The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: A correlative neuroanatomical and behavioral study

Neuroscience

Volumn 96, Issue 4, 2000, Pages 735-742

  Lanca A J ^a,b   Adamson, K L ^a   Coen, K M ^a   Chow, B L C ^a   Corrigall, W A ^a,b,c  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Brainstem; Drug reinforcement; Microinfusions; Neurochemical lesions; Reward

Indexed keywords

CHOLINERGIC RECEPTOR BLOCKING AGENT; DIHYDRO BETA ERYTHROIDINE; ETHYLCHOLINE MUSTARD AZIRIDINIUM; NEUROTOXIN; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NICOTINE;

ARTICLE; BRAIN STEM; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; HISTOCHEMISTRY; MALE; NISSL SUBSTANCE; NONHUMAN; PRIORITY JOURNAL; RAT; REWARD; SUBSTANTIA NIGRA; TEGMENTUM; VENTRAL TEGMENTUM;

ACETYLCHOLINE; ANIMALS; AZIRIDINES; BEHAVIOR, ANIMAL; CHOLINE; CHOLINERGIC FIBERS; DENERVATION; DIHYDRO-BETA-ERYTHROIDINE; EXCITATORY AMINO ACID AGONISTS; IBOTENIC ACID; MALE; NERVE DEGENERATION; NEUROMUSCULAR BLOCKING AGENTS; NEURONS; NEUROTOXINS; NICOTINE; NICOTINIC AGONISTS; PONS; RATS; RATS, LONG-EVANS; SELF ADMINISTRATION; TEGMENTUM MESENCEPHALI; TOBACCO USE DISORDER;

EID: 0034057786     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(99)00607-7     Document Type: Article

References (71)

