Ultrastructural localization of high-affinity choline transporter in the rat anteroventral thalamus and ventral tegmental area: Differences in axon morphology and transporter distribution

Journal of Comparative Neurology

Volumn 518, Issue 11, 2010, Pages 1908-1924

  Holmstrand, Ericka C ^a   Asafu Adjei, Josephine ^c   Sampson, Allan R ^c   Blakely, Randy D ^a   Sesack, Susan R ^a,b  

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

^b UNIVERSITY OF PITTSBURGH   (United States)

^c VANDERBILT UNIVERSITY   (United States)

Author keywords

Acetylcholine; Dopamine; Limbic; Pedunculopontine tegmentum

Indexed keywords

CARRIER PROTEIN; CHOLINE TRANSPORTER; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; MALE; NERVE CELL MEMBRANE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SYNAPSE VESICLE; SYNAPTOGENESIS; THALAMUS; VENTRAL TEGMENTUM;

ANIMALS; AXONS; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE TRANSPORT PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; THALAMUS; VENTRAL TEGMENTAL AREA;

EID: 77952210780     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22310     Document Type: Article

References (109)

1. Alkondon M, Albuquerque EX. 2006. Subtype-specific inhibition of nicotinic acetylcholine receptors by choline: a regulatory pathway. J Pharmacol Exp Ther 318:268-275. (Pubitemid 43920765)
2. Alkondon M, Pereira EFR, Cortes WS, Maelicke A, Albuquerque EX. 1997. Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734-2742. (Pubitemid 28082962)
3. Antonelli T, Beani L, Bianchi C, Pedata F, Pepeu G. 1981. Changes in synaptosomal high affinity choline uptake following electrical stimulation of guinea-pig cortical slices: effect of atropine and physostigmine. Br J Pharmacol 74: 525-531. (Pubitemid 12239819)
4. Apparsundaram S, Martinez V, Parikh V, Kozak R, Sarter M. 2005. Increased capacity and density of choline transporters situated in synaptic membranes of the right medial prefrontal cortex of attentional task-performing rats. J Neurosci 25:3851-3856. (Pubitemid 40570418)
5. Baude A, Nusser Z, Moinár E, Mcllhinney RA, Somogyi P. 1995. High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and nonsynaptic sites in rat hippocampus. Neuroscience 69: 1031-1055.
6. Bazalakova MH, Wright J, Schneble EJ, McDonald MP, Heilman CJ, Levey Al, Blakely RD. 2007. Deficits in acetylcholine homeostasis, receptors and behaviors in choline transporter heterozygous mice. Genes Brain Behav 6:411-424. (Pubitemid 47024956)
7. Beaudet A, Sotelo C. 1981. Synaptic remodeling of serotonin axon terminals in rat agranular cerebellum. Brain Res 206: 305-329. (Pubitemid 11170214)
8. Beckstead RM, Domesick VB, Nauta WJH. 1979. Efferent connections of the substantia nigra and ventral tegmental area in the rat Brain Res 175:191-217.
9. Bentivoglio M, Kultas-IIinsky K, IIinsky I. 1993. Limbic thalamus: structure, intrinsic organization, and connections. In: Vogt BA, Gabriel M, editors. Neurobiology of cingulate cortex and limbic Thalamus. Boston: Birkhauser. p 71-122.
10. Bernard V, Somogyi P, Bolam JP. 1997. Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat J Neurosci 17:819-833.
11. Bolton RF, Cornwall J, Phillipson OT. 1993. Collateral axons of cholinergic pontine neurones projecting to midline, mediodorsal and parafascicular thalamic nuclei in the rat. J Chem Neuroanat 6:101-114. (Pubitemid 23128947)
12. Breer H, Knipper M. 1990. Regulation of high affinity choline uptake. J Neurobiol 21:269-275. (Pubitemid 20108081)
