CART peptide-immunoreactive neurones in the nucleus accumbens in monkeys: Ultrastructural analysis, colocalization studies, and synaptic interactions with dopaminergic afferents

Journal of Comparative Neurology

Volumn 407, Issue 4, 1999, Pages 491-511

  Smith, Y ^a,b   Kieval, J ^a   Couceyro, P R ^a   Kuhar, M J ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amphetamine; Cocaine; Dense core vesicles; GABA; Ventral striatum

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AMPHETAMINE; COCAINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CORPUS STRIATUM; DENDRITE; DENDRITIC SPINE; DOPAMINERGIC NERVE CELL; FEMALE; IMMUNOREACTIVITY; MALE; NERVE CELL STIMULATION; NONHUMAN; NUCLEUS ACCUMBENS; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SYNAPSE; SYNAPSE VESICLE; ULTRASTRUCTURE;

ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; DOPAMINE; FEMALE; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; MACACA MULATTA; MALE; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; NEURONS; NEURONS, AFFERENT; NUCLEUS ACCUMBENS; PARVALBUMINS; PRIMATES; SAIMIRI; SOMATOSTATIN; SYNAPSES; TISSUE DISTRIBUTION; TYROSINE 3-MONOOXYGENASE;

EID: 0033577723     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990517)407:4<491::AID-CNE3>3.0.CO;2-0     Document Type: Article

References (124)

1. Alheid GF, Heimer L, Switzer RC III. 1990. Basal ganglia. In: Paxinos G, editor. The human nervous system. Sydney: Academic Press. p 483-582.
2. Anderson KD, Reiner A. 1990. Extensive co-occurrence of substance P and dynorphin in striatal projection neurons: an evolutionarily conserved feature of basal ganglia organization. J Comp Neurol 295:339-369.
3. Angulo JA, McEwen BS. 1994. Molecular aspects of neuropeptide regulation and function in the corpus striatum and nucleus accumbens. Brain Res Rev 19:1-28.
4. Arneric SP, Meeley MP, Reis DJ. 1986. Somatostatin and CCK-8 modulate release of striatal amino acids: role of dopamine receptors. Peptides 7:97-103.
5. 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.
6. Bennett BD, Bolam JP. 1993. Two populations of calbindin D28k-immunoreactive neurones in the striatum of the rat. Brain Res 610:305-310.
7. Berendse HW, Groenewegen HJ, Lohman AHM. 1992. Compartmental distribution of ventral striatal neurons projecting to the mesencephalon in the rat. J Neurosci 12:2079-2103.
8. Berridge CW, Startford TL, Foote SL, Kelley AE. 1997. Distribution of dopamine β-hydroxylase-like immunoreactive fibers within the shell subregion of the nucleus accumbens. Synapse 27:230-241.
9. Betancur C, Rostène W, Bérod A. 1997. Chronic cocaine increases neurotensin gene expression in the shell of the nucleus accumbens and in discrete regions of the striatum. Mol Brain Res 44:334-340.
10. Bolam JP, Powell JF, Wu J-Y, Smith AD. 1985. Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: a correlated light and electron microscopic study including a combination of Golgi impregnation with immunocytochemistry. J Comp Neurol 237:1-20.
11. Brog JS, Salyapongse A, Deutch AY, Zahm DS. 1993. The patterns of afferent innervation of the core and shell in the "accumbens" part of the ventral striatum: immunohistochemical detection of retrogradely transported Fluoro-gold. J Comp Neurol 338:255-278.
12. Cain ST, Griff D, Joyner CM, Ellinwood EH, Nemeroff CB. 1993. Chronic continuous or intermittent infusion of cocaine differentially alter the concentration of neurotensin-like immunoreactivity in specific rat brain regions. Neuropsychopharmacology 8:259-265.
13. Choi WS, Ronnekleiv OK. 1996. Effects of in utero cocaine exposure on the expression of mRNAs encoding the dopamine transporter and the D1, D2 and D5 dopamine receptor subtypes in fetal rhesus monkey. Dev Brain Res 96:249-260.
14. Côté P-Y, Sadikot AF, Parent A. 1991. Complementary distribution of calbindin D-28K and parvalbumin in the basal forebrain and midbrain of the squirrel monkey. Eur J Neurosci 3:1316-1329.
