The mesopontine rostromedial tegmental nucleus: An integrative modulator of the reward system

Basal Ganglia

Volumn 1, Issue 4, 2011, Pages 191-200

  Lavezzi, Heather N ^a   Zahm, Daniel S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Drug abuse; Reward; Substantia nigra compacta; Ventral tegmental area

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 3,4 METHYLENEDIOXYMETHAMPHETAMINE; 4 HYDROXYBUTYRIC ACID; ALCOHOL; AMPHETAMINE; CAFFEINE; DIAZEPAM; KETAMINE; MECAMYLAMINE; METHYLPHENIDATE; MORPHINE; NEUROTRANSMITTER; PHENCYCLIDINE; PSYCHOSTIMULANT AGENT; RIMONABANT; TETRAHYDROCANNABINOLIC ACID;

ANATOMICAL VARIATION; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; DOPAMINERGIC TRANSMISSION; DRUG ABUSE; DRUG DEPENDENCE; EFFERENT NERVE; GABAERGIC TRANSMISSION; HABENULA; MESOPONTINE ROSTROMEDIAL TEGMENTAL NUCLEUS; NERVE CELL; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY NERVE; SUBSTANTIA NIGRA PARS COMPACTA; TEGMENTUM; VENTRAL TEGMENTUM;

EID: 83155181553     PISSN: 22105336     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.baga.2011.08.003     Document Type: Review

References (100)

