Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T20:57:46.595Z Has data issue: false hasContentIssue false
  • English
  • Français

Neurotransmitters in the Mammalian Striatum: Neuronal Circuits and Heterogeneity

Published online by Cambridge University Press:  05 January 2016

K. Semba ,
H.C. Fibiger  and
S.R. Vincent
K. Semba*
Affiliation:
Division of Neurological Sciences, Department of Psychiatry, University of British Columbia, Vancouver
H.C. Fibiger
Affiliation:
Division of Neurological Sciences, Department of Psychiatry, University of British Columbia, Vancouver
S.R. Vincent
Affiliation:
Division of Neurological Sciences, Department of Psychiatry, University of British Columbia, Vancouver
*
Department of Neurological Sciences, Department of Psychiatry, The University of British Columbia, 2136 West Mall, Vancouver, B.C., Canada V6T 2A1
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The major input and output pathways of the mammalian striatum have been well established. Recent studies have identified a number of neurotransmitters used by these pathways as well as by striatal interneurons, and have begun to unravel their synaptic connections. The major output neurons have been identified as medium spiny neurons which contain ɣ-aminobutyric acid (GABA), endogeneous opioids, and substance P. These neurons project to the pallidum and substantia nigra in a topographic and probably chemically organized manner. The major striatal afferents from the cerebral cortex, thalamus, and substantia nigra terminate, at least in part, on these striatal projection neurons. Striatal interneurons contain acetylcholine, GABA, and somatostatin plus neuropeptide Y, and appear to synapse on striatal projection neurons. In recent years, much activity has been directed to the neurochemical and hodological heterogeneities which occur at a macroscopic level in the striatum. This has led to the concept of a patch-matrix organization in the striatum.

Type
Research Article
Information
Canadian Journal of Neurological Sciences , Volume 14 , Issue S3 , August 1987 , pp. 386 - 394
Copyright
Copyright © Canadian Neurological Sciences Federation 1987

References

REFERENCES

1.Carpenter, MB.Anatomy of the corpus striatum and brain stem integrating systems. In: Handbook of Physiology. Sect. 1 The Nervous System, Vol. 2. Motor Control, Part 2, Brookhart, JM, Mountcastle, VB, Brooks, VB, eds. American Physiological Society, Washington, DC, 1981: 947–995.Google Scholar
2.Graybiel, AM, Ragsdale, CW Jr.Biochemical anatomy of the striatum. In: Chemical Neuroanatomy, Emson, PC, ed. Raven Press, New York, 1983: 427–504.Google Scholar
3.Groves, PM.A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res Rev 1983; 5: 109–132.CrossRefGoogle Scholar
4.Bolam, JP.Synapses of identified neurons in the neostriatum. In: Functions of the basal ganglia (Ciba Foundation Symposium 107), Pitman, London, 1984: 30–47.Google Scholar
5.Mcgeer, EG, Staines, WA, Mcgeer, PL. Neurotransmitters in the basal ganglia. Can J Neurol Sci 1984; 11: 89–99.CrossRefGoogle ScholarPubMed
6.Parent, A.Comparative neurobiology of the basal ganglia. Wiley, New York, 1986.Google Scholar
7.Kitai, ST, Kocsis, JD.Wood, J.Origin and characteristics of the cortico-caudate afferents: An anatomical and electrophysiological study. Brain Res 1976; 118: 137–141.CrossRefGoogle ScholarPubMed
8.Jones, EG, Coulter, JD, Burton, H, et al. Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys. J Comp Neurol 1977; 173: 53–80.CrossRefGoogle ScholarPubMed
19.Royce, GJ.Laminar origin of cortical neurons which project upon the caudate nucleus: A horseradish peroxidase investigation in the cat. J Comp Neurol 1982; 205: 8–29.CrossRefGoogle ScholarPubMed
10.Fisher, RS, Shiota, C, Levine, MS, et al. Interhemispheric organiza-tion of corticocaudate projections in the cat: A retrograde double-labelling study. Neurosci Lett 1984; 48: 369–373.CrossRefGoogle Scholar
