 2013, 341:1521-1525.
13. 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 2006, 49:589-601.
14. Burton M.J., Rolls E.T., Mora F. Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food. Exp. Neurol. 1976, 51:668-677.
15. Cannon W.B. Organization for physiological homeostasis. Physiol. Rev. 1929, 9:399-431.
16. Chen T.-W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
17. Chergui K., Charléty P.J., Akaoka H., Saunier C.F., Brunet J.-L., Buda M., Svensson T.H., Chouvet G. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur. J. Neurosci. 1993, 5:137-144.
18. Collins A.L., Greenfield V.Y., Bye J.K., Linker K.E., Wang A.S., Wassum K.M. Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation. Sci. Rep. 2016, 6:20231.
19. Cunningham-Williams R.M., Cottler L.B., Compton W.M., Spitznagel E.L. Taking chances: problem gamblers and mental health disorders--results from the St. Louis Epidemiologic Catchment Area Study. Am. J. Public Health 1998, 88:1093-1096.
20. David V., Durkin T.P., Cazala P. Self-administration of the GABAA antagonist bicuculline into the ventral tegmental area in mice: dependence on D2 dopaminergic mechanisms. Psychopharmacology (Berl.) 1997, 130:85-90.
21. Di Chiara G., Imperato A. Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA 1988, 85:5274-5278.
22. Di Ciano P., Cardinal R.N., Cowell R.A., Little S.J., Everitt B.J. 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. 2001, 21:9471-9477.
23. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J. Neurosci. 1993, 13:3839-3847.
24. Dobi A., Margolis E.B., Wang H.-L., Harvey B.K., Morales M. Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J. Neurosci. 2010, 30:218-229.
25. Dreyer J.K., Vander Weele C.M., Lovic V., Aragona B.J. Functionally Distinct Dopamine Signals in Nucleus Accumbens Core and Shell in the Freely Moving Rat. J. Neurosci. 2016, 36:98-112.
26. Everitt B.J., Parkinson J.A., Olmstead M.C., Arroyo M., Robledo P., Robbins T.W. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann. N Y Acad. Sci. 1999, 877:412-438.
27. Faber R.J., Christenson G.A., De Zwaan M., Mitchell J. Two forms of compulsive consumption: comorbidity of compulsive buying and binge eating. J. Consum. Res. 1995, 22:296-304.
28. Gallistel C.R., Gomita Y., Yadin E., Campbell K.A. Forebrain origins and terminations of the medial forebrain bundle metabolically activated by rewarding stimulation or by reward-blocking doses of pimozide. J. Neurosci. 1985, 5:1246-1261.
29. Grace A.A., Floresco S.B., Goto Y., Lodge D.J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 2007, 30:220-227.
30. Grossman S.P., Dacey D., Halaris A.E., Collier T., Routtenberg A. Aphagia and adipsia after preferential destruction of nerve cell bodies in hypothalamus. Science 1978, 202:537-539.
31. Gunaydin L.A., Grosenick L., Finkelstein J.C., Kauvar I.V., Fenno L.E., Adhikari A., Lammel S., Mirzabekov J.J., Airan R.D., Zalocusky K.A., et al. Natural neural projection dynamics underlying social behavior. Cell 2014, 157:1535-1551.
32. Hamid A.A., Pettibone J.R., Mabrouk O.S., Hetrick V.L., Schmidt R., Vander Weele C.M., Kennedy R.T., Aragona B.J., Berke J.D. Mesolimbic dopamine signals the value of work. Nat. Neurosci. 2016, 19:117-126.
33. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature 2005, 437:556-559.
34. Hoebel B.G., Teitelbaum P. Hypothalamic control of feeding and self-stimulation. Science 1962, 135:375-377.
35. Horvitz J.C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 2000, 96:651-656.
36. Howe M.W., Tierney P.L., Sandberg S.G., Phillips P.E.M., Graybiel A.M. Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 2013, 500:575-579.