15. Couceyro PR, Koylu EO, Kuhar MJ. 1997. Further studies on the anatomical distribution of CART by in situ hybridization. J Chem Neuroanat 12:229-241.
16. Couceyro PR, Paquet M, Koylu E, Kuhar MJ, Smith Y. 1998. Cocaine-and amphetamine-regulated transcript (CART) peptide immunoreactivity in myenteric plexus neurons of the rat ileum and cOlocalization with choline acetyltransferase. Synapse 30:1-8.
17. Cox HM, Rudolph A, Gschmeissner S. 1994. Ultrastructural co-localization of neuropeptide Y and vasoactive intestinal polypeptide in neurosecretory vesicles of submucous neurons in the rat jejunum. Neuroscience 59:469-476.
18. Curran EJ, Watson SJ Jr. 1995. Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361:57-76.
19. Dale N, Ottersen OP, Roberts A, Storm-Mathisen J. 1986. Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324:255-257.
20. Dali Vechia SE, Paré J-F, Lambert PD, Couceyro PR, Kuhar MJ, Smith Y. 1998. Synaptic interactions between CART peptide-immunoreactive terminals and midbrain dopaminergic neurons in the rat. Soc Neurosci Abstr 24:2043.
21. Daunais JB, Nader MA, Porrino LJ. 1997. Long-term cocaine self-administration decreases striatal preproenkephalin mRNA in rhesus monkeys. Pharmacol Biochem Behav 57:471-475.
22. Desjardins C, Parent A. 1992. Distribution of somatostatin immunoreactivity in the forebrain of the squirrel monkey: basal ganglia and amygdala. Neuroscience 47:115-133.
23. DiFiglia M, Pasik T, Pasik P. 1980. Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J Neurocytol 9:471-492.
24. Douglass J, Daoud S. 1996. Characterization of the human cDNA and genomic DNA encoding CART: a cocaine-and amphetamine-regulated transcript. Gene 169:241-245.
25. Douglass J, McKinzie AA, Couceyro PR. 1995. PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J Neurosci 15:2471-2481.
26. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR, Kuhar MJ, Saper CB, Elmquist JK. 1999. Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron (in press).
27. Ellis Y, Davies JA. 1994. The effect of neuropeptides on the release of neurotransmitter amino acids from rat striatum. Neuropeptides 26:65-69.
28. Fallon JH, Ciofi P. 1990. Dynorphin-containing neurons. In: Björklund A, Hökfelt T, Kuhar MJ, editors. Handbook of chemical neuroanatomy: neuropeptides in the CNS. Amsterdam: Elsevier. p 1-130.
29. Fang Y, Janowsky A, Rinnekleiv OK. 1997. Cocaine exposure in fetal rhesus monkey: consequences for dopamine D1-and D2-like receptor binding densities. Dev Brain Res 104:163-174.
30. Gautvik KM, de Lecea L, Gautvik VT, Danielson PE, Tranque P, Dopazo A, Bloom FE, Sutcliffe JG. 1996. Overview of the most prevalent hypothalamus-specific mRNAs, as identified by directional tag PCR subtraction. Proc Natl Acad Sci USA 93:8733-8738.
31. Gerfen CR. 1988. Synaptic organization of the striatum. J Electron Microsc Techn 10:265-281.
32. Gerfen CR. 1992. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Ann Rev Neurosci 15:285-320.
33. Gerfen CR, Young WS III. 1988. Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res 460:161-167.
34. Gracy KN, Svingos AL, Pickel VM. 1997. Dual ultrastructural localization of μ-opioid receptors and NMDA-type glutamate receptors in the shell of the rat nucleus accumbens. J Neurosci 17:4839-4848.
35. Groenewegen HJ, Becker NEHM, Lohman AHM. 1980. Subcortical afferents of the nucleus accumbens septi in the cat, studies with retrograde axonal transport of horseradish peroxidase and bisbenzimide. Neuroscience 5:1903-1916.
36. Groenewegen HJ, Wright CI, Beijer AV 1996. The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res 107:485-511.
37. Haber SN, Lynd E, Klein C, Groenewegen HJ. 1990. Topographic organization of the ventral striatal efferent projections in the rhesus monkey: an anterograde tracing study. J Comp Neurol 293:282-298.