1. Dahlstrom A., Fuxe K. Localization of monoamines in the lower brain stem. Experientia 1964, 20:398-399.
2. Andén N.E., Carlsson A., Dahlström A., Fuxe K., Hillarp N.Å., Larsson K. Demonstration and mapping out of nigro-neostriatal dopaminergic neurons. Life Sci 1964, 3:523-530.
3. Andén N.E., Dahlström A., Fuxe K., Larsson K. Mapping out of catecholaminergic and 5-hydroxytryptamine neurons innervating the telencephalon and diencephalon. Life Sci 1965, 4:1275-1279.
4. Andén N.E., Dahlström A., Fuxe K., Larsson K., Olson L., Ungerstedt U. Ascending monoamine neurons to the telencephalon and diencephalon. Acta Physiol Scand 1966, 67:313-326.
5. Andén N.E., Fuxe K., Hamberger B., Hökfelt T. A quantitative study on the nigro-striatal dopamine neuron system in the rat. Acta Physiol Scand 1966, 67:306-312.
6. Björklund A., Lindvall O. Dopamine-containing systems in the CNS. Classical Transmitters in the CNS. Handbook of Chemical Neuroanatomy, vol. 2, Part I 1984, 55-122. Elsevier, Amsterdam. A. Björklund, T. Hökfelt (Eds.).
7. Kelly P.H., Seviour P.W., Iversen S.D. Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum. Brain Res 1975, 94:507-522.
8. Wise R.A. Dopamine, learning and motivation. Nature Rev Neurosci 2004, 5:1-12.
9. Guarraci F.A., Frohardt R.J., Kapp B.S. Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 1999, 827:28-40.
10. Guarraci F.A., Frohardt R.J., Falls W.A., Kapp B.S. The effects of intra-amygdaloid infusions of a D2 dopamine receptor antagonist on Pavlovian fear conditioning. Behav Neurosci 2000, 114:647-651.
11. Fadok J.P., Dickerson T.M., Palmiter R.D. Dopamine is necessary for cue-dependent fear conditioning. J Neurosci 2009, 29:11089-11097.
12. Kalivas P.W., Webber B. Amphetamine injection into the ventral mesencephalon sensitizes rats to peripheral amphetamine and cocaine. J Pharmacol ExpTherap 1988, 245:1095-1102.
13. Kalivas P.W., Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Rev 1991, 16:223-244.
14. Hooks M.S., Jones H.G., Liem B.J., Justice J.B. Sensitization and individual differences to IP amphetamine, cocaine, or caffeine following repeated intracranial amphetamine infusions. Pharmacol Biochem Behav 1992, 43:815-823.
15. Perugini M., Vezina P. Amphetamine administered to the ventral tegmental area sensitizes rats to the locomotor effects of nucleus accumbens amphetamine. J Pharmacol Exp Ther 1994, 270:690-696.
16. Cador M., Bjijou Y., Caihol S., Stinus L. d-amphetamine-induced behavioral sensitization: implication of a glutamatergic medial prefrontal cortex-ventral tegmental area innervation. Neurosci 1995, 94:705-721.
17. Cador M., Bjijou Y., Stinus L. Evidence of a complete independence of the neurobiological substrates for the induction and expression of behavioral sensitization to amphetamine. Neuroscience 1999, 65:385-395.
18. 1 receptors of the ventral tegmental area in the behavioral sensitization induced by intra-ventral tegmental area injections of d-amphetamine. J Pharmacol Exp Ther 1996, 277:1177-1187.
19. 1 dopamine receptor activation is necessary for the induction of sensitization by amphetamine in the ventral tegmental area. J Neurosci 1996, 16:2411-2420.
20. Vanderschuren L.J., Kalivas P.W. Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies. Psychopharmacol 2000, 151:99-120.
21. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol 1998, 80:1-27.
22. Schultz W. Multiple dopamine functions at different time courses. Ann Rev Neurosci 2007, 30:259-288.
23. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.
24. Herkenham M., Nauta W.J. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 1979, 187:19-47.
25. Araki M., McGeer P.L., Kimura H. The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method. Brain Res 1988, 441:319-330.
26. Omelchenko N., Sesack S.R. Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol 2006, 494:863-875.
27. Christoph G.R., Leonzio R.J., Wilcox K.S. Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci 1986, 6:613-619.
28. Gao D.M., Huffman D., Benabid A.L. Simultaneous recording of spontaneous activities and nociceptive responses from neurons in the pars compacta of substantia nigra and in the lateral habenula. Eur J Neurosci 1996, 8:1474-1478.
29. Ji H., Shepard P.D. Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA(A) receptor-mediated mechanism. J Neurosci 2007, 27:6923-6930.
30. Matsumoto M., Hikosaka O. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 2007, 447:1111-1115.
31. Shumake J., Ilango A., Scheich H., Wetzel W., Ohl F.W. Differential neuromodulation of acquisition and retrieval of avoidance learning by the lateral habenula and ventral tegmental area. J Neurosci 2010, 30:5876-5883.
32. Geisler S., Derst C., Veh R.W., Zahm D.S. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 2007, 27:5730-5743.
33. Brinschwitz K., Dittgen A., Madai V.I., Lommel R., Geisler S., Veh W. Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 2010, 168:463-476.
34. Chou T.C., Baxter M.G., Saper C.B. A novel afferent to dopaminergic neurons regulates fear-induced freezing. Soc Neurosci Abstr 2004, 30:783.13.
35. Jhou T.C., Gallagher M. Paramedian raphe neurons that project to midbrain dopamine neurons are activated by aversive stimuli. Soc Neurosci Abstr 2007, 33:425.5.
36. 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.