37. Ikemoto S., Murphy J.M., McBride W.J. Self-infusion of GABA(A) antagonists directly into the ventral tegmental area and adjacent regions. Behav. Neurosci. 1997, 111:369-380.
38. Ikemoto S., Murphy J.M., McBride W.J. Regional differences within the rat ventral tegmental area for muscimol self-infusions. Pharmacol. Biochem. Behav. 1998, 61:87-92.
39. Ito R., Dalley J.W., Robbins T.W., Everitt B.J. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J. Neurosci. 2002, 22:6247-6253.
40. Jennings J.H., Ung R.L., Resendez S.L., Stamatakis A.M., Taylor J.G., Huang J., Veleta K., Kantak P.A., Aita M., Shilling-Scrivo K., et al. Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 2015, 160:516-527.
41. Johnson S.W., North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 1992, 12:483-488.
42. Johnson S.W., Seutin V., North R.A. Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science 1992, 258:665-667.
43. 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. Hypothalamic neurotensin projections promote reward by enhancing glutamate transmission in the VTA. J. Neurosci. 2013, 33:7618-7626.
44. Klapoetke N.C., Murata Y., Kim S.S., Pulver S.R., Birdsey-Benson A., Cho Y.K., Morimoto T.K., Chuong A.S., Carpenter E.J., Tian Z., et al. Independent optical excitation of distinct neural populations. Nat. Methods 2014, 11:338-346.
45. Ko D., Wanat M.J. Phasic Dopamine Transmission Reflects Initiation Vigor and Exerted Effort in an Action- and Region-Specific Manner. J. Neurosci. 2016, 36:2202-2211.
46. Lammel S., Hetzel A., Häckel O., Jones I., Liss B., Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773.
47. Lammel S., Ion D.I., Roeper J., Malenka R.C. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 2011, 70:855-862.
48. Lammel S., Lim B.K., Ran C., Huang K.W., Betley M.J., Tye K.M., Deisseroth K., Malenka R.C. Input-specific control of reward and aversion in the ventral tegmental area. Nature 2012, 491:212-217.
49. 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., et al. Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab. 2009, 10:89-98.
50. Nair-Roberts R.G., Chatelain-Badie S.D., Benson E., White-Cooper H., Bolam J.P., Ungless M.A. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 2008, 152:1024-1031.
51. Navarro M., Olney J.J., Burnham N.W., Mazzone C.M., Lowery-Gionta E.G., Pleil K.E., Kash T.L., Thiele T.E. Lateral hypothalamus GABAergic neurons modulate consummatory behaviors regardless of the caloric content or biological relevance of the consumed stimuli. Neuropsychopharmacology 2016, 41:1505-1512.
52. Nieh E.H., Matthews G.A., Allsop S.A., Presbrey K.N., Leppla C.A., Wichmann R., Neve R., Wildes C.P., Tye K.M. Decoding neural circuits that control compulsive sucrose seeking. Cell 2015, 160:528-541.
53. Niv Y., Daw N.D., Joel D., Dayan P. Tonic dopamine: opportunity costs and the control of response vigor. Psychopharmacology (Berl.) 2007, 191:507-520.
54. Olds J., Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 1954, 47:419-427.
55. Opland D., Sutton A., Woodworth H., Brown J., Bugescu R., Garcia A., Christensen L., Rhodes C., Myers M., Leinninger G. Loss of neurotensin receptor-1 disrupts the control of the mesolimbic dopamine system by leptin and promotes hedonic feeding and obesity. Mol. Metab. 2013, 2:423-434.
56. Owesson-White C.A., Roitman M.F., Sombers L.A., Belle A.M., Keithley R.B., Peele J.L., Carelli R.M., Wightman R.M. Sources contributing to the average extracellular concentration of dopamine in the nucleus accumbens. J. Neurochem. 2012, 121:252-262.
57. Phillips P.E.M., Stuber G.D., Heien M.L.A.V., Wightman R.M., Carelli R.M. Subsecond dopamine release promotes cocaine seeking. Nature 2003, 422:614-618.