11.Kemp, JM, Powell, TPS. The site of termination of afferent fibers in the caudate nucleus. Phil Trans Roy Soc. London, 1971: 262: 413–427.Google ScholarPubMed
12.Somogyi, P, Bolam, JP, Smith, AD. 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 1981; 195: 567–584.CrossRefGoogle ScholarPubMed
13.Fonnum, F, Storm-Mathisen, J, Divac, I. Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibers in rat brain. Neurosci 1981; 6: 863–873.CrossRefGoogle ScholarPubMed
14.Jones, EG, Leavitt, RY. Retrograde axonal transport and the dem-constration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J Comp Neurol 1974; 154: 349–378.CrossRefGoogle Scholar
15.Royce, GJ.Autoradiographic evidence for a discontinuous projec- tion to the caudate nucleus from the centromedian nucleus in the cat. Brain Res 1978; 146: 145–150.CrossRefGoogle Scholar
16.Beckstead, RM.The thalamostriatal projection in the cat. J Comp Neurol 1984; 223: 313–346.CrossRefGoogle ScholarPubMed
17.Kitai, ST.Electrophysiology of the corpus striatum and brain stem integrating systems. In: Handbook of Physiology, Sect. I. The Nervous System, Vol 2. Motor control, Part 2, Brookhart, JM, Mountcastle, VB, Brooks, VB, eds. American Physiological Society, Washington, D.C., 1981: 997–1015.Google Scholar
18.Saelens, JK, Edwards-Neale, S, Simke, JP. Further evidence for cholinergic thalamo-striatal neurons. J Neurochem 1979; 32: 1093–1094.CrossRefGoogle ScholarPubMed
19.Fibiger, HC.The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res Rev 1982; 4: 327–388.CrossRefGoogle Scholar
20.Sugimoto, T, Takada, M, Kaneko, T, et al. Substance P-positive thalamocaudate neurons in the center median-parafascicular complex in the cat. Brain Res 1984; 323: 181–184.CrossRefGoogle Scholar
21.Sugimoto, T, Itoh, KYasui, Y, et al. Coexistence of neuropeptides in projection neurons of the thalamus in the cat. Brain Res 1985: 347: 381–384.CrossRefGoogle ScholarPubMed
22.Covenas, R, Romo, R, Cheramy, A, et al. Immunocytochemical study of enkephalin-like cell bodies in the thalamus of the cat. Brain Res 1986; 377: 355–361.CrossRefGoogle ScholarPubMed
23.Fibiger, HC, Pudritz, RE, Mcgeer, PL, et al. Axonal transport in nigro-striatal and nigro-thalamic neurons: Effects of medial fore-brain bundle lesions and 6-hydroxydopamine. J Neurochem 1972; 19: 1697–1708.CrossRefGoogle ScholarPubMed
24.Guyenet, PG, Crane, JK. Non-dopaminergic nigrostriatal pathway. Brain Res 1981; 213: 291–305.CrossRefGoogle ScholarPubMed
25.Vander Kooy, D, Coscina, DV, Hattori, T. Is there a non-dopaminergic nigrostriatal pathway? Neurosci 1981; 6: 345–357.CrossRefGoogle Scholar
26.Gerfen, CR, Herkenham, M, Thibault, J. The neostriatal mosaic : II. Compartmental organization of mesotriatal dopaminergic and non-dopaminergic systems. J Neurosci (In press).Google Scholar
27.Bouyer, JJ, Park, DK, Joh, TH, et al. Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res 1984; 302: 267–275.CrossRefGoogle ScholarPubMed
28.Freund, TF, Powell, JF, Smith, AD. Tyrosine hydroxylase-immuno-reactive boutons in synaptic contacts with identified striatonigral neurons, with particular reference to dendritic spines. Neurosci 1984; 13: 1189–1216.CrossRefGoogle ScholarPubMed
29.Hökfelt, T, Skirboll, L, Rehfeld, JF, et al. A subpopulation of mesencephalic dopamine neurons projecting to limbic areas contains a cholecystokinin-like peptide: Evidence from immuno-histochemistry combined with retrograde tracing. Neurosci 1980: 5: 2093–2124.CrossRefGoogle Scholar
30.Zaborszky, L, Alheid, AF, Beinfeld, MC, et al. Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study. Neurosci 1985; 14: 427–453.CrossRefGoogle ScholarPubMed
31.Hökfelt, T, Everitt, BJ, Theodorsson-Norheim, E, et al. Occur-rence of neurotensin-like immunoreactivity in subpopulations of hypothalamic, mesencephalic, and medullary catecholamine neurons. J Comp Neurol 1984: 222: 543–559.CrossRefGoogle Scholar
32.Kalivas, PW, Miller, JS. Nerotensin neurons in the ventral tegmen-tal area project to the medial nucleus accumbens. Brain Res 1984; 300: 157–160.CrossRefGoogle Scholar