38. Hamel E, Beaudet A. 1987. Opioid receptors in rat neostriatum: radioautographic distribution at the electron microscopic level. Brain Res 401:239-257.
39. Harvey J, Lacey MG. 1996. Endogenous and exogenous dopamine depress EPSCs in rat nucleus accumbens in vitro via D1 receptor activation. J Physiol 492:143-154.
40. Hathway GJ, Emson PC, Humphrey PP, Kendrick KM. 1998. Somatostatin potently stimulates in vivo striatal dopamine and gamma-aminobutyric acid release by a glutamate-dependent action. J Neurochem 70:1740-1749.
41. Heimer L, Switzer RD, Van Hoesen GW. 1982. Ventral striatum and ventral pallidum. Trends Neurosci 5:83-87.
42. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125.
43. Heimer L, Zahm DS, Alheid GF. 1995. Basal ganglia. In: Paxinos G, editor. The rat nervous system, 2nd ed. San Diego: Academic Press. p 579-628.
44. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P. 1985. Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
45. Hsu S, Raine L, Fanger H. 1981. Use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody preparation (PAP) procedures. J Histochem Cytochem 29:577-580.
46. Hurd YL, Herkenham M. 1992. Influence of a single injection of cocaine, amphetamine or GBR 12909 on mRNA expression of striatal neuropeptides. Mol Brain Res 16:97-104.
47. Hussain Z, Totterdell S. 1994. Calbindin-D28k immunoreactive neurons form two populations in the rat nucleus accumbens: a compartmental study. Brain Res 656:191-198.
48. Ikemoto K, Kitahama K, Maeda T, Satoh K. 1996a. The distribution of noradrenaline, serotonin and gamma-aminobutyric acid in the monkey nucleus accumbens. Prog Neuropsychopharmacol Biol Psychiatry 20: 1403-1412.
49. Ikemoto K, Satoh K, Kitahama K, Geffard M, Maeda T. 1996b. Electronmicroscopic study of dopaminergic structures in the medial subdivision of the monkey nucleus accumbens. Exp Brain Res 111:41-50.
50. Johnson LR, Aylward RLM, Hussain Z, Totterdell S. 1994. Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience 61:851-865.
51. Kawaguchi Y, Wilson CJ, Emson PC. 1995. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
52. Kelley AE, Swanson CJ. 1997. Feeding induced by blockade of AMPA and kainate receptors within the ventral striatum: a microinfusion mapping study. Behav Brain Res 89:107-113.
53. Kerkerian-Le Goff L, Forni C, Samuel D, Bloc A, Dusticier N, Nieoullon A. 1992. Intracerebroventricular administration of neuropeptide Y affects parameters of dopamine, glutamate and GABA activities in the rat striatum. Brain Res Bull 28:187-193.
54. Kita H, Kitai ST. 1990. Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol 298:40-49.
55. Kita H, Kosaka T, Heizmann CW. 1990. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536:1-15.
56. Kong JY, Thireson-Klein AK, Klein RL. 1990. Are NPY and enkephalins costored in the same noradrenergic neurons and vesicles? Peptides 11:565-575.
57. Koob GF. 1992. Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Neurosci 13:177-184.
58. Koob GF, Bloom FE. 1988. Cellular and molecular mechanisms of drug dependence. Science 242:713-723.
59. Koylu EO, Couceyro PR, Lambert PD, Ling NC, DeSouza EB, Kuhar MJ. 1997. Immunohistochemical localization of novel CART peptides in rat hypothalamus, pituitary and adrenal gland. J Neuroendocr 9:823-833.
60. Koylu EO, Couceyro PR, Lambert PD, Kuhar MJ. 1998. Cocaine-and amphetamine-regulated transcript peptide immunohistochemical localization in the rat brain. J Comp Neurol 391:115-132.
61. Kristensen P, Judge ME, Thim L, Ribel U, Christjansen KN, Wulff BS, Clausen JT, Jensen PB, Madsen OD, Vrang N, Larsen PJ, Hastrup S. 1998. Hypothalamic CART is a new anorectic peptide regulated by leptin. Nature 393:72-76.
