Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area

Journal of Comparative Neurology

Volumn 483, Issue 2, 2005, Pages 217-235

  Omelchenico, Natalia ^a   Sesack, Susan R ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; GABA; Mesopontine tegmentum; Nucleus accumbens; Prefrontal cortex

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE;

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; MALE; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; TEGMENTUM; VENTRAL TEGMENTUM;

ACETYLCHOLINE; ANIMALS; BIOTIN; CHOLINERGIC FIBERS; DEXTRANS; DOPAMINE; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURAL PATHWAYS; PONS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; STILBAMIDINES; SYNAPTIC TRANSMISSION; TEGMENTUM MESENCEPHALI; VENTRAL TEGMENTAL AREA;

EID: 13244287714     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20417     Document Type: Article

References (97)

1. Alderson HL, Latimer MP, Blaha CD, Phillips AG, Winn P. 2004. An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience 125:349-358.
2. Aston-Jones G, Zhu Y, Card JP. 2004. Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: possible interneuronal pool. J Neurosci 24:2313-2321.
3. Bayer VE, Pickel VM. 1990. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and neuronal associations. J Neurosci 10:2996-3013.
4. Bechara A, van der Kooy D. 1989. The tegmental pedunculopontine nucleus: a brain-stem output of the limbic system critical for the conditioned place preferences produced by morphine and amphetamine. J Neurosci 9:3400-3409.
5. Berridge KC, Robinson TE. 1998. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-306.
6. Bevan MD, Bolam JP. 1995. Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 15:7105-7120.
7. Blaha CD, Allen LF, Das S, Inglis WL, Latimer MP, Vincent SR, Winn P. 1996. Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats. J Neurosci 16:714-722.
8. Brozoski T, Brown R, Rosvold H, Goldman P. 1979. Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 205:929-932.
9. Carlin R. 1980. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86:831-843.
10. Carr DB, Sesack SR. 2000a. GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38:114-123.
11. Carr DB, Sesack SR. 200Ob. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20: 3864-3873.
12. Charara A, Smith Y, Parent A. 1996. 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 364:254-266.
13. Chergui K, Charlety PJ, Akaoka H, Saunier CF, Brunet J-L, Svensson TH, Chouvet G. 1993. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 5:137-144.
14. Chergui K, Suaud-Chaguy MF, Gonon F. 1994. Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain in vivo. Neuroscience 62:641-645.
15. Clarke NP, Bevan MD, Cozzari C, Hartman B, Bolam JP. 1997. Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and eubthalamic nucleus of the rat. Neuroscience 81: 371-385.
16. Clements JR, Toth DD, Highfield DA, Grant SJ. 1991. Glutamate-like immunoreactivity is present within cholinergic neurons of the laterodorsal tegmental and pedunculopontine nuclei. Adv Exp Med Biol 295:127-142.
17. Cornwall J, Cooper JD, Phillipson OT. 1990. Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res Bull 25:271-284.
18. Cucchiaro JB, Uhlrich DJ, Sherman SM. 1988. Parabrachial innervation of the cat's dorsal lateral geniculate nucleus: an electron microscopic study using the tracer Phaseolus vulgaris leucoagglutinin (PHA-L). J Neurosci 8:4576-4588.
19. Dani JA, Ji D, Zhou FM. 2001. Synaptic plasticity and nicotine addiction. Neuron 31:349-352.
20. Datta S, Siwek DF. 2002. Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J Neurosci Res 70:611-621.
21. el Mansari M, Sakai K, Jouvet M. 1989. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76:519-529.
22. Erhardt S, Mathe JM, Chergui K, Engberg G, Svensson TH. 2002. GABA(B) receptor-mediated modulation of the firing pattern of ventral tegmental area dopamine neurons in vivo. Naunyn Schmied Arch Pharmacol 365:173-180.
23. Ford B, Holmes CJ, Mainville L, Jones BE. 1995. GABAergic neurons in the rat pontomesencephalic tegmentum: codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J Comp Neurol 363:177-196.
24. Forster GL, Blaha CD. 2000. Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur J Neurosci 12:3596-3604.
25. Garzon M, Pickel VM. 2000. Dendritic and axonal targeting of the vesicular acetylcholine transporter to membranous cytoplasmic organelles in laterodorsal and pedunculopontine tegmental nuclei. J Comp Neurol 419:32-48.
26. Garzon M, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. 1999. Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J Comp Neurol 410:197-210.
27. Grace AA, Onn S. 1989. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9:3463-3481.
28. Gray EG. 1959. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420-433.
29. Hallanger AE, Wainer BH. 1988. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 274:483-515.
30. Hollerman JR, Schultz W. 1998. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci 1:304-309.