33.Parent, A, Descarries, L, and Beaudet, A. Organization of ascend-ing serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of [3H] 5-hydroxy-tryptamine. Neurosci 1981:6: 115–138.CrossRefGoogle Scholar
34.Descarries, L, Berthelet, F, Garcia, S, et al. Dopaminergic projec-tion from nucleus raphe dorsalis to neostriatum in the rat. J Comp Neurol 1986; 249: 511–520.CrossRefGoogle ScholarPubMed
35.Steinbusch, HWM, Sauren, Y, Groenewegen, HJ, etal. Histaminergic projections from the premammillary and posterior hypothalamic region to the caudate-putamen complex in the rat. Brain Res 1986; 368: 389–393.CrossRefGoogle Scholar
36.Staines, WA, Atmadja, S, Fibiger, HC. Demonstration of a pallidostriatal pathway by retrograde transport of HRP-labelled lectin. Brain Res 1981; 206: 446–450.CrossRefGoogle Scholar
37.Beckstead, RM.A pallidostriatal projection in the cat and monkey. Brain Res Bull 1983a; 11: 629–632.CrossRefGoogle Scholar
37a.Parent, A, Mackey, A, De Bellefeuille, L. The subcortical afferents to caudate nucleus and putamen in primate: A fluorescenece retrograde double labelling study. Neuroscience, 1983; 10: 1137–1150.CrossRefGoogle Scholar
38.Beckstead, RM. A reciprocal axonal connection between the subthalamic nucleus and the neostriatum in the cat. Brain Res 1983b; 275: 137–142.CrossRefGoogle ScholarPubMed
39.Kelly, AE, Domesick, VB, Nauta, WJH. The amygdalostriatal projection in the rat: An anatomical study by anterograde and retrograde tracing method. Neurosci 1982; 7: 615–630.CrossRefGoogle Scholar
40.Fass, B, Talbot, K, Butcher, LL. Evidence that efferents from the basolateral amygdala innervate the dorsolateral neostriatum in rats. Neurosci Lett 1984; 44: 71–75.CrossRefGoogle ScholarPubMed
41.Russchen, FT, Bakst, I, Amaral, DG, et al. The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res 1985; 329: 241–257.CrossRefGoogle ScholarPubMed
42.Meyer, DK, Beinfeld, MC, Oertel, WH, et al. Origin of the cholecystokinin-containing fibers in the rat caudatoputamen. Science 1982; 215: 187–188.CrossRefGoogle ScholarPubMed
43.Saper, CB, Loewy, AD. Projections of the pedunculopontine teg- mental nucleus in the rat: Evidence foradditional extrapyramidal circuitry. Brain Res 1982; 252: 367–372.CrossRefGoogle Scholar
44.Kim, JS, Bak, IJ, Hassler, R, et al. Role of -v-aminobutyric acid (GABA) in the extrapyramidal motor system. 2. Some evidence for the existence of a type of GABA-rich strionigral neuron. Exp Brain Res 1971; 14: 95–104.CrossRefGoogle Scholar
45.Fibiger, HC.Organization of GABA-containing neurons in some extrapyramidal nuclei. J Can Neurol Sci 1980; 7: 251:252.CrossRefGoogle ScholarPubMed
46.Staines, WA, Nagy, JI, Vincent, SR, et al. Neurotransmitters con-tained in the efferents of the striatum. Brain Res 1980; 194: 391–402.CrossRefGoogle Scholar
47.Bolam, JP, Clarke, DH, Smith, AD, et al. A type of aspiny neuron in the rat neostriatum accumlates [3H]-ϒ-aminobuty ric acid : combination of Golgi-staining, autoradiography and electron microscopy. J Comp Neurol 1983; 213: 121–134.CrossRefGoogle Scholar
48.Bolam, JP, Somogyi, P, Takagi, H, et al. Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: A correlated light and electron microscopic study. J Neurocytol 1983; 12: 325–344.CrossRefGoogle Scholar
49.Bolam, JP, Powell, JF, Wu, J-Y, et al. 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 1985,237: 1–20.CrossRefGoogle ScholarPubMed
50.Ribak, CE, Vaughn, JE, Roberts, E.The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol 1979; 187: 261–284.CrossRefGoogle ScholarPubMed
51.Ribak, CE.The GABAergic neurons of the extrapyramidal system as revealed by immunocytochemistry. In: GABA and the basal ganglia, ed. Di Chiara, G, Gessa, GL.Raven Press, New York 1981, 187: 261:284.Google Scholar
52.Panula, P, Wu, J-Y, Emson, P.Ultrastructure of GABA-neurons in cultures of rat neostriatum. Brain Res 1981; 219: 202–207.CrossRefGoogle ScholarPubMed
53.Oertel, WH, Mugnaini, E.lmmunocytochemical studies of GABA-ergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci Lett 1984; 47: 233–238.CrossRefGoogle Scholar
