The heterogeneity of ventral tegmental area neurons: Projection functions in a mood-related context

Neuroscience

Volumn 282, Issue , 2014, Pages 101-108

  Walsh, J J ^a   Han, M H ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Animal models; Depression; Mood disorders; Neural circuits; Projection functions; Ventral tegmental area

Indexed keywords

AMPA RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VESICULAR GLUTAMATE TRANSPORTER 2;

AMYGDALOID NUCLEUS; ANHEDONIA; AVERSIVE BEHAVIOR; BRAIN NERVE CELL; CELL HETEROGENEITY; DEPRESSION; DOPAMINERGIC NERVE CELL; GABAERGIC SYSTEM; HUMAN; IMMOBILIZATION STRESS; MOOD DISORDER; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; NUCLEUS ACCUMBENS; OPTOGENETICS; PATHOGENESIS; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; REWARD; SOCIAL STRESS; VENTRAL TEGMENTUM; VIRAL GENE DELIVERY SYSTEM; AMYGDALA; ANIMAL; METABOLISM; NERVE CELL; NERVE TRACT; PHYSIOLOGY; CELL FUNCTION; CELLULAR DISTRIBUTION; MEDIAL PREFRONTAL CORTEX; NERVE CONDUCTION; NEUROCHEMISTRY; NEUROPHYSIOLOGY; PROTEIN EXPRESSION;

AMYGDALA; ANIMALS; HUMANS; MOOD DISORDERS; NEURAL PATHWAYS; NEURONS; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; REWARD; VENTRAL TEGMENTAL AREA;

EID: 84906322854     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.06.006     Document Type: Review

References (65)