62. Kuhar MJ, Dall Vechia S. 1999. CART peptides: Novel addiction and feeding-related neuropeptides. Trends Neurosci (in press).
63. Kuhar MJ, Boja MC, Ra JW. 1991. The dopamine hypothesis of reinforcing properties of cocaine. Trends Neurosci 14:299-302.
64. Lambert PD, Couceyro PR, Koylu EO, Ling NC, De Souza EB, Kuhar MJ. 1997. CART peptides have a physiological role in the central control of food intake. Soc Neurosci Abstr 23:966.
65. Lambert PD, Couceyro PR, McGirr KM, Dall Vechia SA, Smith Y, Kuhar MJ. 1998. CART peptides in the central control of feeding and interactions with neuropeptide Y. Synapse 29:293-298.
66. Lambert P, Couceyro PR. 1999. CART peptides: a new family of neuropeptides with therapeutic potential in obesity and feeding disorders. Drug News Perspect (in press).
67. Le Moine C, Bloch B. 1996. Expression of the D-3 dopamine receptor in peptidergic neurons of the nucleus accumbens: comparisons with the D1 and D2 dopamine receptors. Neuroscience 73:131-143.
68. Levey AI, Bolam JP, Hallanger AE, Demuth RE, Mesulam M-M, Wainer BH. 1986. A light and electron microscopic procedure for sequential double antigen localization using diaminobenzidine and benzidine dihydrochloride. J Histochem Cytochem 34:1449-1457.
69. Lindefors N. 1992. Amphetamine and haloperidol modulate preprotachykinin A mRNA expression in rat nucleus accumbens and caudateputamen. Mol Brain Res 13:151-154.
70. Lindefors N, Hurd YL, O'Conner WT, Brene S, Persson H, Ungerstedt U. 1992. Amphetamine regulation of acetylcholine and γ-aminobutyric acid in nucleus accumbens. Neuroscience 48:439-448.
71. Llewellyn-Smith I, Pilowsky P, Minson JB. 1993. The tungstate-stabilized tetramethylbenzidine reaction for light and electron microscopic immunocytochemistry and for revealing biocytin-filled neurons. J Neurosci Methods 46:27-40.
72. Lu W, Chen H, Xue CJ, Wolf ME. 1997. Repeated amphetamine administration alters the expression of mRNA for AMPA receptor subunits in the rat nucleus accumbens and prefrontal cortex. Synapse 26:269-280.
73. Lu XY, Ghasemzadeh MB, Kalivas PW. 1998. Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger mRNAs in the neurons projecting from the nucleus accumbens. Neuroscience 82:767-780.
74. Lynd-Balta E, Haber SN. 1994a. The organization of midbrain projections to the ventral striatum in the primates. Neuroscience 59:609-623.
75. Lynd-Balta E, Haber SN. 1994b. Primate striatonigral projections: a comparison of the sensorimotor-related striatum and the ventral striatum. J Comp Neurol 345:562-578.
76. Majeed NH, Przewlocka B, Wedzony K, Przewlocki R. 1986. Stimulation of food intake following opioid microinjection into the nucleus accumbens septi in rats. Peptides 7:711-716.
77. Maldonado-Irizarry CS, Swanson CJ, Kelley AE. 1995. Glutamate receptors in the nucleus accumbens shell control feeding behavior via the lateral hypothalamus. J Neurosci 15:6779-6788.
78. Martin LJ, Hadfield MG, Dellovade TL, Price DL. 1991. The striatal mosaic in primates: patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum. Neuroscience 43:397-417.
79. Meredith GE, Wouterlood FG. 1990. Hippocampal and midline thalamic fibers and terminals in relation to the choline acetyltransferase-immunoreactive neurons in nucleus accumbens of the rat: a light and electron microscopic study. J Comp Neurol 296:204-221.
80. Meredith GE, Ingham CA, Voorn P, Arbuthnott GW. 1993. Ultrastructural characteristics of enkephalin-immunoreactive boutons and their postsynaptic targets in the shell and core of the nucleus accumbens of the rat. J Comp Neurol 332:224-236.
81. 28k. J Comp Neurol 365:628-639.