54.Fisher, RS, Buchwald, NA, Hull, CD, et al. The GABAergic striatonigral neurons of the cat: demonstration by double peroxidase labeling. Brain Res 1986; 398: 148–156.CrossRefGoogle ScholarPubMed
55.Clarke, DJ, Smith, AD, Bolam, JP.Uptake of [3H] taurine into medium-size neurons and into identified striatonigral neurons in the rat neostriatum. Brain Res 1983; 289: 342–348.CrossRefGoogle ScholarPubMed
56.Aronin, N, Difiglia, M, Graveland, GA, et al. Localization of immu-noreacti ve enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res 1984; 300: 376–380.CrossRefGoogle Scholar
57.Morelli, M, Di Chiara, G.Coexistence of GABA and enkephalin striatal neurons and possible coupling of G AB A-ergic and opiatergic systems in the basal ganglia. Neuropharm 1984; 23: 847.CrossRefGoogle Scholar
58.Zahm, DS, Zaborszky, L, Alones, VE, et al. Evidence for the coexistence of glutamate decarboxylase and met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum. Brain Res 1985;325:317–321.CrossRefGoogle ScholarPubMed
59.Aronin, N, Chase, K, Difiglia, M.Glutamic acid decarboxylase and enkephalin immunoreactive axon terminals in the rat neostriatum synapse with striatonigral neurons. Brain Res 1986; 365:151–158.CrossRefGoogle ScholarPubMed
60.Penny, GR, Afsharpour, S, Kitai, ST.The glutamate decarboxylase leucine enkephalin-, methionine enkephalin- and substance P-immunoreactive neurons in the neostriatum of the rat and cat: evidence for partial population overlap. Neurosci 1986; 17: 1011–1045.CrossRefGoogle ScholarPubMed
61.Hökfelt, T, Elde, R, Johansson, O, et al. The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 1977; 5: 25–31.CrossRefGoogle ScholarPubMed
62.Cuello, AC, Paxinos, G.Evidence for a long leu-enkephalin striopallidal pathway in rat brain. Nature 1978; 271: 178–180.CrossRefGoogle ScholarPubMed
63.Sugimoto, T, Mizuno, N.Immunohistochemical demonstration of neurotensin in striatal neurons of the cat, with particular reference to coexistence with enkephalin. Brain Res 1986;398:195–198.CrossRefGoogle ScholarPubMed
64.Haber, S, Elde, R.The distribution of enkephalin immunoreactive neuronal cell bodies in the monkey brain: Preliminary observations. Neurosci Lett 1982; 32: 247–252.CrossRefGoogle ScholarPubMed
65.Inagaki, S, Parent, A.Distribution of enkephalin-immunoreactive neurons in the forebrain and upper brainstem of the squirrel monkey. Brain Res 1985; 359: 267–280.CrossRefGoogle ScholarPubMed
66.Pickel, VM, Sumal, KK, Beckley, SC, et al. lmmunocytochemical localization of enkephalin in the neostriatum of rat brain: A light and electron microscopic study. J Comp Neurol 1980; 189:721–740.Google Scholar
67.Kubota, Y, Inagaki, S, Kilo, S, et al. Ultrastructural evidence of dopaminergic input to enkephalinergic neurons in rat neostriatum. Brain Res 1986; 367: 374–378.CrossRefGoogle ScholarPubMed
68.Difiglia, M, Aronin, N, Martin, JB.Light and electron microscopic localization of immunoreactive leu-enkephalin in the monkey basal ganglia. J Neurosci 1982; 2: 303–320.CrossRefGoogle ScholarPubMed
69.Somogyi, P, Priestly, JV, Cuello, AC, et al. Synaptic connections of enkephalin-immunoreactive nerve terminals in the neostriatum: A correlated light and electron microscopic study. J Neurocytol 1982b; 11: 779–807.CrossRefGoogle ScholarPubMed
70.Bouyer, JJ, Miller, RJ, Pickel, VM.Ultrastructural relation between cortical afferents and terminals containing enkephalin-like immunoreactivity in the rat neostriatum. Regulat Pep 1984a;8:105–115.CrossRefGoogle Scholar
71.Somogyi, P, Priestley, JV, Cuello, AC, et al. Synaptic connections of substance P-immunoreactive nerve terminals in the substantia nigra of the rat: A correlated light- and electron- microscopic study. Cell Tissue Res 1982a; 223: 469–486.CrossRefGoogle Scholar
72.Bolam, JP, Somogyi, P, Totterdell, S, et al. A second type of striatonigral neurons: A comparison between light and electron microscopic levels. Neurosci 1981; 6: 2141–2157.CrossRefGoogle ScholarPubMed