1. Anstrom K.K., Woodward D.J. Restraint increases dopaminergic burst firing in awake rats. Neuropsychopharmacology 2005, 30:1832-1840.
2. Argilli E., Sibley D.R., Malenka R.C., England P.M., Bonci A. Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J Neurosci 2008, 28:9092-9100.
3. Bannon M.J., Roth R.H. Pharmacology of mesocortical dopamine neurons. Pharmacol Rev 1983, 35:53-68.
4. Bayer V.E., Pickel V.M. GABA-labeled terminals form proportionally more synapses with dopaminergic neurons containing low densities of tyrosine hydroxylase-immunoreactivity in rat ventral tegmental area. Brain Res 1991, 559:44-55.
5. Berton O., McClung C.A., Dileone R.J., Krishnan V., Renthal W., Russo S.J., Graham D., Tsankova N.M., Bolanos C.A., Rios M., Monteggia L.M., Self D.W., Nestler E.J. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 2006, 311:864-868.
6. Berube-Carriere N., Riad M., Dal Bo G., Levesque D., Trudeau L.E., Descarries L. The dual dopamine-glutamate phenotype of growing mesencephalic neurons regresses in mature rat brain. J Comp Neurol 2009, 517:873-891.
7. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.
8. Cameron D.L., Wessendorf M.W., Williams J.T. A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids. Neuroscience 1997, 77:155-166.
9. Cao J.L., Covington H.E., Friedman A.K., Wilkinson M.B., Walsh J.J., Cooper D.C., Nestler E.J., Han M.H. Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J Neurosci 2010, 30:16453-16458.
10. Chaudhury D., Walsh J.J., Friedman A.K., Juarez B., Ku S.M., Koo J.W., Ferguson D., Tsai H.C., Pomeranz L., Christoffel D.J., Nectow A.R., Ekstrand M., Domingos A., Mazei-Robison M.S., Mouzon E., Lobo M.K., Neve R.L., Friedman J.M., Russo S.J., Deisseroth K., Nestler E.J., Han M.H. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 2013, 493:532-536.
11. Chen B.T., Bowers M.S., Martin M., Hopf F.W., Guillory A.M., Carelli R.M., Chou J.K., Bonci A. Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 2008, 59:288-297.
12. Dal Bo G., St-Gelais F., Danik M., Williams S., Cotton M., Trudeau L.E. Dopamine neurons in culture express VGLUT2 explaining their capacity to release glutamate at synapses in addition to dopamine. J Neurochem 2004, 88:1398-1405.
13. Dal Bo G., Berube-Carriere N., Mendez J.A., Leo D., Riad M., Descarries L., Levesque D., Trudeau L.E. Enhanced glutamatergic phenotype of mesencephalic dopamine neurons after neonatal 6-hydroxydopamine lesion. Neuroscience 2008, 156:59-70.
14. de Oliveira A.R., Reimer A.E., de Macedo C.E., de Carvalho M.C., Silva M.A., Brandao M.L. Conditioned fear is modulated by D2 receptor pathway connecting the ventral tegmental area and basolateral amygdala. Neurobiol Learn Mem 2011, 95:37-45.
15. de Oliveira A.R., Reimer A.E., Brandao M.L. Mineralocorticoid receptors in the ventral tegmental area regulate dopamine efflux in the basolateral amygdala during the expression of conditioned fear. Psychoneuroendocrinology 2014, 43:114-125.
16. Fadok J.P., Darvas M., Dickerson T.M., Palmiter R.D. Long-term memory for pavlovian fear conditioning requires dopamine in the nucleus accumbens and basolateral amygdala. PLoS One 2010, 5:e12751.
17. Feder A., Nestler E.J., Charney D.S. Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 2009, 10:446-457.
18. Ford C.P., Mark G.P., Williams J.T. Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 2006, 26:2788-2797.
19. Fremeau R.T., Kam K., Qureshi T., Johnson J., Copenhagen D.R., Storm-Mathisen J., Chaudhry F.A., Nicoll R.A., Edwards R.H. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 2004, 304:1815-1819.
20. Friedman A.K., Walsh J.J., Juarez B., Ku S.M., Chaudhury D., Wang J., Li X., Dietz D.M., Pan N., Vialou V.F., Neve R.L., Yue Z., Han M.H. Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science 2014, 344:313-319.
21. Grace A.A., Onn S.P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 1989, 9:3463-3481.
22. Greba Q., Gifkins A., Kokkinidis L. Inhibition of amygdaloid dopamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res 2001, 899:218-226.
23. Hnasko T.S., Hjelmstad G.O., Fields H.L., Edwards R.H. Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J Neurosci 2012, 32:15076-15085.
24. Kitai S.T., Shepard P.D., Callaway J.C., Scroggs R. Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 1999, 9:690-697.
25. Krishnan V., Han M.H., Graham D.L., Berton O., Renthal W., Russo S.J., Laplant Q., Graham A., Lutter M., Lagace D.C., Ghose S., Reister R., Tannous P., Green T.A., Neve R.L., Chakravarty S., Kumar A., Eisch A.J., Self D.W., Lee F.S., Tamminga C.A., Cooper D.C., Gershenfeld H.K., Nestler E.J. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 2007, 131:391-404.
26. Lammel S., Hetzel A., Hackel O., Jones I., Liss B., Roeper J. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 2008, 57:760-773.
27. 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.
28. 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.
29. Lamont E.W., Kokkinidis L. Infusion of the dopamine D1 receptor antagonist SCH 23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res 1998, 795:128-136.
30. Ljungberg T., Apicella P., Schultz W. Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 1992, 67:145-163.