82. Mitchell BS, Stauber VV. 1993. Localization of substance P and leucine enkephalin in the nerve terminals of the guinea pig paracervical ganglion. Histochem J 25:144-149.
83. Mogenson GJ, Jones DL, Yim CY. 1980. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14:69-97.
84. Newman R, Winans SS. 1980. An experimental study of the ventral striatum of the golden hamster. I. Neuronal connections of the nucleus accumbens. J Comp Neurol 191:167-192.
85. Nicola SM, Malenka RC. 1997. Dopamine depresses excitatory and inhibitory synaptic transmission by distinct mechanisms in the nucleus accumbens. J Neurosci 17:5697-5710.
86. Nicola SM, Malenka RC. 1998. Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J Neurophysiol 79:1768-1776.
87. Nicola SM, Kombian SB, Malenka RC. 1996. Psychostimulants depress excitatory synaptic transmission in the nucleus accumbens via presynaptic D1-like dopamine receptors. J Neurosci 16:1591-1604.
88. O'Donnell P, Grace AA. 1994. Tonic D2-mediated attenuation of cortical excitation in nucleus accumbens neurons recorded in vitro. Brain Res 634:105-112.
89. Paré J-F, Dall Vechia SE, Lambert P, Couceyro P, Kuhar MJ, Smith Y. 1998. CART peptide-immunoreactive neurons in the monkey PVN: electron microscopic characterization and synaptic relationships with NPY-immunoreactive terminals. Soc Neurosci Abstr. 24:2043.
90. Pelletier G. 1984. Ultrastructural colocalization of some neuroactive substances in the rat brain. In: Chan-Palay V, Palay SL, editors. Coexistence of neuroactive substances in neurons. New York: John Wiley. p 63-71.
91. Phend KD, Weinberg RJ, Rustioni A. 1992. Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J Histochem Cytochem 40:1011-1020.
92. Pickel VM, Towle AC, Joh TH, Chan J. 1988. Gamma-aminobutyric acid in the medial rat nucleus accumbens: ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents. J Comp Neurol 272:1-14.
93. Pontieri FE, Tanda G, DiChiara G. 1995. Intravenous cocaine, morphine, and amphetamine preferentially increase extracellular dopamine in the "shell" as compared with the "core" of the rat nucleus accumbens. Proc Natl Acad Sci USA 92:12304-12308.
94. Przewlocka B, Lason W. 1995. Adaptive changes in the proenkephalin and D2 dopamine receptor mRNA expression after chronic cocaine in the nucleus accumbens and striatum of the rat. Eur Neuropsychopharmacol 5:465-469.
95. Reynolds ES. 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17:208-212.
96. 2 dopamine receptors differentially increase FOS-like immunoreactivity in accumbal projections to the ventral pallidum and midbrain, Neuroscience 64:1019-1034.
97. Rye DB, Saper CB, Wainer BH. 1984. Stabilization of the tetramethylbenzidine (TMB) reaction product. J Histochem Cytochem 32:1145-1153.
98. Segal DM, Moraes CT, Mash DC. 1997. Up-regulation of D3 dopamine receptor mRNA in the nucleus accumbens of human cocaine fatalities. Mol Brain Res 45:335-339.
99. Sesack SR, Pickel VM. 1990. In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res 527:266-279.
100. Sidibé M, Smith Y. 1996. Differential synaptic innervation of striatofugal neurones projecting to the internal or external segments of the globus pallidus by thalamic afferents in the squirrel monkey. J Comp Neurol 365:445-455.
101. Sills TL, Vaccarino FJ. 1996. Individual differences in sugar consumption following systemic or intraaccumbens administration of low doses of amphetamine in nondeprived rats. Pharmacol Biochem Behav 54:665-670.
102. Smith AD, Bolam JP. 1990. The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259-265.
103. Smith Y, Bennett BD, Bolam JP, Parent A, Sadikot AF. 1994. Synaptic relationships between dopaminergic afferents and cortical or thalamic input at the single cell level in the sensorimotor territory of the striatum in monkey. J Comp Neurol 344:1-19.
104. Smith Y, Koylu EO, Couceyro P, Kuhar MJ. 1997a. Ultrastructural localization of CART (Cocaine-and Amphetamine-regulated transcript) peptides in the nucleus accumbens of monkeys. Synapse 27:90-94.
