Activation of VTA GABA Neurons Disrupts Reward Consumption

Neuron

Volumn 73, Issue 6, 2012, Pages 1184-1194

  Van Zessen, Ruud ^a,b   Phillips, Jana L ^a   Budygin, Evgeny A ^c   Stuber, Garret D ^a  

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

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICIPATION; ARTICLE; ASSOCIATION; CONDITIONING; CONTROLLED STUDY; FOREBRAIN; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; IN VIVO STUDY; MOUSE; NERVE CELL STIMULATION; NERVE EXCITABILITY; NERVE PROJECTION; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REWARD; SIGNAL DETECTION; VENTRAL TEGMENTUM;

ANALYSIS OF VARIANCE; ANIMALS; BACTERIAL PROTEINS; BEHAVIOR, ANIMAL; BIOPHYSICS; CUES; DOPAMINE; DOPAMINERGIC NEURONS; ELECTRIC STIMULATION; EXPLORATORY BEHAVIOR; FOOD PREFERENCES; GABA ANTAGONISTS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL PATHWAYS; OPTICS AND PHOTONICS; PATCH-CLAMP TECHNIQUES; PYRIDAZINES; REWARD; RHODOPSIN; SUBSTANTIA NIGRA; SUCROSE; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84858626050     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.02.016     Document Type: Article

References (63)