1. Armstrong D.M., Saper C.B., Levey A.I., Wainer B.H., Terry R.D. Distribution of cholinergic neurons in rat brain: demonstration by the immunocytochemical localization of choline acetyltransferase. J. comp. Neurol. 216:1983;53-68.
2. Bechara A., Nader K., van der Kooy D. A two-separate-motivational-systems hypothesis of opioid addiction. Pharmac. Biochem. Behav. 59:1998;1-17.
3. Bechara A., van der Kooy D. 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. 9:1989;3400-3409.
4. Beninato M., Spencer R.F. A cholinergic projection to the rat substantia nigra from the pedunculopontine tegmental nucleus. Brain Res. 412:1987;169-174.
5. Beninato M., Spencer R.F. The cholinergic innervation of the rat substantia nigra: a light and electron microscopic immunocytochemical study. Expl Brain. Res. 72:1988;178-184.
6. Blaha C.D., Allen L.F., Das S., Inglis W.L., Latimer M.P., Vincent S.R., Winn P. 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. 16:1996;714-722.
7. Blaha C.D., Winn P. Modulation of dopamine efflux in the striatum following cholinergic stimulation of the substantia nigra in intact and pedunculopontine tegmental nucleus-lesioned rats. J. Neurosci. 13:1993;1035-1044.
8. Bolam J.P., Francis C.M., Henderson Z. Cholinergic input to dopaminergic neurons in the substantia nigra: a double immunocytochemical study. Neuroscience. 41:1991;483-494.
9. Book A.A., Wiley R.G., Schweitzer J.B. Specificity of 192 IgG-saporin for NGF receptor-positive cholinergic basal forebrain neurons in the rat. Brain Res. 590:1992;350-355.
10. Clarke P.B.S., Hommer D.W., Pert A., Skirboll L.R. Innervation of substantia nigra neurons by cholinergic afferents from the pedunculopontine nucleus in the rat: neuroanatomical and electrophysiological evidence. Neuroscience. 23:1987;1011-1019.
11. Corrigall W.A., Coen K.M., Adamson K.L. Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res. 653:1994;278-284.
12. Corrigall W.A., Coen K.M., Adamson K.L., Chow B.L.C. The mu opioid agonist DAMGO alters the intravenous self-administration of cocaine in rats: mechanisms in the ventral tegmental area. Psychopharmacology. 141:1999;428-435.
13. Corrigall W.A., Coen K.M., Adamson K.L., Chow B.L.C. Manipulations of mu-opioid and nicotinic cholinergic receptors in the pontine tegmental region alter cocaine self-administration. Psychopharmacology. 145:1999;412-417.
14. Corrigall W.A., Franklin K.B.J., Coen K.M., Clarke P.B.S. The mesolimbic dopaminergic system is implicated in the reinforcing effects of nicotine. Psychopharmacology. 107:1992;285-289.
15. Cuello A. C., Garofalo L., Kenigsberg R. L., Maysinger D., Pioro E. P. and Ribeiro-da-Silva A. (1990) Degeneration and regeneration of basal forebrain cholinergic neurons. In Trophic Factors in the Nervous System (eds Horrocks L. A., Neff N. H., Yates A. J. and Hadjiconstantinou M.), pp. 307-326. Raven, New York.
16. Dunbar J.S., Hitchcock K., Latimer M., Rugg E.L., Ward N., Winn P. Excitotoxin lesions of the pedunculopontine tegmental nucleus of the rat. II. Examination of eating and drinking, rotation, and reaching and grasping following unilateral ibotenate or quinolinate lesion. Brain Res. 589:1992;194-206.
17. Fisher A., Mantione C.R., Abraham D.J., Hanin I. Long-term central cholinergic hypofunction induced in mice by ethylcholine aziridinium ion (AF64A) in vivo. J. Pharmac. exp. Ther. 222:1982;140-145.
18. Goldsmith M., van der Kooy D. Separate non-cholinergic descending and cholinergic ascending projections from the nucleus tegmenti pedunculopontinus. Brain Res. 445:1988;364-386.
19. Gould E., Woolf N.J., Butcher L.L. Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. J. comp. Neurol. 287:1989;495-514.
20. Hallanger A.E., Levey A.I., Lee H.J., Rye D.B., Wainer B.H. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. comp. Neurol. 262:1987;105-124.
21. Hallanger A.E., Wainer B.H. Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J. comp. Neurol. 274:1988;483-515.
22. Hanin I. (1990) AF64A-induced cholinergic hypofunction. In Progress in Brain Research: Cholinergic Neurotransmission: Functional and Clinical Aspects (eds Aquilonius S.-M. and Gillberg P.-G.), pp. 289-300. Elsevier, Amsterdam.