13. Corrigall WA, Coen KM, Zhang J, Adamson LK. 2002. Pharmacological manipulations of the pedunculopontine tegmental nucleus in the rat reduce self-administration of both nicotine and cocaine. Psychopharmacology (Berl) 160: 198-205. (Pubitemid 34212246)
14. Crawley JN, Olschowka JA, Diz DI, Jacobowitz DM. 1985. Behavioral significance of the coexistence of substance P, corticotropin releasing factor, and acetylcholinesterase in lateral dorsal tegmental neurons projecting to the medial frontal cortex of the rat. Peptides 6:891-901.
15. Datta S, Siwek DF. 2002. Single cell activity patterns of pedunculopontine tegmentum neurons across the sleepwake cycle in the freely moving rats. J Neurosci Res 70: 611-621. (Pubitemid 35253531)
16. Descarries L, Gisiger V, Steriade M. 1997. Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53: 603-625.
17. Eiden LE. 1998. The cholinergic gene locus. J Neurochem 70: 2227-2240.
18. Erickson JD, Varoqui H, Schäfer M, Modi W, Diebler MF, Weihe E, Rand J, Eiden LE, Bonner TI, Usdin T. 1994. Functional characterization of the mammalian vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J Biol Chem 269:21929-21932.
19. Ferguson SM, Blakely RD. 2004. The choline transporter resurfaces: new roles for synaptic vesicles? Mol Interv 4: 22-37.
20. Ferguson SM, Savchenko V, Apparsundaram S, Zwick M, Wright J, Heilman C-J, Yi H, Levey AI, Blakely RD. 2003. Vesicular localization and activity-dependent trafficking of presynaptic choline transportera J Neurosci 23:9697-9709.
21. Ferguson SM, Bazalakova M, Savchenko V, Tapia JC, Wright J, Blakely RD. 2004. Lethal impairment of cholinergic neurotransmission in hemicholinium-3- sensitive choline transporter knockout mice. Proc Natl Acad Sci U S A 101: 8762-8767. (Pubitemid 38745845)
22. Gabriel M, Foster K, Orona E. 1980. Interaction of laminae of the cingulate cortex with the anteroventral thalamus during behavioral learning. Science 208:1050-1052. (Pubitemid 10052432)
23. Garzón 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. (Pubitemid 29323072)
24. Gates J Jr, Ferguson SM, Blakely RD, Apparsundaram S. 2004. Regulation of choline transporter surface expression and phosphorylation by protein kinase C and protein phosphatase 1/2A. J Pharmacol Exp Ther 310:536-545. (Pubitemid 38988897)
25. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490:270-294. (Pubitemid 41140993)
26. Gonzalo-Ruiz A, Sanz-Anquela MJ, Lieberman AR. 1995. Cholinergic projections to the anterior thalamic nuclei in the rat a combined retrograde tracing and choline acetyl transferase immunohistochemical study. Anat Embryol 192:335-349.
27. Gould E, Woolf NJ, Butcher LL. 1989. Cholinergic projections to the substantia nigra from the pedunculopontine and laterodorsal tegmental nuclei. Neuroscience 28:611-623. (Pubitemid 19081019)
28. Grant SJ, Highfield DA. 1991. Extracellular characteristics of putative cholinergic neurons in the rat laterodorsal tegmental nucleus. Brain Res 559:64-74.
29. Grove EA. 1988. Efferent connections of the substantia innominata in the rat J Comp Neurol 277:347-364.
30. Guseva MV, Hopkins DM, Pauly JR. 2006. An autoradiographic analysis of rat brain nicotinic receptor plasticity following dietary choline modification. Pharmacol Biochem Behav 84:26-34.
31. 3H]choline uptake in rat striatal synaptosomes. Brain Res 62: 523-529.
32. Haga T, Noda H. 1973. Choline uptake systems of rat brain synaptosomes. Biochim Biophys Acta 291:564-575.
33. 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.
34. Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH. 1987. The origins of cholinergic and other subcortical afferents to the thalamus in the rat J Comp Neurol 262:105-124.
35. Hallanger AE, Price SD, Lee HJ, Steininger TL, Wainer BH. 1990. Ultrastructure of cholinergic synaptic terminals in the thalamic anteroventral, ventroposterior, and dorsal lateral geniculate nuclei of the rat J Comp Neurol 299: 482-492.
36. Heckers S, Geula C, Mesulam MM. 1992. Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325:68-82.
37. Holmstrand EC, Sesack SR, Blakely RD. 2006. Ultrastructural characterization of the expression of the high-affinity choline transporter in the rat ventral tegmental area. Soc Neurosci Abstr 728.6.
38. Holmstrand EC, Sesack SR, Blakely RD. 2008. High affinity choline transporter in the rat ventral tegmental area and anteroventral thalamus: colocalization with the vesicular acetylcholine transporter and subcellular distribution to the plasma membrane. Soc Neurosci Abstr 129.2.
39. Ikemoto S, Panksepp J. 1996. Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav Neurosci 110:331-345. (Pubitemid 26125078)
40. 3H]choline into the forebrain of the rat. Exp Brain Res 65:437-448.
41. Jones IW, Wonnacott S. 2004. Precise localization of α.7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci 24: 11244-11252.
42. Jourdain A, Semba K, Fibiger HC. 1989. Basal forebrain and mesopontine tegmental projections to the reticular thalamic nucleus: an axonal collateralization and immunohistochemical study in the rat. Brain Res 505:55-65. (Pubitemid 20011110)
43. Kobayashi Y, Isa T. 2002. Sensory-motor gating and cognitive control by the brainstem cholinergic system. Neural Netw 15:731-741. (Pubitemid 34947471)
44. Koyama Y, Jodo E, Kayama Y. 1994. Sensory responsiveness of "broad-spike" neurons in the laterodorsal tegmental nucleus, locus coeruleus and dorsal raphe of awake rats: implications for cholinergic and monoaminergic neuronspecific responses. Neuroscience 63:1021-1031.
45. Kus L, Borys E, Ping Chu Y, Ferguson SM, Blakely RD, Emborg ME, Kordower JH, Levey Al, Mufson EJ. 2003. Distribution of high affinity choline transporter immunoreactivity in the primate central nervous system. J Comp Neurol 463: 341-357. (Pubitemid 36842400)
46. Lança AJ, Adamson KL, Coen KM, Chow BL, Corrigall WA. 2000. The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: a correlative neuroanatomical and behavioral study. Neuroscience 96:735-742.
47. Laviolette SR, van der Kooy D. 2003. The motivational valence of nicotine in the rat ventral tegmental area is switched from rewarding to aversive following blockade of the αα7subunit-containing nicotinic acetylcholine receptor. Psychopharmacology (Berl) 166:306-313.
48. Lecomte MJ, De Gois S, Guerci A, Ravassard P, Faucon-Biguet N, Mallet J, Berrard S. 2005. Differential expression and regulation of the high-affinity choline transporter CHT1 and choline acetyltransferase in neurons of superior cervical ganglia. Mol Cell Neurosci 28:303-313. (Pubitemid 40202591)
49. Levey AI, Hallanger AE, Wainer BH. 1987. Choline acetyltransferase immunoreactivity in the rat thalamus. J Comp Neurol 257:317-332.
50. Lisman JE, Harris KM. 1993. Quantal analysis and synaptic anatomy-integrating two views of hippocampal plasticity. Trends Neurosci 16:141-147. (Pubitemid 23085470)
51. Littell RC, Nilliken GA, Stroup WW, Wolfinger RD, Schabenberger O. 2006. SAS for mixed models. Cary, NC: SAS Institute, Inc.
52. Löffelholz K, Klein J. 2006. Precursors: choline and glucose. In: Giacobini E, Pepeu G, editors. The brain cholinergic system in health and disease. Boca Raton, FL: Informa Healthcare, p 75-84.
