Lateral hypothalamic area glutamatergic neurons and their projections to the lateral habenula regulate feeding and reward

Journal of Neuroscience

Volumn 36, Issue 2, 2016, Pages 302-311

  Stamatakis, Alice M ^a,b   Van Swieten, Maaike ^a,c   Basiri, Marcus L ^a,b   Blair, Grace A ^a   Kantak, Pranish ^a   Stuber, Garret D ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Aversion; Feeding; Habenula; Hypothalamus; Optogenetics; Reward

Indexed keywords

BACTERIAL PROTEIN; CASPASE 3; FLUORESCENT DYE; GLUTAMIC ACID; PHOTOPROTEIN; SLC17A6 PROTEIN, MOUSE; VESICULAR GLUTAMATE TRANSPORTER 2; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VIAAT PROTEIN, MOUSE; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL; C57BL MOUSE; CYTOLOGY; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; GENE VECTOR; GENETICS; HABENULA; INSTRUMENTAL CONDITIONING; LATERAL HYPOTHALAMUS; MALE; METABOLISM; MOUSE; NERVE CELL; NERVE TRACT; PHYSIOLOGY; REWARD; TRANSGENIC MOUSE;

ANIMALS; BACTERIAL PROTEINS; CASPASE 3; CONDITIONING, OPERANT; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; FLUORESCENT DYES; GENETIC VECTORS; GLUTAMIC ACID; HABENULA; HYPOTHALAMIC AREA, LATERAL; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL PATHWAYS; NEURONS; REWARD; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84954350379     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1202-15.2016     Document Type: Article

References (39)