58. Phillipson O.T. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J. Comp. Neurol. 1979, 187:117-143.
59. Powley T.L., Keesey R.E. Relationship of body weight to the lateral hypothalamic feeding syndrome. J. Comp. Physiol. Psychol. 1970, 70:25-36.
60. Rick C.E., Lacey M.G. Rat substantia nigra pars reticulata neurones are tonically inhibited via GABAA, but not GABAB, receptors in vitro. Brain Res. 1994, 659:133-137.
61. Roberts D.C.S., Koob G.F. Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats. Pharmacol. Biochem. Behav. 1982, 17:901-904.
62. Salamone J.D., Correa M. The mysterious motivational functions of mesolimbic dopamine. Neuron 2012, 76:470-485.
63. Salamone J.D., Cousins M.S., McCullough L.D., Carriero D.L., Berkowitz R.J. Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption. Pharmacol. Biochem. Behav. 1994, 49:25-31.
64. Salamone J.D., Correa M., Mingote S.M., Weber S.M. Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr. Opin. Pharmacol. 2005, 5:34-41.
65. Saper C.B., Swanson L.W., Cowan W.M. An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J. Comp. Neurol. 1979, 183:689-706.
66. Saunders B.T., Robinson T.E. The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur. J. Neurosci. 2012, 36:2521-2532.
67. Singh J., Desiraju T., Raju T.R. Comparison of intracranial self-stimulation evoked from lateral hypothalamus and ventral tegmentum: analysis based on stimulation parameters and behavioural response characteristics. Brain Res. Bull. 1996, 41:399-408.
68. Stricker E.M., Swerdloff A.F., Zigmond M.J. Intrahypothalamic injections of kainic acid produce feeding and drinking deficits in rats. Brain Res. 1978, 158:470-473.
69. Stuber G.D., Wise R.A. Lateral hypothalamic circuits for feeding and reward. Nat. Neurosci. 2016, 19:198-205.
70. Sugita S., Johnson S.W., North R.A. Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons. Neurosci. Lett. 1992, 134:207-211.
71. Szczypka M.S., Mandel R.J., Donahue B.A., Snyder R.O., Leff S.E., Palmiter R.D. Viral gene delivery selectively restores feeding and prevents lethality of dopamine-deficient mice. Neuron 1999, 22:167-178.
72. Szczypka M.S., Kwok K., Brot M.D., Marck B.T., Matsumoto A.M., Donahue B.A., Palmiter R.D. Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 2001, 30:819-828.
73. Tan K.R., Yvon C., Turiault M., Mirzabekov J.J., Doehner J., Labouèbe G., Deisseroth K., Tye K.M., Lüscher C. GABA neurons of the VTA drive conditioned place aversion. Neuron 2012, 73:1173-1183.
74. Valenstein E.S., Cox V.C., Kakolewski J.W. Modification of motivated behavior elicited by electrical stimulation of the hypothalamus. Science 1968, 159:1119-1121.
75. van Zessen R., Phillips J.L., Budygin E.A., Stuber G.D. Activation of VTA GABA neurons disrupts reward consumption. Neuron 2012, 73:1184-1194.
76. Vanderschuren L.J.M.J., Di Ciano P., Everitt B.J. Involvement of the dorsal striatum in cue-controlled cocaine seeking. J. Neurosci. 2005, 25:8665-8670.
77. Watabe-Uchida M., Zhu L., Ogawa S.K., Vamanrao A., Uchida N. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 2012, 74:858-873.
78. Wise R.A. Role of brain dopamine in food reward and reinforcement. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2006, 361:1149-1158.
79. Wyvell C.L., Berridge K.C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J. Neurosci. 2000, 20:8122-8130.
80. You Z.-B., Chen Y.-Q., Wise R.A. Dopamine and glutamate release in the nucleus accumbens and ventral tegmental area of rat following lateral hypothalamic self-stimulation. Neuroscience 2001, 107:629-639.