1. Adamantidis A.R., Tsai H.C., Boutrel B., Zhang F., Stuber G.D., Budygin E.A., Tourino C., Bonci A., Deisseroth K., de Lecea L. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J. Neurosci. 2011, 31:10829-10835.
2. Bonci A., Williams J.T. Increased probability of GABA release during withdrawal from morphine. J. Neurosci. 1997, 17:796-803.
3. Brischoux F., Chakraborty S., Brierley D.I., Ungless M.A. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc. Natl. Acad. Sci. USA 2009, 106:4894-4899.
4. Bromberg-Martin E.S., Hikosaka O. Midbrain dopamine neurons signal preference for advance information about upcoming rewards. Neuron 2009, 63:119-126.
5. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.
6. Chergui K., Charlety 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.
7. Cohen J.Y., Haesler S., Vong L., Lowell B.B., Uchida N. Neuro-type-specific signalts for reward and punishment in the ventral tegmental area. Nature 2012, 482:85-88.
8. Cousins M.S., Sokolowski J.D., Salamone J.D. Different effects of nucleus accumbens and ventrolateral striatal dopamine depletions on instrumental response selection in the rat. Pharmacol. Biochem. Behav. 1993, 46:943-951.
9. Day J.J., Roitman M.F., Wightman R.M., Carelli R.M. Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens. Nat. Neurosci. 2007, 10:1020-1028.
10. Deister C.A., Teagarden M.A., Wilson C.J., Paladini C.A. An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J. Neurosci. 2009, 29:15888-15897.
11. Fields H.L., Hjelmstad G.O., Margolis E.B., Nicola S.M. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu. Rev. Neurosci. 2007, 30:289-316.
12. Hanlon E.C., Baldo B.A., Sadeghian K., Kelley A.E. Increases in food intake or food-seeking behavior induced by GABAergic, opioid, or dopaminergic stimulation of the nucleus accumbens: is it hunger?. Psychopharmacology (Berl.) 2004, 172:241-247.
13. Ikemoto S., Panksepp J. Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav. Neurosci. 1996, 110:331-345.
14. Jhou T.C., Fields H.L., Baxter M.G., Saper C.B., Holland P.C. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 2009, 61:786-800.
15. Johnson S.W., North R.A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 1992, 12:483-488.
16. Johnson S.W., North R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J. Physiol. 1992, 450:455-468.
17. 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.
18. Kelley A.E. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci. Biobehav. Rev. 2004, 27:765-776.
19. Kiyatkin E.A., Rebec G.V. Heterogeneity of ventral tegmental area neurons: single-unit recording and iontophoresis in awake, unrestrained rats. Neuroscience 1998, 85:1285-1309.
20. Krause M., German P.W., Taha S.A., Fields H.L. A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J. Neurosci. 2010, 30:4746-4756.
21. Lobb C.J., Wilson C.J., Paladini C.A. A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. J. Neurophysiol. 2010, 104:403-413.
22. Luscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
23. Madhavan A., Bonci A., Whistler J.L. Opioid-Induced GABA potentiation after chronic morphine attenuates the rewarding effects of opioids in the ventral tegmental area. J. Neurosci. 2010, 30:14029-14035.
24. Margolis E.B., Lock H., Hjelmstad G.O., Fields H.L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?. J. Physiol. 2006, 577:907-924.
25. Matsumoto M., Hikosaka O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 2009, 459:837-841.
26. Mileykovskiy B., Morales M. Duration of inhibition of ventral tegmental area dopamine neurons encodes a level of conditioned fear. J. Neurosci. 2011, 31:7471-7476.
27. Mirenowicz J., Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 1996, 379:449-451.
28. 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.
29. Nestler E.J., Carlezon W.A. The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 2006, 59:1151-1159.
30. Nowend K.L., Arizzi M., Carlson B.B., Salamone J.D. D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption. Pharmacol. Biochem. Behav. 2001, 69:373-382.
31. Nugent F.S., Penick E.C., Kauer J.A. Opioids block long-term potentiation of inhibitory synapses. Nature 2007, 446:1086-1090.
32. Overton P., Clark D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 1992, 10:131-140.
33. Paladini C.A., Tepper J.M. GABA(A) and GABA(B) antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse 1999, 32:165-176.
34. Paladini C.A., Iribe Y., Tepper J.M. GABAA receptor stimulation blocks NMDA-induced bursting of dopaminergic neurons in vitro by decreasing input resistance. Brain Res. Brain Res. Rev. 1999, 832:145-151.
35. Pan W.X., Schmidt R., Wickens J.R., Hyland B.I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J. Neurosci. 2005, 25:6235-6242.
36. Phillips P.E., Stuber G.D., Heien M.L., Wightman R.M., Carelli R.M. Subsecond dopamine release promotes cocaine seeking. Nature 2003, 422:614-618.
37. Roitman M.F., Stuber G.D., Phillips P.E., Wightman R.M., Carelli R.M. Dopamine operates as a subsecond modulator of food seeking. J. Neurosci. 2004, 24:1265-1271.
38. Salamone J.D., Zigmond M.J., Stricker E.M. Characterization of the impaired feeding behavior in rats given haloperidol or dopamine-depleting brain lesions. Neuroscience 1990, 39:17-24.
39. Salamone J.D., Mahan K., Rogers S. Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol. Biochem. Behav. 1993, 44:605-610.
40. Salamone J.D., Wisniecki A., Carlson B.B., Correa M. Nucleus accumbens dopamine depletions make animals highly sensitive to high fixed ratio requirements but do not impair primary food reinforcement. Neuroscience 2001, 105:863-870.
41. Schultz W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 1998, 80:1-27.
42. Sparta D.R., Stamatakis A.M., Phillips J.L., Hovelso N., van Zessen R., Stuber G.D. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat. Protoc. 2011, 7:12-23.
43. Steffensen S.C., Svingos A.L., Pickel V.M., Henriksen S.J. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J. Neurosci. 1998, 18:8003-8015.
44. Stuber G.D., Wightman R.M., Carelli R.M. Extinction of cocaine self-administration reveals functionally and temporally distinct dopaminergic signals in the nucleus accumbens. Neuron 2005, 46:661-669.
45. Stuber G.D., Klanker M., de Ridder B., Bowers M.S., Joosten R.N., Feenstra M.G., Bonci A. Reward-predictive cues enhance excitatory synaptic strength onto midbrain dopamine neurons. Science 2008, 321:1690-1692.
46. Stuber G.D., Hnasko T.S., Britt J.P., Edwards R.H., Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci. 2010, 30:8229-8233.
47. 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., et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 2011, 475:377-380.
48. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
49. 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.
50. 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. this issue.
51. Tecuapetla F., Patel J.C., Xenias H., English D., Tadros I., Shah F., Berlin J., Deisseroth K., Rice M.E., Tepper J.M., et al. Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J. Neurosci. 2010, 30:7105-7110.
52. Tobler P.N., Fiorillo C.D., Schultz W. Adaptive coding of reward value by dopamine neurons. Science 2005, 307:1642-1645.
53. Tsai H.C., Zhang F., Adamantidis A., Stuber G.D., Bonci A., de Lecea L., Deisseroth K. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009, 324:1080-1084.
54. Ungerstedt U. Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol. Scand. Suppl. 1971, 367:95-122.
55. Ungless M.A., Argilli E., Bonci A. Effects of stress and aversion on dopamine neurons: implications for addiction. Neurosci. Biobehav. Rev. 2010, 35:151-156.
56. Van Bockstaele E.J., Pickel V.M. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res. 1995, 682:215-221.
57. Vong L., Ye C., Yang Z., Choi B., Chua S., Lowell B.B. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 2011, 71:142-154.
58. Waelti P., Dickinson A., Schultz W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 2001, 412:43-48.
59. Wise R.A. Dopamine, learning and motivation. Nat. Rev. Neurosci. 2004, 5:483-494.
60. Witten I.B., Steinberg E.E., Lee S.Y., Davidson T.J., Zalocusky K.A., Brodsky M., Yizhar O., Cho S.L., Gong S., Ramakrishnan C., et al. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 2011, 72:721-733.
61. Yamaguchi T., Wang H.L., Li X., Ng T.H., Morales M. Mesocorticolimbic glutamatergic pathway. J. Neurosci. 2011, 31:8476-8490.
62. Zweifel L.S., Parker J.G., Lobb C.J., Rainwater A., Wall V.Z., Fadok J.P., Darvas M., Kim M.J., Mizumori S.J., Paladini C.A., et al. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc. Natl. Acad. Sci. USA 2009, 106:7281-7288.
63. Zweifel L.S., Fadok J.P., Argilli E., Garelick M.G., Jones G.L., Dickerson T.M., Allen J.M., Mizumori S.J., Bonci A., Palmiter R.D. Activation of dopamine neurons is critical for aversive conditioning and prevention of generalized anxiety. Nat. Neurosci. 2011, 14:620-626.