37. Jhou T.C., Geisler S., Marinelli M., Degarmo B.A., Zahm D.S. The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 2009, 513:566-596.
38. Kaufling J., Veinante P., Pawlowski S.A., Freund-Mercier M.J., Barrot M. Γ-aminobyturic acid cells with cocaine-induced ΔFosB in the ventral tegmental area innervate mesolimbic neurons. Biol Psych 2010, 67:88-92.
39. Scammell T.E., Estabrooke I.V., McCarthy M.T., Chemelli R.M., Yanagi-sawa M., Miller M.S., et al. Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 2000, 20:8620-8628.
40. Perrotti L.I., Bolanos C.A., Choi K.H., Russo S.J., Edwards S., Ulery P.G., et al. DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment. Eur J Neurosci 2005, 21:2817-2824.
41. Geisler S., Marinelli M., Degarmo B., Becker M.L., Freiman A.J., Beales M., et al. Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacol 2008, 33:2688-2700.
42. Kaufling J., Veinante P., Pawlowski S.A., Freund-Mercier M.J., Barrot M. Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol 2009, 513:597-621.
43. Hong S., Hikosaka O. Negative reward signals from lateral habenula to dopamine neurons are mediated by a group of medial mesopontine neurons. Soc Neurosci Abstr 2009, 482:6.
44. Hong S., Jhou T.C., Smith M.K., Saleem K.S., Hikosaka O. Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci 2011, 11457-11471.
45. Lecca S., Melis M., Luchicchi A., Ennas M.G., Castelli M.P., Muntoni A.L., et al. Effects of drugs of abuse on putative rostromedial tegmental neurons, inhibitory afferents to midbrain dopamine cells. Neuropsychopharmacol 2011, 36:589-602.
46. Kaufling J., Waltisperger E., Bourdy R., Valera A., Veinante P., Freund-Mercier M.J., et al. Pharmacological recruitment of the GABAergic tail of the ventral tegmental area by acute drug exposure. Br J Pharmacol 2010, 161:1677-1691.
47. Olson V.G., Nestler E.J. Topographical organization of GABAergic neurons within the ventral tegmental area of the rat. Synapse 2007, 61:87-95.
48. Yamaguchi T., Sheen W., Morales M. Glutamatergic neurons are present in the rat ventral tegmental area. Eur J Neurosci 2007, 25:106-118.
49. Zahm D.S., Becker M.L., Freiman A.J., Strauch S., Degarmo B., Geisler S., et al. Fos after single and repeated self-administration of cocaine and saline in the rat: emphasis on the basal forebrain and recalibration of expression. Neuropsychopharmacol 2010, 35:445-463.
50. Jhou T.C., Xu S., Ikemoto S. Self-administration of a mu-opioid agonist into the rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons and other arousal systems. Soc Neurosci Abstr 2009, 683.1.
51. Balcita-Pedicino J.J., Omelchenko N., Bell R., Sesack S.R. The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J Comp. Neurol 2010, 519:1143-1164.
52. Lavezzi H.N., Parsley K.P., Ariel M., Zahm D.S. Fos expression in a projection from the rostromedial tegmental nucleus (RMTg) to the pars dissipata of the pedunculopontine tegmental nucleus (PPTg) following administration of methamphetamine in the rat. Soc Neurosci Abstr 2010, 491.4.
53. Oakman S.A., Faris P.L., Kerr P.E., Cozzari C., Hartman B.K. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 1995, 15:5859-5869.
54. Vertes R.P. A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 1991, 313:643-668.
55. Rye D.B., Saper C.B., Lee H.J., Wainer B.H. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 1987, 259:483-528.
56. Steininger T.L., Rye D.B., Wainer B.H. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrpyramidal area in the albino rat. I. Retrograd tracing studies. J Comp Neurol 1992, 321:515-543.
57. Spann B.M., Grofova I. Nigropeduncuolopontine projection in the rat: an anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L). J Comp Neurol 1991, 311:375-388.
58. Gastard M., Jensen S.L., Martin J.R., Williams E.A., Zahm D.S. The caudal sublenticular region/anterior amygdaloid area is the only part of the rat forebrain and mesopontine tegmentum occupied by magnocellular cholinergic neurons that receives outputs from the central division of extended amygdala. Brain Res 2002, 957:207-222.
59. Aston-Jones G., Zhu Y., Card J.P. Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: possible interneuronal pool. J Neurosci 2004, 24:2313-2321.
60. Zahm D.S., Arends J.J.A., Parsley K.P., Geisler S. Projection to the mesopontine rostromedial tegmental nucleus from the lateral preoptic area. Soc Neurosci Abstr 2011, 79.09.
61. Kowski A.B., Geisler S., Krauss M., Veh R.W. Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 2008, 507:1465-1478.
62. Colussi-Mas J., Geisler S., Zimmer L., Zahm D.S., Bérod A. Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study. Eur J Neurosci 2007, 26:1011-1025.
63. Omelchenko N., Bell R., Sesack S.R. Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 2009, 30:1239-1250.
64. Charara A., Smith Y., Parent A. Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J Comp Neurol 1996, 364:254-266.
65. Clements J.R., Grant S. Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci Lett 1990, 120:70-73.
66. Jia H.-G., Yamuy J., Sampogna S., Morales F.R., Chase M.H. Colocalization of -aminobutyric acid and acetylcholine in neurons in the laterodorsal and pedunculopontine tegmental nuclei in the cat: a light and electron microscopic study. Brain Res 2003, 992:205-219.
67. Hui-Ling W., Morales M. Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic, and GABAergic neurons in the rat. Eur J Neurosci 2009, 29:340-358.