73.Vincent, SR, Hökfelt, T, Christensson, I, et al. Dynorphin- immunoreactive neurons in the central nervous system of the rat. Neurosci Lett 1982a; 33: 185–190.CrossRefGoogle ScholarPubMed
74.Vincent, SR, Hökfelt, T, Christensson, I, et al. Immunohistochemi-cal evidence for a dynorphin immunoreactive striato-nigral pathway. Europ J Pharmacol 1982b; 85: 251–252.CrossRefGoogle Scholar
75.Kanazawa, I, Emson, PC, Cuello, AC. Evidence for the existence of substance P-containingfibres in striato-nigral and pallidonigral pathways in rat brain. Brain Res 1977; 119: 447–453.CrossRefGoogle ScholarPubMed
76.Cuello, AC, Kanazawa, I.The distribution of substance ? immunoreactive fibers in the rat central nervous system. J Comp Neurol 1978; 178: 129–156.CrossRefGoogle ScholarPubMed
77.Ljungdahl, A, Hökfelt, T, Nilsson, G.Distribution of substance P-like immunoreactivity in the central nervous system of the rat -1. Cell bodies and nerve terminals. Neurosci 1978; 3: 861–943.CrossRefGoogle Scholar
78.Beach, TG, Mcgeer, EG.The distribution of substance ? in the primate basal ganglia: An Immunohistochemical study of baboon and human brain. Neurosci 1984; 13: 29–52.CrossRefGoogle ScholarPubMed
79.Difiglia, M, Aronin, N, Leeman, SE.Immunoreactive substance P in the substantia nigra of the monkey: light and electron microscopic localization. Brain Res 1981; 233: 381–388.CrossRefGoogle Scholar
80.Haber, S, Elde, R.Correlation between met-enkephalin and sub-stance P immunoreactivity in the primate globus pallidus. Neurosci 1981; 6: 1291–1298.CrossRefGoogle Scholar
81.Haber, SN, Nauta, WJH.Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neurosci 1983; 9: 245–260.CrossRefGoogle ScholarPubMed
82.Lehmann, J, Fibiger, HC. Acetylcholinesterase and the cholinergic neurons. Life Sci 1979; 25: 1939–1947.CrossRefGoogle Scholar
83.Kimura, H, Mcgeer, PL, Peng, F, et al. Choline acetyltransferase- containing neurons in rodent brain demonstrated by immunohistochemistry. Science 1980; 208: 1057–1069.CrossRefGoogle ScholarPubMed
84.Satoh, K, Armstrong, DM, Fibiger, HC. A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltrans-ferase immunohistochemistry. Brain Res Bull 1983a; 11:693–720.CrossRefGoogle Scholar
85.Kimura, H, Mcgeer, PL, Peng, JH, et al. The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 1981; 200: 151–201.CrossRefGoogle ScholarPubMed
86.Vincent, SR, Reiner, PB. The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull 1987; 18: 371–415.CrossRefGoogle ScholarPubMed
87.Satoh, K, Fibiger, HC.Distribution of central cholinergic neurons in the baboon (Papio papio). I. General morphology. J Comp Neurol 1985; 236: 197–214.CrossRefGoogle ScholarPubMed
88.Satoh, K, Staines, WA, Atmadja, S, et al. Ultrastructural observa-tions of the cholinergic neuron in the rat striatum as identified by acetylcholinesterase pharmacohistochemistry. Neurosci 1983b; 10: 1121–1136.CrossRefGoogle Scholar
88a.Bolam, JP, Ingham, CA, Smith, AD. The section-Golgi-impregnation procedure - 3. Combination of Golgi-impregnation with enzyme histochemistry and electron microscopy to characterize acetyl-cholinesterase-containing neurons in the rat neostriatum. Neurosci 1984; 12: 687–709.CrossRefGoogle ScholarPubMed
89.Bolam, JP, Wainer, BH, Smith, AD.Characterization of cholinergic neurons in the rat neostriatum. A combination of choline acetyltransferase immunocytochemistry. Golgi-impregnation and electron microscopy. Neurosci 1984; 12: 711–718.CrossRefGoogle ScholarPubMed
90.Phelps, PE, Houser, CR, Vaughn, JE. Immuncytochemical localiza-tion of choline acetyltransferase within the rat neostriatum: A correlated light and electron microscopic study cholinergic neurons and synapses. J Comp Neurol 1985; 238: 286–307.CrossRefGoogle Scholar
91.Bolam, JP, Ingham, CA, Izzo, PN, et al. Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: A double immunocytochemi-cal study in the rat. Brain Res 1986; 397: 279–289.CrossRefGoogle ScholarPubMed
