Distribution of tyrosine hydroxylase-expressing interneurons with respect to anatomical organization of the neostriatum

Frontiers in Systems Neuroscience

Volumn , Issue JUNE 2011, 2011, Pages

  Ünal, Bengi ^a   Ibáñez Sandoval, Osvaldo ^a   Shah, Fulva ^a   Abercrombie, Elizabeth D ^a   Tepper, James M ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

Dopamine island; GABAergic; Matrix; Striatum; Striosome

Indexed keywords

GREEN FLUORESCENT PROTEIN; MU OPIATE RECEPTOR; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL COMPARTMENTALIZATION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME LOCALIZATION; EXTRACELLULAR MATRIX; FLUORESCENCE ANALYSIS; IMMUNOFLUORESCENCE TEST; INTERNEURON; MOUSE; NEOSTRIATUM; NEUROANATOMY; NONHUMAN; PROTEIN EXPRESSION;

EID: 84856140879     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2011.00041     Document Type: Article

References (80)

1. Albin, R. L., Young, A. B., and Penney, J. B. (1989). The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366-375.
2. Arlotta, P., Molyneaux, B. J., Jabaudon, D., Yoshida, Y., and Macklis, J. D. (2008). Ctip2 controls the differentiation of medium spiny neurons and the estab-lishment of the cellular architecture of the striatum. J. Neurosci. 28, 622-632.
3. Berendse, H. W., Voorn, P., te Kortschot, A., and Groenewegen, H. J. (1988). Nuclear origin of thalamic afferents of the ventral striatum determines their relation to patch/matrix configura-tions in enkephalin-immunoreactivity in the rat. J. Chem. Neuroanat. 1, 3-10.
4. Bernácer, J., Prensa, L., and Giménez-Amaya, J. M. (2005). Morphological features, distribution and compart-mental organization of the nicotina-mide adenine dinucleotide phosphate reduced-diaphorase interneurons in the human striatum. J. Comp. Neurol. 489, 311-327.
5. Bernácer, J., Prensa, L., and Giménez-Amaya, J. M. (2007). Cholinergic interneurons are differentially dis-tributed in the human striatum. PLoS ONE 2, e1174. doi: 10.1371/journal. pone.0001174
6. Betarbet, R., Turner, R., Chockkan, V., DeLong, M. R., Allers, K. A., Walters, J., Levey, A. I., and Greenamyre, J. T. (1997). Dopaminergic neurons intrin-sic to the primate striatum. J. Neurosci. 17, 6761-6768.
7. Bolam, J. P., Izzo, P. N., and Graybiel, A. M. (1988). Cellular substrate of the histo-chemically defined striosome/matrix system of the caudate nucleus: a com-bined Golgi and immunocytochemi-cal study in cat and ferret. Neuroscience 24, 853-875.
8. Brown, L. L., Feldman, S. M., Smith, D. M., Cavanaugh, J. R., Ackermann, R. F., and Graybiel, A. M. (2002). Differential metabolic activity in the striosome and matrix compartments of the rat striatum during natural behaviors. J. Neurosci. 22, 305-314.
9. Busceti, C. L., Biagioni, F., Mastroiacovo, F., Bucci, D., Lenzi, P., Pasquali, L., Trabucco, A., Nicoletti, F., and Fornai, F. (2008). High number of striatal dopaminergic neurons during early postnatal development: correlation analysis with dopaminergic fibers. J. Neural Trans. 115, 1375-1383.
10. Chesselet, M. F., and Graybiel, A. M. (1986). Striatal neurons expressing somatostatin-like immunoreactivity: evidence for a peptidergic interneu-ronal system in the cat. Neuroscience 17, 547-571.
11. Cosette, M., Levesque, D., and Parent, A. (2005a). Neurochemical characteriza-tion of dopaminergic neurons in the human striatum. Parkinsonism Relat. Disord. 11, 277-286.
12. Cosette, M., Lecomte, F., and Parent, A. (2005b). Morphology and distribu-tion of dopaminergic neurons intrin-sic to the human striatum. J. Chem. Neuroanat. 29, 1-11.
13. Cowan, R. L., Wilson, C. J., Emson, P. C., and Heizmann, C. W. (1990). Parvalbumin-containing GABAergic interneurons in the rat neostriatum. J. Comp. Neurol. 302, 197-205.