105. Smith Y, Paré J-F, Koylu E, Couceyro P, Ince E, Levey AI, Kuhar MJ. 1997b. CART peptide immunoreactivity in the nucleus accumbens of monkeys: electron microscopic analysis and co-localization studies. Soc Neurosci Abstr 23:966.
106. Smith Y, Bevan MD, Shink E, Bolam JP. 1998. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387.
107. Somogyi P, Bolam JP, Smith AD. 1981. Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons: a light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195:567-584.
108. Somogyi P, Hodgson AJ, Chubb IW, Penke B, Erdei A. 1985. Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 33:240-248.
109. Sorg BA, Guminski BJM, Hooks MS, Kalivas PW. 1995. Cocaine alters glutamic acid decarboxylase differentially in the nucleus accumbens core and shell. Mol Brain Res 29:381-386.
110. Spiess J, Villareal J, Vale W. 1981. Isolation and sequence analysis of a somatostatin-like polypeptide from ovine hypothalamus. Biochemistry 20:1982-1988.
111. Stratford TR, Kelley AE. 1997. GABA in the nucleus accumbens shell participates in the central regulation of feeding behavior. J Neurosci 17:4434-4440.
112. Taber MT, Fibiger HC. 1997. Feeding-evoked dopamine release in the nucleus accumbens: regulation by glutamatergic mechanisms. Neuroscience 76:1105-1112.
113. Takagi H, Somogyi P, Somogyi J, Smith AD. 1983. Fine structural studies on a type of somatostatin-immunoreactive neuron and its synaptic connections in the rat neostriatum. J Comp Neurol 214:1-16.
114. Thim L, Nielsen PF, Judge ME, Andersen AS, Diers I, Egel-Mitani M, Hastrup S. 1998. Purification and characterisation of a new hypothalamic satiety peptide, cocaine and amphetamine regulated transcript (CART), produced in yeast. FEBS Lett 428:263-268.
115. Totterdell S, Smith AD. 1989. Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat 2:285-298.
116. Tsumori T, Ando A, Domoto T, Oki M, Nakamura T. 1994. Coexistence of vasoactive intestinal polypeptide and neuropeptide Y immunoreactivity within axon terminals in the canine and human lower esophageal sphineter: electron microscopy by a double immunogold labeling procedure. Acta Anat 149:272-278.
117. Van Bockstaele EJ, Sesack SR, Pickel VM. 1994. Dynorphin-immunoreactive terminals in the rat nucleus accumbens: cellular sites for modulation of target neurons and interactions with catecholamine afferents. J Comp Neurol 341:1-15.
118. Van Bockstaele EJ, Gracy KN, Pickel VM. 1995. Dynorphin-immunoreactive neurons in the rat nucleus accumbens: ultrastructure and synaptic input from terminals containing substance P and/or dynorphin. J Comp Neurol 351:117-133.
119. Voorn P, Jorritsma-Byham B, Van Dijk C, Buijs RM. 1986. The dopaminergic innervation of the ventral striatum in the rat: a light-and electron-microscopical study with antibodies against dopamine. J Comp Neurol 251:84-89.
120. Wilson CJ, Groves PM. 1980. Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J Comp Neurol 194: 599-615.
121. Wise RA, Fotuhi M, Colle LM. 1989. Facilitation of feeding by nucleus accumbens amphetamine injections: latency and speed measures. Biochem Behav 32:769-772.
122. Yim CY, Mogenson GJ. 1988. Neuromodulatory action of dopamine in the nucleus accumbens: an in vivo intracellular study. Neuroscience 26:403-415.
123. Zahm DS, Heimer L. 1993. Specificity in the efferent projections of the nucleus accumbens in the rat: comparison of the rostral pole projection patterns with those of the core and shell. J Comp Neurol 327:220-232.
124. Zhang Y, Landas K, Mueller H, Angulo JA. 1997. Progressive augmentation of striatal and accumbal preprotachykinin mRNA levels by chronic treatment with methamphetamine and effect of concurrent administration of the N-methyl-D-aspartate receptor antagonist MK-801. Neuropharmacology 36:325-334