92.Wainer, BH, Bolam, JP, Freund, TF, et al. Cholinergic synapses in the rat brain: A correlated light and electron microscopic immunohistochemical study employing a monoclonal antibody against choline acetyltransferase. Brain Res 1984; 308: 69–76.CrossRefGoogle Scholar
93.Finley, JCW, Grossman, GH, Dimeo, P, et al. Somatostatin-containing neurons in the rat brain: Widespread distribution revealed by immunocytochemistry after pretreatment with pronase. Am J Anat 1978; 153: 483–488.CrossRefGoogle ScholarPubMed
94.Chesselet, MF, Graybiel, AM. Striatal neurons expressing somato-statin-like immunoreactivity: Evidence for peptidergic interneu-ronal system in the cat. Neurosci 1986; 17: 547–571.CrossRefGoogle ScholarPubMed
95.Smith, Y, Parent, A.Neuropeptide Y-immunoreactive neurons in the striatum of cat and monkey: Morphological characteristics, intrinsic organization and co-localization with somatostatin. Brain Res 1986; 372: 241–252.CrossRefGoogle Scholar
96.Vincent, SR, Skirboll, L, Hökfelt, T, et al. Coexistence of somatostatin-and avian pancreatic polypeptide (APP)-like immunoreactivity in some forebrain neurons. Neurosci 1982c; 7: 439–446.CrossRefGoogle ScholarPubMed
97.Vincent, SR, Johansson, O, Hökfelt, T, et al. NADPH-diaphorase: A selective histochemical marker for striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities. J Comp Neurol 1983a; 217: 252–263.CrossRefGoogle ScholarPubMed
98.Vincent, SR, Staines, WA, Fibiger, HC. Histochemical demonstra-tion of separate populations of somatostatin and cholinergic neurons in the rat striatum. Neurosci Lett 1983b; 35: 111–114.CrossRefGoogle Scholar
99.Difiglia, M, Aronin, N. Ultrastructural features of immunoreactive somatostatin neurons in the rat caudate nucleus. J Neurosci 1982; 2: 1267–1274.CrossRefGoogle ScholarPubMed
100.Takagi, H, Somogyi, P, Somogyi, J, et al. Fine structural studies on a type of somatostatin-immunoreactive neuron and its synaptic connections in the rat neostriatum: A correlated light and electron microscopic study. J Comp Neurol 1983; 214: 1–16.CrossRefGoogle ScholarPubMed
101.Vincent, SR, Johansson, O.Striatal neurons containing both somatostatin-and avian pancreatic polypeptide (APP)-like immunoreactivities and NADPH-diaphorase activity: A light and electron microscopic study. J Comp Neurol 1983;217:264–270.CrossRefGoogle ScholarPubMed
102.Takagi, H, Mizuta, H, Matsuda, T, et al. The occurrence of cholecystokinin-like immunoreactive neurons in the rat neostriatum: light and electron microscopic analysis. Brain Res 1984; 309: 346–349.CrossRefGoogle ScholarPubMed
103.Hökfelt, T, Schultzberg, M, Lundberg, JM, et al. Distribution of vasoactive intestinal polypeptide in the central and peripheral nervous systems as revealed by immunocytochemistry. In: Said, SI, ed. Vasoactive Intestinal Peptide. Raven Press, New York, 1982: 65–90.Google Scholar
104.Skofitsch, G, Jacobowitz, DM. Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides 1985; 6: 509–546.CrossRefGoogle ScholarPubMed
105.Mensah, PL.The internal organization of the mouse caudate nucleus: Evidence for cell clustering and regional variation. Brain Res 1977; 137: 53–66.CrossRefGoogle ScholarPubMed
106.Mensah, PL.Distribution of the largest neuron in mouse caudate-putamen nucleus: Its position in large-cell - medium-cell clusters. Exp Brain Res 1980; 38: 267–271.CrossRefGoogle ScholarPubMed
107.Goldman-Rakic, PS.Cytoarchitectonic heterogeneity of the primate neostriatum: Subdivision into island and matrix cellular compartments. J Comp Neurol 1982; 205: 398–413.CrossRefGoogle ScholarPubMed
108.Graybiel, AM, Ragsdale, CW Jr.Histochemically distinct compartments in the striatum of human, monkey, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci 1978; 75: 5723–5726.CrossRefGoogle ScholarPubMed
109.Pert, CB, Kuhar, MJ, Snyder, SH.Opiate receptor: Autoradiographic localization in rat brain. Proc Natl Acad Sci 1978; 73: 3729–3733.CrossRefGoogle Scholar
110.Herkenham, M, Pert, CB.Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 1981;291:415–418.CrossRefGoogle ScholarPubMed