1. Aponte Y, Atasoy D, Sternson SM (2011) AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat Neurosci 14:351-355. CrossRef Medline
2. Atasoy D, Betley JN, Su HH, SternsonSM (2012) Deconstruction of a neural circuit for hunger. Nature 488:172-177. CrossRef Medline
3. Berk ML, Finkelstein JA (1982) Efferent connections of the lateral hypothalamic area of the rat: an autoradiographic investigation. Brain Res Bull 8:511-526. CrossRef Medline
4. 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
5. Chen Y, Lin YC, Kuo TW, Knight ZA (2015) Sensory detection of food rapidly modulates arcuate feeding circuits. Cell 160:829-841. CrossRef Medline
6. Christoph GR, Leonzio RJ, Wilcox KS (1986) Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci 6:613- 619. Medline
7. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW (2010) Pathwayspecific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65:230 -245. CrossRef Medline
8. Geisler S, Zahm DS (2005) Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490: 270-294. CrossRef Medline
9. Geisler S, Derst C, Veh RW, Zahm DS (2007) Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27:5730 -5743. CrossRef Medline
10. Harrell LE, Decastro JM, Balagura S (1975) A critical evaluation of body weight loss following lateral hypothalamic lesions. Physiol Behav 15:133- 136. CrossRef Medline
11. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556 -559. CrossRef Medline
12. Hoebel BG, Teitelbaum P (1962) Hypothalamic control of feeding and selfstimulation. Science 135:375-377. CrossRef Medline
13. Jennings JH, Rizzi G, Stamatakis AM, Ung RL, Stuber GD (2013) The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science 341:1517-1521. CrossRef Medline
14. Jennings JH, Ung RL, Resendez SL, Stamatakis AM, Taylor JG, Huang J, Veleta K, Kantak PA, Aita M, Shilling-Scrivo K, Ramakrishnan C, Deisseroth K, Otte S, Stuber GD (2015) Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 160:516 -527. CrossRef Medline
15. Kempadoo KA, Tourino C, Cho SL, Magnani F, Leinninger GM, Stuber GD, Zhang F, Myers MG, 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. CrossRef Medline
16. Krashes MJ, Koda S, Ye C, Rogan SC, Adams AC, Cusher DS, Maratos-Flier E, Roth BL, Lowell BB (2011) Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J Clin Invest 121:1424 -1428. CrossRef Medline
17. Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212-217. CrossRef Medline
18. Leinninger GM, Jo YH, Leshan RL, Louis GW, Yang H, Barrera JG, Wilson H, Opland DM, Faouzi MA, Gong Y, Jones JC, Rhodes CJ, Chua S Jr, Diano S, Horvath TL, Seeley RJ, Becker JB, Münzberg H, Myers MG Jr (2009) Leptin acts via leptin receptor-expressing lateral hypothalamic neurons to modulate the mesolimbic dopamine system and suppress feeding. Cell Metab 10:89 -98. CrossRef Medline
19. Luquet S, Perez FA, Hnasko TS, Palmiter RD (2005) NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310:683- 685. CrossRef Medline
20. Margules DL, Olds J (1962) Identical "feeding" and "rewarding" systems in the lateral hypothalamus of rats. Science 135:374 -375. CrossRef Medline
21. Matsui A, Williams JT (2011) Opioid-sensitive GABA inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J Neurosci 31:17729 -17735. CrossRef Medline
22. Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111-1115. CrossRef Medline
23. Meister B (2007) Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav 92:263- 271. CrossRef Medline
24. Nieh EH, Matthews GA, Allsop SA, Presbrey KN, Leppla CA, Wichmann R, Neve R, Wildes CP, Tye KM (2015) Decoding neural circuits that control compulsive sucrose seeking. Cell 160:528 -541. CrossRef Medline
25. Oertel WH, Nitsch C, Mugnaini E (1984) Immunocytochemical demonstration of the GABA-ergic neurons in rat globus pallidus and nucleus entopeduncularis and their GABA-ergic innervation. Adv Neurol 40:91- 98. Medline
26. Poller WC, Madai VI, Bernard R, Laube G, Veh RW (2013) A glutamatergic pro- jection from the lateral hypothalamus targets VTA-projecting neurons in the lateral habenula of the rat. Brain Res 1507:45-60. CrossRef Medline
27. Root DH, Mejias-Aponte CA, Qi J, MoralesM (2014) Role of glutamatergic projections from ventral tegmental area to lateral habenula in aversive conditioning. J Neurosci 34:13906 -13910. CrossRef Medline
28. Rosin DL, Weston MC, Sevigny CP, Stornetta RL, Guyenet PG (2003) Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J Comp Neurol 465:593- 603. CrossRef Medline
29. Saper CB, Chou TC, Elmquist JK (2002) The need to feed: homeostatic and hedonic control of eating. Neuron 36:199 -211. CrossRef Medline
30. Schallert T, Whishaw IQ (1978) Two types of aphagia and two types of sensorimotor impairment after lateral hypothalamic lesions: observations in normal weight, dieted, and fattened rats. J Comp Physiol Psychol 92: 720-741. Medline
31. Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74:475- 481. CrossRef Medline
32. Shabel SJ, Proulx CD, Piriz J, Malinow R (2014) Mood regulation. GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment. Science 345:1494 -1498. CrossRef Medline
33. Stamatakis AM, Stuber GD (2012) Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci 15: 1105-1107. CrossRef Medline
34. Stamatakis AM, Jennings JH, Ung RL, Blair GA, Weinberg RJ, Neve RL, Boyce F, Mattis J, Ramakrishnan C, Deisseroth K, Stuber GD (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80:1039 -1053. CrossRef Medline
35. Stephenson DT, Li Q, Simmons C, Connell MA, Meglasson MD, Merchant K, Emborg ME (2005) Expression of GAD65 and GAD67 immunoreactivity in MPTP-treated monkeys with or without L-DOPA administration. Neurobiol Dis 20:347-359. CrossRef Medline
36. van denTop M, Lee K, Whyment AD, Blanks AM, Spanswick D (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7:493- 494. CrossRef Medline Von Der
37. Porten K, Davis JR (1979) Weight loss following LH lesions independent of changes in motor activity or metabolic rate. Physiol Behav 23:813- 819. Medline
38. Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell BB (2011) Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154. CrossRef Medline
39. Yang CF, Chiang MC, Gray DC, Prabhakaran M, Alvarado M, Juntti SA, Unger EK, Wells JA, Shah NM (2013) Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153:896 -909. CrossRef Medline