68. Alderson H.L., Faulconbridge L.F., Gregory L.P., Latimer M.P., Winn P. Behavioural sensitisation to repeated d-amphetamine: effects of excitotoxic lesions of the pedunculopontine tegmental nucleus. Neuroscience 2003, 118:311-315.
69. Nelson C.L., Wetter J.B., Milovanovic M., Wolf M.E. The laterodorsal tegmentum contributes to behavioral sensitization to amphetamine. Neuroscience 2007, 146:41-49.
70. Geisler S., Zahm D.S. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 2005, 490:270-294.
71. Robbins T.W., Granon S., Muir J.L., Durantou F., Harrison A., Everitt B.J. Neural systems underlying arousal and attention. Implications for drug abuse. Ann NY Acad Sci 1998, 846:222-237.
72. Jolas T., Nestler E.J., Aghajanian G.K. Chronic morphine increases GABA tone on serotonergic neurons of the dorsal raphe nucleus: association with an up-regulation of the cyclic AMP pathway. Neuroscience 2000, 95:433-443.
73. Shin R., Ikemoto S. The GABAB receptor agonist baclofen administered in the median and dorsal raphe nuclei is rewarding as shown by intracranial self-administration and conditioned place preference in rats. Psychopharmacol 2010, 208:545-554.
74. Nishikawa T., Scatton B. Inhibitory influence of GABA on central serotonergic transmission. Involvement of the habenulo-raphe pathways in the GABAergic inhibition of ascending cerebral serotonergic neurons. Brain Res 1985, 331:81-90.
75. Kalen P., Strecker R.E., Rosengren E., Bjorklund A. Regulation of serotonin release by the lateral habenula-dorsal raphe pathway in the rat as demonstrated by in vivo microdialysis: role of excitatory amino acids and GABA. Brain Res 1989, 492:187-202.
76. Scarnati E, Florio T, Capozzo A, Confalone G, Mazzone P. The pedunculopontine tegmental nucleus: implications for a role in modulating spinal cord motoneuron excitability. J Neural Transm 2010; [epub ahead of print] doi:10.1007/s00702-010-0532-2.
77. Jhou T.C. Neural mechanisms of freezing and passive aversive behaviors. J Comp Neurol 2005, 493:111-114.
78. Lenard L.G., Beer B. 6-Hydroxydopamine and avoidance. possible role of response suppression. Pharmacol Biochem Behav 1975, 3:873-878.
79. LeDoux J.E., Iwata J., Cicchetti P., Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 1988, 8:2517-2529.
80. Kim J.J., Rison R.A., Fanselow M.S. Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear. Behav Neurosci 1993, 107:991-997.
81. Hopkins D.A., Holstege G. Amygdaloid projections to the mesencephalon, pons, and medulla oblongata in the cat. Brain Res Rev 1978, 56:27-78.
82. Holstege G., Meiners L., Tan K. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Exp Brain Res 1985, 58:379-391.
83. Treit D., Menard J. Dissociations among the anxiolytic effects of septal, hippocampal, and amygdaloid lesions. Behav Neurosci 1997, 111:653-658.
84. Pezuk P., Aydin E., Aksoy A., Canbeyli R. Effects of BNST lesions in female rats on forced swimming and navigational learning. Brain Res 2008, 1228:199-207.
85. Sartorius A., Henn F.A. Deep brain stimulation of the lateral habenula in treatment resistant major depression. Med Hypoth 2007, 69:1305-1308.
86. Sartorius A., Kiening K.L., Kirsch P., von Gall C.C., Haberkorn U., Unterberg A.W., et al. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psych 2010, 67:e9-e11.
87. Braak H., Braak E. Pathoanatomy of Parkinson's disease. J Neurol 2000, 247:II3-II10.
88. Marui W., Iseki E., Nakai T., Miura S., Kato M., Ueda K., et al. Progression and staging of Lewy pathology in brains from patients with dementia with Lewy bodies. J Neurol Sci 2002, 195:153-159.
89. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Seur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003, 24:197-211.
90. Beach T.G., Adler C.H., Lue L., Sue L.I., Bachalakuri J., Henry-Watson J., et al. Unified staging system for Lewy body disorders: correlation with nigrostriatal degeneration, cognitive impairment and motor dysfunction. Acta Neuropathol 2009, 117:613-634.
91. Mayeux R., Smith M., Goetz C. Does a long preclinical period occur in Parkinson's disease?. Neurology 1991, 41(Suppl 1):8-13.
92. Koller W.C., Langston J.W., Hubble J.P., Irwin I., Zack M., Golbe L., et al. Does a long preclinical period occur in Parkinson's disease?. Neurology 1991, 41(Suppl 1):8-13.
93. Lang A.E., Lozano A.M. Parkinson' Disease. First of two parts. New Eng J Med 1998, 339:1044-1053.
94. Ahlskog J.E. Dopamine and Parkinson disease. Neurol 2007, 69:1701-1711.
95. Savica R., Rocca W.A., Ahlskog J.E. When does parkinsonism start?. Arch Neurol 2010, 67:798-801.
96. Chaudhuri K.R. The debate of motor versus non-motor aspects of Parkinson's disease: time for marriage. Basal Ganglia 2011, 1:47-48.
97. Wise R.A., Yokel R.A., DeWit H. Both positive reinforcement and conditioned aversion from amphetamine and from apo- morphine in rats. Science 1976, 191:1273-1275.
98. Koob G.F., Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacol 2001, 24:97-129.
99. Simpson G.R., Riley A.L. Morphine preexposure facilitates morphine place preference and attenuates morphine taste aversion. Pharmacol Biochem Behav 2005, 80:471-479.
100. Hutchison M.A., Riley A.L. Adolescent exposure to nicotine alters the aversive effects of cocaine in adult rats. Neurotoxicol Teratol 2008, 30:404-411.