111.Graybiel, AM, Ragsdale, CW Jr, Yoneoka, ES, et al. An immunohis- tochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining. Neurosci 1981; 6: 377–397.CrossRefGoogle Scholar
112.Graybiel, AM, Pickel, VM, Joh, TH, et al. Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum. Proc Natl Acad Sci 1981; 78: 5871–5875.CrossRefGoogle ScholarPubMed
113.Graybiel, AM, Chesselet, MF.Compartmental distribution of striatal cell bodies expressing [Met]enkephalin-like immunoreactivity. Proc Natl Acad Sci 1984; 81: 7980–7984.CrossRefGoogle ScholarPubMed
114.Goedert, M, Mantyh, PW, Hunt, SP, et al. Mosaic distribution of neurotensin-like immunoreactivity in the cat striatum. Brain Res 1983; 274: 176–179.CrossRefGoogle ScholarPubMed
115.Goedert, M, Mantyh, PW, Emson, PC, et al. Inverse relationship between neurotensin receptors and nerotensin-like immunoreactivity in cat striatum. Nature 1984; 307: 543–546.CrossRefGoogle ScholarPubMed
116.Gerfen, CR.The neostriatal mosaic: Compartmentalization of corticostriatal input and striatonigral output systems. Nature 1984; 311: 461–464.CrossRefGoogle ScholarPubMed
117.Gerfen, CR.The neostriatal mosaic. I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J Comp Neurol 1985; 236: 454–476.CrossRefGoogle Scholar
118.Sandell, JH, Graybiel, AM, Chesselet, MF.A new enzyme marker for striatal compartmentalization: NADPH diaphorase activity in the caudate nucleus and putamen of the cat. J Comp Neurol 1986; 243: 326–334.CrossRefGoogle ScholarPubMed
119.Graybiel, AM.Neurochemically specified subsystems in the basal ganglia, In: Evered, D, O’Connor, M, eds. Functions of the basal ganglia (Ciba Foundation Symposium 107), Pitman, London, 1984b: 114–149.Google ScholarPubMed
120.Graybiel, AM, Baughman, RW, Eckenstein, F.Cholinergic neuropil of the striatum observes striosomal boundaries. Nature 1986; 323: 625–627.CrossRefGoogle ScholarPubMed
121.Nastuk, MA, Graybiel, AM.Patterns of muscarinic cholinergic binding in the striatum and their relation to dopamine islands and striosomes. J Comp Neurol 1985; 237: 176–194.CrossRefGoogle ScholarPubMed
122.Brand, S.A comparison of the distribution of acetylcholinesterase and muscarinic cholinergic receptors in the feline neostriatum. Neurosci Lett 1980; 17: 113–117.CrossRefGoogle ScholarPubMed
123.Olson, L, Seiger, A, Fuxe, K.Heterogeneity of striatal and limbic dopamine innervation: Highly fluorescent islands in developing and adult rats. Brain Res 1972; 44: 283–288.CrossRefGoogle ScholarPubMed
124.Moon Edley, S, Herkenham, M.Comparative development of striatal opiate receptors and dopamine revealed by autoradiography and histofluorescence. Brain Res 1984; 305: 27–42.CrossRefGoogle ScholarPubMed
125.Agnati, LF, Fuxe, K, Anderson, K, et al. The mesolimbic dopamine system: Evidence for a high amine turnover and for a heterogeneity of the dopamine neurons population. Neurosci Lett 1980; 18: 45–51.CrossRefGoogle ScholarPubMed
126.Tennyson, VM, Barrett, RE, Cohen, G, et al. The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and (3H) dopamine uptake. Brain Res 1972; 46: 251–285.CrossRefGoogle Scholar
127.Fukui, K, Kariyama, H, Kashiba, A, et al. Further confirmation of heterogeneity of the rat striatum: Different mosaic patterns of dopamine fibers after administration of methamphetamine or reserpine. Brain Res 1986; 382: 81–86.CrossRefGoogle ScholarPubMed
128.Joyce, JN, Douglas, WS, Marshall, JF.Human striatal dopamine receptors are organized in compartments. Proc Natl Acad Sci 1986; 83: 8002–8006.CrossRefGoogle ScholarPubMed
129.Künzle, J.Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. Brain Res 1975; 88: 195–210.CrossRefGoogle Scholar
130.Kalil, K.Patch-like termination of thalamic fibers in the putamen of the rhesus monkey: An autoradiographic study. Brain Res 1978; 140: 333–339.CrossRefGoogle ScholarPubMed
131.Donoghue, JP, Herkenham, M.Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 1986; 365: 397–403.CrossRefGoogle ScholarPubMed