53. Losier BJ, Semba K. 1993. Dual projections of single cholinergic and aminergic brainstem neurons to the thalamus and basal forebrain in the rat. Brain Res 604:41-52. (Pubitemid 23080096)
54. Mathiisen TM, Nagelhus EA, Jouleh B, Torp R, Frydenlund DS, Mylonakou M-N, Amiry-Moghaddam M, Covolan L, Utvik JK, Riber B, Gujord KM, Knutsen J, Skare Ø, Laake P, Davanger S, Haug F-M, Rinvik E, Ottersen OP. 2005. Postembedding immunogold cytochemistry of membrane molecules and amino acid transmitters in the central nervous system. In: Zaborszky L, Wouterlood FG, Lanciego JL, editors. Neuroanatomical tract-tracing 3: molecules, neurons, and systems. New York: Springer, p 72-108.
55. Mike A, Castro NG, Albuquerque EX. 2000. Choline and acetylcholine have similar kinetic properties of activation and desensitization on the α7 nicotinic receptors in rat hippocampal neurons. Brain Res 882:155-168.
56. Misawa H, Nakata K, Matsuura J, Nagao M, Okuda T, Haga T. 2001. Distribution of the high-affinity choline transporter in the central nervous system of the rat. Neuroscience 105: 87-98. (Pubitemid 32722096)
57. Murrin LC, Kuhar MJ. 1976. Activation of high-affinity choline uptake in vitro by depolarizing agents. Mol Pharmacol 12: 1082-1090.
58. Nakata K, Okuda T, Misawa H. 2004. Ultrastructural localization of high-affinity choline transporter in the rat neuromuscular junction: enrichment on synaptic vesicles. Synapse 53:53-56. (Pubitemid 38703005)
59. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman B. 1995. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 15: 5859-5869.
60. Oakman SA, Faris PL, Cozzari C, Hartman BK. 1999. Characterization of the extent of pontomesencephalic cholinergic neurons projections to the thalamus: comparison with projections to midbrain dopaminergic groups. Neuroscience 94:529-547. (Pubitemid 29436079)
61. Oda S, Kuroda M, Kakuta S, Tanihata S, Ishikawa Y, Kishi K. 2003. Ultrastructure of ascending cholinergic terminals in the anteroventral thalamic nucleus of the rat: a comparison with the mammillothalamic terminals. Brain Res Bull 59:473-483. (Pubitemid 36173603)
62. Okuda T, Haga T. 2003. High-affinity choline transporter. Neurochem Res 28:483-488.
63. Omelchenko N, Sesack SR. 2005. Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 483:217-235.
64. Omelchenko N, Sesack SR. 2006. Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol 494:863-875. (Pubitemid 43063984)
65. Oshima S, Yamada K, Shirakawa T, Watanabe M. 2004. Changes of high-affinity choline transporter CHT1 mRNA expression during degeneration and regeneration of hypoglossal nerves in mice. Neurosci Lett 365:97-101. (Pubitemid 38881632)
66. Pan WX, Hyland BI. 2005. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J Neurosci 25:4725-4732.
67. Parent A, Paré D, Smith Y, Steriade M. 1988. Basai forebrain cholinergic and noncholinergic projections to the thalamus and brainstem in cats and monkeys. J Comp Neurol 277: 281-301. (Pubitemid 19002136)
68. Parent M, Descarries L. 2008. Acetylcholine innervation of the adult rat thalamus: distribution and ultrastructural features in dorsolateral geniculate, parafascicular, and reticular thalamic nuclei. J Comp Neurol 511:678-691.
69. Parikh V, Apparsundaram S, Kozak R, Richards JB, Sarter M. 2006. Reduced expression and capacity of the striatal high-affinity choline transporter in hyperdopaminergic mice. Neuroscience 141:379-389.