23. Hefti F., Hartikka J., Junard E. O. and Knusel B. (1990) Development of cholinergic neurons in septum, nucleus basalis, striatum and pons in culture and their response to nerve growth factor. In Trophic Factors in the Nervous System (eds Horrocks L. A., Neff N. H., Yates A. J. and Hadjiconstantinou M.), pp. 327-337. Raven, New York.
24. Honda T., Semba K. Serotonergic synaptic input to cholinergic neurons in the rat mesopontine tegmentum. Brain Res. 647:1994;299-306.
25. Hope B.T., Maicael G.J., Knigge K.M., Vincent S.R. Neuronal NADPH diaphorase is a nitric oxide synthase. Proc. natn. Acad. Sci. U.S.A. 88:1991;2811-2814.
26. Hortnagl H., Potter P.E., Hanin I. Effect of cholinergic deficit induced by ethylcholine aziridinium (AF64A) on noradrenergic and dopaminergic parameters in rat brain. Brain Res. 421:1987;75-84.
27. Hortnagl H., Potter P.E., Hanin I. Effect of cholinergic deficit induced by ethylcholine aziridinium (AF64A) on serotonergic parameters in rat brain. Neuroscience. 22:1987;203-213.
28. Inglis W.L., Allen L.F., Whitelaw R.B., Latimer M.P., Brace H.M., Winn P. An investigation into the role of the pedunculopontine tegmental nucleus in the mediation of locomotion and orofacial stereotypy induced by d-amphetamine and apomorphine in the rat. Neuroscience. 58:1994;817-833.
29. Keating G.L., Blaha C.D., Winn P., DiCiano P., Latimer M.P., Phillips A.G. Amphetamine self-administration is enhanced by excitotoxin lesions of the pedunculopontine tegmental nucleus in rats. Soc. Neurosci. Abstr. 23:1997;2145.
30. Kofman O., McGlynn S.M., Olmstead M.C., Yeomans J.S. Differential effects of atropine, procaine and dopamine in the rat ventral tegmentum on lateral hypothalamic rewarding brain stimulation. Behav. Brain Res. 38:1990;55-68.
31. Kofman O., Yeomans J.S. Cholinergic antagonists in ventral tegmentum elevate thresholds for lateral hypothalamic and brainstem self-stimulation. Pharmac. Biochem. Behav. 31:1989;547-559.
32. Lança A.J. Reduction of voluntary alcohol intake in the rat by modulation of the dopaminergic mesolimbic system: transplantation of ventral mesencephalic cell suspensions. Neuroscience. 58:1994;359-369.
33. Lança A.J., De Cabo C., Arifuzzaman A.I., Vaccarino F.J. Cholecystokinergic innervation of the nucleus accumbens subregions. Peptides. 19:1998;859-868.
34. 8-vasopressin. Neuroscience. 91:1999;1331-1341.
35. Lavoie B., Parent A. 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. 344:1994;190-209.
36. Leanza G., Nilsson O.G., Wiley R.G., Bjorklund A. Selective lesioning of the basal forebrain cholinergic system by intraventricular 192 IgG-saporin: behavioural, biochemical and stereological studies in the rat. Eur. J. Neurosci. 7:1995;329-343.
37. Levy A., Kant G.J., Meyerhoff J.L., Jarrard L.E. Non-cholinergic neurotoxic effects of AF64A in the substantia nigra. Brain Res. 305:1984;169-172.
38. Mantione C.R., Zigmond M.J., Fisher A., Hanin I. Selective presynaptic cholinergic neurotoxicity following intrahippocampal AF64A injection in rats. J. Neurochem. 41:1983;251-255.
39. Nader K., Bechara A., Roberts D.C.S., van der Kooy D. Neuroleptics block high- but not low-dose heroin place preferences: further evidence for a two-system model of motivation. Behav. Neurosci. 108:1994;1128-1138.
40. 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. 15:1995;5859-5869.
41. Olmstead M.C., Franklin K.B.J. Effects of pedunculopontine tegmental nucleus lesions on morphine-induced conditioned place preference and analgesia in the formalin test. Neuroscience. 57:1993;411-418.
42. Olmstead M.C., Franklin K.B.J. Lesions of the pedunculopontine tegmental nucleus block drug-induced reinforcement but not amphetamine-induced locomotion. Brain Res. 638:1994;29-35.
43. Olmstead M.C., Franklin K.B.J. Lesions of the pedunculopontine tegmental nucleus abolish catalepsy and locomotor depression induced by morphine. Brain Res. 662:1994;134-140.
44. Olmstead M.C., Munn E.M., Franklin K.B.J., Wise R. Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J. Neurosci. 18:1998;5035-5044.
45. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic, New York.
46. Reiner P.B., Vincent S.R. Topographic relations of cholinergic and noradrenergic neurons in the feline pontomesencephalic tegmentum: an immunocytochemical study. Brain Res. Bull. 19:1987;705-714.