31. Lobo M.K., Covington H.E., Chaudhury D., Friedman A.K., Sun H., Damez-Werno D., Dietz D.M., Zaman S., Koo J.W., Kennedy P.J., Mouzon E., Mogri M., Neve R.L., Deisseroth K., Han M.H., Nestler E.J. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 2010, 330:385-390.
32. Margolis E.B., Lock H., Chefer V.I., Shippenberg T.S., Hjelmstad G.O., Fields H.L. Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc Natl Acad Sci U S A 2006, 103:2938-2942.
33. Margolis E.B., Mitchell J.M., Ishikawa J., Hjelmstad G.O., Fields H.L. Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition. J Neurosci 2008, 28:8908-8913.
34. Margolis E.B., Toy B., Himmels P., Morales M., Fields H.L. Identification of rat ventral tegmental area GABAergic neurons. PLoS One 2012, 7:e42365.
35. Marinelli M., White F.J. Enhanced vulnerability to cocaine self-administration is associated with elevated impulse activity of midbrain dopamine neurons. J Neurosci 2000, 20:8876-8885.
36. Mendez J.A., Bourque M.J., Dal Bo G., Bourdeau M.L., Danik M., Williams S., Lacaille J.C., Trudeau L.E. Developmental and target-dependent regulation of vesicular glutamate transporter expression by dopamine neurons. J Neurosci 2008, 28:6309-6318.
37. Mirenowicz J., Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 1996, 379:449-451.
38. 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.
39. Nestler E.J., Carlezon W.A. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 2006, 59:1151-1159.
40. Omelchenko N., Sesack S.R. Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 2009, 63:895-906.
41. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
42. Razzoli M., Andreoli M., Michielin F., Quarta D., Sokal D.M. Increased phasic activity of VTA dopamine neurons in mice 3 weeks after repeated social defeat. Behav Brain Res 2011, 218:253-257.
43. Reimer R.J., Edwards R.H. Organic anion transport is the primary function of the SLC17/type I phosphate transporter family. Pflugers Arch 2004, 447:629-635.
44. Roeper J. Dissecting the diversity of midbrain dopamine neurons. TINS 2013, 36:336-342.
45. Schultz W. The phasic reward signal of primate dopamine neurons. Adv Pharmacol 1998, 42:686-690.
46. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 1998, 80:1-27.
47. Shi W.X. Electrophysiological characteristics of dopamine neurons: a 35-year update. J Neural Transm Suppl 2009, 103-119.
48. Shin L.M., Wright C.I., Cannistraro P.A., Wedig M.M., McMullin K., Martis B., Macklin M.L., Lasko N.B., Cavanagh S.R., Krangel T.S., Orr S.P., Pitman R.K., Whalen P.J., Rauch S.L. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 2005, 62:273-281.
49. 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.
50. 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.
51. Sulzer D., Joyce M.P., Lin L., Geldwert D., Haber S.N., Hattori T., Rayport S. Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 1998, 18:4588-4602.
52. Takamori S. VGLUTs: 'exciting' times for glutamatergic research?. Neurosci Res 2006, 55:343-351.
53. Tritsch N.X., Ding J.B., Sabatini B.L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 2012, 490:262-266.
54. 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.
55. Tye K.M., Mirzabekov J.J., Warden M.R., Ferenczi E.A., Tsai H.C., Finkelstein J., Kim S.Y., Adhikari A., Thompson K.R., Andalman A.S., Gunaydin L.A., Witten I.B., Deisseroth K. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 2013, 493:537-541.
56. Ungless M.A., Grace A.A. Are you or aren't you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci 2012, 35:422-430.
57. Ungless M.A., Whistler J.L., Malenka R.C., Bonci A. Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 2001, 411:583-587.
58. Valenti O., Cifelli P., Gill K.M., Grace A.A. Antipsychotic drugs rapidly induce dopamine neuron depolarization block in a developmental rat model of schizophrenia. J Neurosci 2011, 31:12330-12338.
59. Walsh J.J., Friedman A.K., Sun H., Heller E.A., Ku S.M., Juarez B., Burnham V.L., Mazei-Robison M.S., Ferguson D., Golden S.A., Koo J.W., Chaudhury D., Christoffel D.J., Pomeranz L., Friedman J.M., Russo S.J., Nestler E.J., Han M.H. Stress and CRF gate neural activation of BDNF in the mesolimbic reward pathway. Nat Neurosci 2014, 17:27-29.
60. Wise R.A., Bozarth M.A. Brain mechanisms of drug reward and euphoria. Psychiatr Med 1985, 3:445-460.
61. 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., Stuber G.D., Tye K.M., Janak P.H., Deisseroth K. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 2011, 72:721-733.
62. Yamaguchi T., Sheen W., Morales M. Glutamatergic neurons are present in the rat ventral tegmental area. Eur J Neurosci 2007, 25:106-118.
63. Yehuda R., LeDoux J. Response variation following trauma: a translational neuroscience approach to understanding PTSD. Neuron 2007, 56:19-32.
64. Yim C.Y., Mogenson G.J. Electrophysiological studies of neurons in the ventral tegmental area of Tsai. Brain Res 1980, 181:301-313.
65. Zhang T.A., Placzek A.N., Dani J.A. In vitro identification and electrophysiological characterization of dopamine neurons in the ventral tegmental area. Neuropharmacology 2010, 59:431-436.