31. Horner RL, Sanford LD, Annis D, Pack AI, Morrison AR. 1997. Serotonin at the laterodorsal tegmental nucleus suppresses rapid-eye-movement sleep in freely behaving rats. J Neurosci 17:7541-7552.
32. Ikemoto S, Wise RA. 2002. Rewarding effects of the cholinergic agents carbachol and neostigmine in the posterior ventral tegmental area. J Neurosci 22:9895-9904.
33. A receptor blockade in the anterior ventral tegmental area increases extracellular levels of dopamine in the nucleus accumbens of rats. J Neurochem 69:137-143.
34. Ikemoto S, Murphy JM, McBride WJ, 1997b. Self-infusion of GABA(A) antagonists directly into the ventral tegmental area and adjacent regions. Behav Neurosci 111:369-380.
35. Jia HG, Yamuy J, Sampogna S, Morales FR, Chase MH. 2003. Colocalization of gamma-aminobutyric acid and acetylcholine in neurons in the laterodorsal and pedunculopontine tegmental nuclei in the cat: a light and electron microscopic study. Brain Res 992:205-219.
36. Johnson SW, North RA. 1992. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483-488.
37. Jones BE. 1991. Paradoxical sleep and its chemical/structural substrates in the brain. Neuroscience 40:637-656.
38. Kayama Y, Ohta M, Jodo E. 1992. Firing of "possibly" cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness. Brain Res 569:210-220.
39. Koob GF. 1996. Hedonic valence, dopamine and motivation. Mol Psychiatry 1:186-189.
40. Kosaka T, Tauchi M, Dahl JL. 1988. Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 70:605-617.
41. Krettek JE, Price JL. 1977. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171: 157-192.
42. A receptors in the ventral tegmental area control bidirectional reward signalling between dopaminergic and non-dopaminergic neural motivational systems. Eur J Neurosci 13:1009-1015.
43. Lavoie B, Parent A. 1994a. Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344:232-241.
44. Lavoie B, Parent A. 1994b. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190-209.
45. Lee RS, Steffensen SC, Henriksen SJ. 2001. Discharge profiles of ventral tegmental area GABA neurons during movement, anesthesia, and the sleep-wake cycle. J Neurosci 21:1757-1766.
46. Lewis DA, Sesack SR. 1997. Dopamine systems in the primate brain. In: Bloom FE, Björklund A, Hökfelt T, editors. Handbook of chemical neuroanatomy: the primate nervous system, Part 1. Amsterdam: Elsevier, p 261-373.
47. Lokwan SJ, Overton PG, Berry MS, Clark D. 1999. Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons. Neuroscience 92:245-254.
48. Maloney KJ, Mainville L, Jones BE. 1999. Differential c-Fos expression in cholinergic, monoaminergic, and GABAergic cell groups of the pontomesencephalic tegmentum after paradoxical sleep deprivation and recovery. J Neurosci 19:3057-3072.
49. Matthews DE, Farewell VT. 1996. Fisher's test for 2x2 contigency tables. In: Using and understanding medical statistics. Basel: Karger, p 19-37.
50. Miller JD, Farber J, Gatz P, Roffwarg H, German DC. 1983. Activity of mesencephalic dopamine and non-dopamine neurons across stages of sleep and walking in the rat. Brain Res 273:133-141.
51. Miller AD, Forster GL, Metcalf KM, Blaha CD. 2002. Excitotoxic lesions of the pedunculopontine differentially mediate morphine- and d-amphetamine-evoked striatal dopamine efflux and behaviors. Neuroscience 111:351-362.
52. Nader K, van der Kooy D. 1997. Deprivation state switches the neurobiological substrates mediating opiate reward in the ventral tegmental area. J Neurosci 17:383-390.
53. Nakahara D, Ishida Y, Nakamura M, Furuno N, Nishimori T. 2001. Intracranial self-stimulation induces Fos expression in GABAergic neurons in the rat mesopontine tegmentum. Neuroscience 106:633-641.
54. Nisell M, Nomikos GG, Svensson TH. 1994. Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16:36-44.
55. Oades R, Halliday G. 1987. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res Rev 12:117-165.
56. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK. 1995. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 15:5859-5869.
57. Omelchenko NV, Sesack SR. 2002. Projections to the rat ventral tegmental area from the pedunculopontine-laterodorsal tegmentum synapse onto dopamine neurons that project to the nucleus accumbens. Soc Neurosci Abstr 28:460.464.
58. Overton P, Clark D. 1997. Burst firing in midbrain dopaminergic neurons. Brain Res Brain Res Rev 25:312-334.
59. Paladini CA, Iribe Y, Tepper JM. 1999. GABAA receptor stimulation blocks NMDA-induced bursting of dopaminergic neurons in vitro by decreasing input resistance. Brain Res 832:145-151.
60. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
61. Peters A, Palay SL, Webster H. 1991. The fine structure of the nervous system: neurons and their supporting cells. New York: Oxford.
62. Phillipson OT. 1979. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol 187:117-144.
63. Redgrave P, Prescott TJ, Gurney K. 1999. Is the short-latency dopamine response too short to signal reward error? Trends Neuosci 22:146-151.