47. Rodríguez M., Mantolán-Sarmiento B., González-Hernández T. Effects of ethylcholine mustard aziridinium ion (AF64A) on the choline acetyltransferase and nitric oxide synthase activities in the mesopontine cholinergic neurons of the rat. Neuroscience. 82:1998;856-866.
48. Rye D.B., Saper C.B., Lee H.J., Wainer B. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J. comp. Neurol. 259:1987;483-528.
49. Sandberg K., Hanin I., Fisher A., Coyle J.T. Selective cholinergic neurotoxin: AF64A effects in rat striatum. Brain Res. 293:1984;49-55.
50. Sandberg K., Schnaar R.L., McKinney M., Hanin I., Fisher A. AF64A: an active site directed irreversible inhibitor of choline acetyltransferase. J. Neurochem. 44:1985;439-445.
51. Saxena S., Hartman B.K. Topographical organization of the cholinergic cells projecting from the laterodorsal tegmental (LDTg) and pedunculopontine (PPTg) nuclei to the thalamus in rat brain. Soc. Neurosci. Abstr. 15:1989;229.
52. Scherer-Singler U., Vincent S.R., Kimura H., McGeer E.G. Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J. Neurosci. Meth. 9:1983;229-234.
53. Spann B.M., Grofova I. Nigropedunculopontine projection in the rat: an anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L). J. comp. Neurol. 311:1991;375-388.
54. Spann B.M., Grofova I. Cholinergic and non-cholinergic neurons in the rat pedunculopontine tegmental nucleus. Anat. Embryol. 186:1992;215-227.
55. Sugimoto T., Hattori T. Organization of efferent projections of nucleus tegmenti pedunculopontinus pars compacta with special reference to its cholinergic aspects. Neuroscience. 11:1984;931-946.
56. Sugimoto T., Mizukawa K., Hattori T., Konishi A., Kaneko T., Mizuno N. Cholinergic neurons in the nucleus tegmenti pedunculopontinus pars compacta and the caudoputamen of the rat: a light and electron microscope immunohistochemical study using a monoclonal antibody to choline acetyltransferase. Neurosci. Lett. 51:1984;113-117.
57. Suter U., Drinkwater C. C., Heymach J. V., Lindsay R. M. and Shooter E. M. (1992) Investigations on the structure-function relationship of neurotrophins. In Neurotrophic Factors (eds Tsukada Y. and Shooter E.), pp. 27-34. CRC, Boca Raton.
58. Vincent S.R., Satoh K., Armstrong D.M., Fibiger H.C. NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci. Lett. 43:1983;31-36.
59. Vincent S.R., Satoh K., Armstrong D.M., Panula P., Vales W., Fibiger H.C. Neuropeptides and NADPH-diaphorase activity in the ascending cholinergic reticular system of the rat. Neuroscience. 17:1986;167-182.
60. Walsh T. J. and Potter P. E. (1998) Selective cholinergic neurotoxins: AF64A and 192-IgG-saporin. In Highly Selective Neurotoxins: Basic and Clinical Applications (ed. Kostrzewa R. M.), pp. 313-327. Humana, Totawa.
61. Watkins S.S., Epping-Jordan M.P., Koob G.F., Markou A. Blockade of nicotine self-administration with nicotinic antagonists in rats. Pharmac. Biochem. Behav. 62:1999;743-751.
62. Wenk G.L., Stoehr J.D., Quintana G., Mobley S., Wiley R.G. Behavioral, biochemical, histological, and electrophysiological effects of 192 IgG-saporin injections into the basal forebrain of rats. J. Neurosci. 14:1994;5986-5995.
63. Wiley R.G., Oeltmann T.N., Lappi D.A. Immunolesioning: selective destruction of neurons using immunotoxin for rat NGF receptor. Brain Res. 562:1991;149-153.
64. Winn P., Brown V.J., Inglis W.L. On the relationships between the striatum and the pedunculopontine tegmental nucleus. Crit. Rev. Neurobiol. 11:1997;241-261.
65. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: II. Projections to the interpeduncular nucleus. Brain Res. Bull. 14:1986;63-83.
66. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res. Bull. 16:1986;603-637.
67. Woolf N.J., Butcher L.L. Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum. Brain Res. Bull. 23:1989;519-540.
68. Yeomans J.S. Role of tegmental cholinergic neurons in dopaminergic activation, antimuscarinic psychosis and schizophrenia. Neuropsychopharmacology. 12:1995;3-16.
69. Yeomans J., Baptista M. Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward. Pharmac. Biochem. Behav. 57:1997;915-921.
70. Yeomans J.S., Kofman O., McFarlane V. Cholinergic involvement in lateral hypothalamic rewarding brain stimulation. Brain Res. 329:1985;19-26.
71. Yeomans J.S., Mathur A., Tampakeras M. Rewarding brain stimulation: role of tegmental cholinergic neurons that activate dopamine neurons. Behav. Neurosci. 107:1993;1077-1087.