70. Pidoplichko VI, Noguchi J, Areola OO, Liang Y, Peterson J, Zhang T, Dani JA. 2004. Nicotinic cholinergic synaptic mechanisms in the ventral tegmental area contribute to nicotine addiction. Learn Mem 11:60-69. (Pubitemid 38167059)
71. Pierce JP, Lewin GR. 1994. An ultrastructural size principle. Neuroscience 58:441-446.
72. 125I]α-bungarotoxin binding in rat brain after chronic nicotine exposure. Neurosci Lett 404:9-14.
73. Redgrave P, Gurney K, Reynolds J. 2008. What is reinforced by phasic dopamine signals? Brain Res Rev 58:322-339.
74. Ribeiro FM, Alves-Silva J, Volknandt W, Martins-Silva C, Mahmud H, Wilhelm A, Gomez MV, Rylett RJ, Ferguson SS, Prado VF, Prado MA. 2003. The hemicholinium-3 sensitive high affinity choline transporter is internalized by clathrinmediated endocytosis and is present in endosomes and synaptic vesicles. J Neurochem 87:136-146. (Pubitemid 37210648)
75. Roskoski R Jr. 1978. Acceleration of choline uptake after depolarization-induced acetylcholine release in rat cortical synaptosomes. J Neurochem 30:1357-1361.
76. Satoh K, Fibiger HC. 1986. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253:277-302. (Pubitemid 17181056)
77. Schilström B, Fagerquist MV, Zhang X, Hertel P, Panagis G, Nomikos GG, Svensson TH. 2000. Putative role of presynaptic α7* nicotinic receptors in nicotine stimulated increases of extracellular levels of glutamate and aspartate in the ventral tegmental area. Synapse 38:375-383.
78. Schultz W. 2007. Behavioral dopamine signals. Trends Neurosci 30:203-210.
79. Semba K, Reiner PB, Fibiger HC. 1990. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38:643-654. (Pubitemid 20383201)
80. Shibata H. 1992. Topographic organization of subcortical projections to the anterior thalamic nuclei in the rat. J Comp Neurol 323:117-127.
81. Sikes RW, Vogt BA. 1987. Afferent connections of anterior thalamus in rats: sources and association with muscarinic acetylcholine receptors. J Comp Neurol 256:538-551.
82. 3H] leucine and horseradish peroxidase. Brain Res 178:17-40.
83. Simon JR, Kuhar MJ. 1975. Impulse-flow regulation of high affinity-choline uptake in brain cholinergic terminals. Nature 255:162-163.
84. Simon JR, Atweh S, Kuhar MJ. 1976. Sodium-dependent high affinity choline uptake: a regulatory step in the synthesis of acetylcholine. J Neurochem 26:909-922.
85. Slotkin TA, Seidler FJ, Crain BJ, Bell JM, Bisette G, Nemeroff CB. 1990. Regulatory changes in presynaptic cholinergic function assessed in rapid autopsy material from patients with Alzheimer disease: implications for etiology and therapy. Proc Natl Acad Sci U S A 87:2452-2455. (Pubitemid 20141756)
86. Slotkin TA, Nemeroff CB, Bisette G, Seidler FJ. 1994. Overexpression of the high affinity choline transporter in cortical regions affected by Alzheimer's disease. Evidence from rapid autopsy studies. J Clin Invest 94:696-702. (Pubitemid 24978977)
87. Small SV. 1968. Measurement of section thickness. In: Bocciarelli DS, editor. Proceedings of the 4th European Congress on Electron Microscopy. Rome: Tipografia Poliglotta Vaticana, p 609-610.
88. Sofroniew MV, Priestley JV, Consolzaione 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.
89. Sparenborg S, Gabriel M. 1992. Local norepinephrine depletion and learning-related neuronal activity in cingulate cortex and anterior thalamus of rabbits. Exp Brain Res 92: 267-285. (Pubitemid 23018034)
90. Standaert DG, Saper CB, Rye DR, Wainer BH. 1986. Colocalization of atriopeptin-like immunoreactivity with choline acetyltransferase and substance P-like immunoreactivity in the pedunculopontine and laterodorsal tegmental nuclei in the rat. Brain Res 382:163-168.