64. Sanghera MK, Trulson ME, German DC. 1984. Electrophysiological properties of mouse dopamine neurons: in vivo and in vitro studies. Neuroscience 12:793-801.
65. B receptor agonists and antagonists. Brain Res 630:28-31.
66. Satoh K, Fibiger HC. 1986. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253:277-302.
67. Satoh K, Armstrong DM, Fibiger HC. 1983. A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry. Brain Res Bull 11:693-720.
68. Scarnati E, Campana E, Pacitti C. 1984. Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Res 304:351-361.
69. Schmued LC, Kyriakidis K, Fallon JH, Ribak CE. 1989. Neurons containing retrogradely transported Fluoro-Gold exhibit a variety of lysosomal profiles: a combined brightfield, fluorescence, and electron microscopic study. J Neurocytol 18:333-343.
70. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593-1599.
71. Semba K, Fibiger HC. 1992. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and anterograde transport and immunohistochemical study. J Comp Neurol 323: 387-410.
72. Sesack SR, Snyder CL, Lewis DA. 1995. Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J Comp Neurol 363:264-280.
73. Sesack SR, Carr DB, Omelchenko N, Pinto A. 2003. Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions. Ann N Y Acad Sci 1003:36-52.
74. Sofroniew MV, Priestly JV, Consolazione A, Eckenstein F, Cuello AC. 1985. Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res 329:213-223.
75. Somogyi P, Bolam J, Totterdell S, Smith A. 1981. Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labeled nigrostriatal neurones. Brain Res 217:245-263.
76. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ. 1998. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18:8003-8015.
77. Steffensen SC, Lee RS, Stobbs SH, Henriksen SJ. 2001. Responses of ventral tegmental area GABA neurons to brain stimulation reward. Brain Res 906:190-197.
78. Steinfels GF, Heym J, Strecker RE, Jacobs BL. 1983. Behavioral correlates of dopaminergic unit activity in freely moving cats. Brain Res 258:217-228.
79. Steriade M, McCarley RW. 1990. Brainstem control of wakefulness and sleep. New York: Plenum Press.
80. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi R. 1990a. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10:2541-2559.
81. Steriade M, Pare D, Datta S, Oakson G, Curro Dossi R. 1990b. Different cellular types in mesopontine cholinergic nuclei related to pontogeniculo- occipital waves. J Neurosci 10:2560-2579.
82. Sugita. S, Johnson SW, North RA, 1992. Synaptic inputs to GABAA and GABAB receptors originate from discrete afferent neurons. Neurosci Lett 134:207-211.
83. Sutin EL, Jacobowitz DM. 1988. Immunocytochemical localization of peptides and other neurochemicals in the rat laterodorsal tegmental nucleus and adjacent area. J Comp Neurol 270:243-270.
84. Swanson LW. 1982. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321-353.
85. Tepper JM, Martin LP, Anderson DR. 1995. GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J Neurosci 15:3092-3103.
86. Thakkar M, Portas C, McCarley RW. 1996. Chronic low-amplitude electrical stimulation of the laterodorsal tegmental nucleus of freely moving cats increases REM sleep. Brain Res 723:223-227.
87. Trulson ME, Preussler DW. 1984. Dopamine-containing ventral tegmental area neurons in freely moving cats: activity during the sleep-waking cycle and effects of stress. Exp Neurol 83:367-377.
88. Van Bockstaele EJ, Pickel VM. 1995. GABA-containing neurons in the ventral tegmental area project to nucleus accumbens in rat brain. Brain Res 682:215-221.
89. Van Bockstaele EJ, Wright AM, Cestari DM, Pickel VM. 1994. Immunolabeling of retrogradely transported Fluoro-Gold: sensitivity and application to ultrastructural analysis of transmitter-specific mesolimbic circuitry. J Neurosci Methods 55:65-78.
90. Veznedaroglu E, Milner TE. 1992. Elimination of artifactual labeling of hippocampal mossy fibers seen following pre-embedding immunogoldsilver technique by pretreatment with zinc chelator. Microsc Res Tech 23:100-101.
91. Vincent SR, Satoh K, Armstrong DM, Fibiger HC. 1983. Substance P in the ascending cholinergic reticular system. Nature 306:688-691.
92. Watanabe M, Kodama T, Hikosaka K. 1997. Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. J Neurophysiol 78:2795-2798.
93. Westerink BH, Kwint HF, deVries JB. 1996. The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 16:2605-2611.
94. Westerink BH, Enrico P, Feimann J, De Vries JB. 1998. The pharmacology of mesocortical dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and prefrontal cortex of the rat brain. J Pharmacol Exp Ther 285:143-154.
95. White FJ. 1996. Synaptic regulation of mesocorticolimbic dopamine neurons. Annu Rev Neurosci 19:405-436.
96. Winn P, Brown VJ, Inglis WL. 1997. On the relationships between the striatum and the pedunculopontine tegmental nucleus. Grit Rev Neurobiol 11:241-261.
97. Woolf NJ, Butcher LL. 1986. Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603-637.