132.Ragsdale, CW Jr, Graybiel, AM.The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry. Brain Res 1981; 208: 259–266.CrossRefGoogle Scholar
133.Beckstead, RM.Complementary mosaic distributions of thalamic and nigral axons in the caudate nucleus of the cat: Double anterograde labeling combined autoradiography and wheat germ-HRP histochemistry. Brain Res 1985; 335: 135–159.CrossRefGoogle ScholarPubMed
134.Wright, AK, Arbuthnott, GW.The pattern of innervation of the corpus striatum by the substantia nigra. Neurosci 1981; 6: 2063–2067.CrossRefGoogle ScholarPubMed
135.Herkenham, M, Moon Edley, S, Stuart, J.Cell clusters in the nucleus accumbens of the rat, and the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations. Neurosci 1984; 11: 561–593.CrossRefGoogle ScholarPubMed
136.Gerfen, CR, Baimbridge, KG, Thibault, J.The neostriatal mosaic. III. Biochemical and developmental dissociation of dual patch-matrix nigrostriatal systems. J Neurosci (In press).Google Scholar
137.Graybiel, AM, Ragsdale, CW Jr, Moon Edley, S.Compartments in the striatum of the cat observed by retrograde cell labeling. Exp Brain Res 1979; 34: 189–195.CrossRefGoogle ScholarPubMed
138.Kent, JL, Pert, CB, Herkenham, M.Ontogeny of opiate receptors in rat forebrain: Visualization by in vitro autoradiography. Dev Brain Res 1982; 2: 487–504.CrossRefGoogle Scholar
139.Lança, AJ, Boyd, S, Kolb, B, et al. The development of a patchy organization of the rat striatum. Dev Brain Res 1986; 27: 1–10.CrossRefGoogle Scholar
140.Rotter, A, Field, PM, Raisman, G.Muscarinic receptors in the central nervous system of the rat. III. Postnatal development of binding of [?] propylbenzilylcholine mustard. Brain Res 1979; 180(2): 185–205.CrossRefGoogle ScholarPubMed
141.Goedert, M, Hunt, SP, Mantyh, PW, et al. The ontogenetic development of neurotension-like immunoreactivity and neurotensin receptors in the cat striatum. Dev Brain Res 1985; 20: 127–131.CrossRefGoogle Scholar
142.Butcher, LL, Hodge, GK.Postnatal development of acetylchol inesterase in the caudate-putamen and substantia nigra of rats. Brain Res 1976; 106: 223–240.CrossRefGoogle Scholar
143.Graybiel, AM, Ragsdale, CW Jr.Clumping of acetylcholinesterase activity in the developing striatum of the human fetus and young infant. Proc Natl Acad Sci 1980; 77: 1214–1218.CrossRefGoogle ScholarPubMed
144.Graybiel, AM.Correspondence between the dopamine islands and striosomes of the mammalian striatum. Neurosci 1984a; 13: 1157–1187.CrossRefGoogle ScholarPubMed
145.Graybiel, AM, Hickey, TL.Chemospecificity of ontogenetic units in the striatum: Demonstration by combining [3H] thymidine autoradiography and histochemical staining. Proc Natl Acad Sci 1982; 79: 198–202.CrossRefGoogle ScholarPubMed
146.Van der Kooy, D, Fishell, G.Neuronal birthdate underlies the development of striatal compartments. Brain Res 1987; 401: 155–161.CrossRefGoogle ScholarPubMed
147.Marchand, R, Lajoie, L.Histogenesis of the striopallidal system in the rat. Neurogenesis of its neurons. Neurosci 1986; 17:573–590.CrossRefGoogle ScholarPubMed
148.Van der Kooy, D.Development relationships between opiate receptors and dopamine in the formation of caudate-putamen patches. Dev Brain Res 1984; 14: 300–303.CrossRefGoogle Scholar
149.Hubel, DH, Wiesel, TN.Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol (Lond) 1962; 160: 106–154.CrossRefGoogle ScholarPubMed
150.Woolsey, TA, Van Der Loos, H.The structural organisation of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 1970; 17: 205–242.CrossRefGoogle Scholar
151.Heimer, L, Wilson, RD.The subcortical projections of the allocortex: Similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. Golgi Cent Symp Proc 1975: 177–193.Google Scholar
152.Penny, GR, Wilson, CJ, Kitai, ST.The influence of neostriatal patch and matrix compartments on the dendritic geometry of spiny projection neurons in the rat as revealed by intracellular labeling with HRP combined with immunocytochemistry. Soc Neurosci Abstr 1984; 10: 514.Google Scholar