91. Stanton TL, Johnson GV. 1987. In vitro measurements of cholinergic activity in brain regions of hibernating ground squirrels. Brain Res Bull 18:663-667.
92. Sutin EL, Jacobowitz DM. 1990. Localization of substance P mRNA in cholinergic cells of the rat laterodorsal tegmental nucleus: in situ hybridization histochemistry and immunocytochemistry. Cell Mol Neurobiol 10:19-31.
93. Takashina K, Bessho T, Mori R, Eguchi J, Saito K. 2008. MKC231, a choline uptake enhancer: (2) Effect on synthesis and release of acetylcholine in AF64A-treated rats. J Neural Transm 115:1027-1035.
94. Tomimoto H, Kamo H, Kamyama M, McGeer PL, Kimura H. 1987. Descending projections of the basal forebrain in the rat demonstrated by the anterograde neural tracer Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 425:248-255.
95. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK. 1994. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351-373. (Pubitemid 24309899)
96. Uteshev VV, Meyer EM, Papke RL. 2003. Regulation of neuronal function by choline and 40H-GTS-21 through α7 nicotinic receptors. J Neurophysiol 89:1797-1806. (Pubitemid 36444236)
97. Veznedaroglu E, Milner TA. 1992. Elimination of artifactual labeling of hippocampal mossy fibers seen following preembedding immunogold-silver technique by pretreatment with zinc chelator. Microsc Res Tech 23:100-101.
98. Vincent SR, Satoh K, Armstrong DM, Fibiger HC. 1983. Substance P in the ascending cholinergic reticular system. Nature 306:688-691. (Pubitemid 14201853)
99. Vogelsberg V, Neff NH, Had jiconstatntinou M. 1997. Cyclic AMP-mediated enhancement of high-affinity choline transport and acetylcholine synthesis in brain. J Neurochem 68: 1062-1070.
100. Vogt LJ, Vogt BA, Sikes RW. 1992. Limbic thalamus in rabbit: architecture, projections to cingulate cortex and distribution of muscarinic acetylcholine, GABAA, and opioid receptors. J Comp Neurol 319:205-217.
101. Warburton EC, Aggleton JP. 1999. Differential deficits in the Morris water maze following cytotoxic lesions of the anterior thalamus and fornix transection. Behav Brain Res 98: 27-38.
102. Wecker L, Dettbam WD. 1979. Relationship between choline availability and acetylcholine synthesis in discrete regions of rat brain. J Neurochem 32:961-967. (Pubitemid 9134426)
103. Woolf NJ, Gould E, Butcher LL. 1989. Nerve growth factor receptor is associated with cholinergic neurons of the basal forebrain but not the pontomesencephalon. Neuroscience 30:143-152. (Pubitemid 19159803)
104. Yamamura HI, Snyder SH. 1972. Choline: high-affinity uptake by rat brain synaptosomes. Science 178:626-628.
105. Yamamura HI, Snyder SH. 1973. High affinity transport of choline into synaptosomes of rat brain. J Neurochem 21: 1355-1374.
106. Yan Q, Johnson EM Jr. 1989. Immunohistochemical localization and biochemical characterization of nerve growth factor receptor in adult rat brain. J Comp Neurol 290: 585-598. (Pubitemid 20023016)
107. Yeomans JS. 1995. Role of tegmental cholinergic neurons in dopaminergic activation, antimuscarinic psychosis and schizophrenia. Neuropsychopharmaeology 12:3-16.
108. Yeomans JS, Mathur A, Tampakeras M. 1993. Rewarding brain stimulation: role of the tegmental cholinergic neurons that activate dopamine neurons. Behav Neurosci 107: 1077-1087. (Pubitemid 24018218)
109. Zapata A, Capdevila JL, Trullas R. 2000. Role of high-affinity choline uptake on extracellular choline and acetylcholine evoked by NMDA. Synapse 35:272-280. (Pubitemid 30090556)