14. Dubach, M., Schmidt, R., Kunkel, D., Bowden, D. M., Martin, R., and German, D. C. (1987). Primate neostriatal neurons con-taining tyrosine hydroxylase: immunohistochemical evidence. Neurosci. Lett. 75, 205-210.
15. Franklin, K. B. J., and Paxinos, G. (2001). The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
16. Gerfen, C. R. (1989). The neostriatal mosaic: striatal patch-matrix organi-zation is related to cortical lamination. Science 246, 385-388.
17. Gerfen, C. R. (1992). The neostriatal mosaic: multiple levels of compart-mental organization. Trends Neurosci. 15, 133-139.
18. Gerfen, C. R., Baimbridge, K. G., and Miller, J. J. (1985). The neostriatal mosaic: compartmental distribu-tion of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc. Natl. Acad. Sci. U.S.A. 82, 8780-8784.
19. Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, F. J. Jr., and Sibley, D. R. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432.
20. Gerfen, C. R., and Wilson, C. J. (1996). "The basal ganglia," in Handbook of Chemical Neuroanatomy, Vol. 12, Integrated Systems of the CNS, Part III, eds L. W. Swanson, A. Björklund, and T. Hökfelt (Amsterdam: Elsevier), 371-468.
21. Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., and Heintz, N. (2003). A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425, 917-925.
22. Granado, N., Ares-Santos, S., O'Shea, E., Vicario-Abejon, C., Colado, M. I., and Moratalla, R. (2010). Selective vulnerability in striosomes and in the nigrostriatal dopaminergic pathway after methamphetamine administra-tion: early loss of TH in striosomes after methamphetamine. Neurotox. Res. 18, 48-58.
23. Graybiel, A. M., Hirsch, E. C., and Agid, Y. A. (1987). Differences in tyrosine hydroxylase-like immunoreactivity characterize the mesostriatal innerva-tion of striosomes and extrastriosomal matrix at maturity. Proc. Natl. Acad. Sci. U.S.A. 84, 303-307.
24. Graybiel, A. M., Pickel, V. M., Joh, T. H., Reis, D. J., and Ragsdale, C. W. (1981). Direct demonstration of a correspond-ence between the dopamine islands and acetylcholinesterase patches in the developing striatum. Proc. Natl. Acad. Sci. U.S.A. 78, 5871-5875.
25. Hamasaki, T., Goto, S., Nishikawa, S., and Ushio, Y. (2001). A role of netrin-1 in the formation of subcortical struc-ture striatum: repulsive action on the migration of late-born striatal neu-rons. J. Neurosci. 21, 4272-4280.
26. Heimer, L., Alheid, G. F., de Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., and Zahm, D. S. (1997). The accumbens: beyond the core-shell dichotomy. J. Neuropsychiatry Clin. Neurosci. 9, 354-381.
27. Henny, F., and Jones, B. E. (2008). Projections from basal forebrain to prefrontal cortex comprise cholinergic, GABAergic and glutamatergic inputs to pyramidal cells or interneurons. Eur. J. Neurosci. 27, 654-670.
28. Herkenham, M., and Pert, C. B. (1981). Mosaic distribution of opiate recep-Ünal tors, parafascicular projections and acetylcholinesterase in the striatum. Nature 291, 415-418.
29. Holt, D. J., Graybiel, A. M., and Saper, C. B. (1997). Neurochemical architecture of the human striatum. J. Comp. Neurol. 384, 1-25.
30. Huot, P., Levesque, M., and Parent, A. (2007). The fate of striatal dopamin-ergic neurons in Parkinson's disease and Huntington's chorea. Brain 130, 222-232.
31. Huot, P., and Parent, A. (2007). Dopaminergic neurons intrinsic to the striatum. J. Neurochem. 101, 1441-1447.
32. Ibáñez-Sandoval, O., Tecuapetla, F., Unal, B., Shah, F., Koós, T., and Tepper, J. M. (2010). Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J. Neurosci. 30, 6999-7016.
33. Ikemoto, S. (2007). Dopamine reward- circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle com-plex. Brain Res. Rev. 56, 27-78.
34. Janis, L. S., Cassidy, R. M., and Kromer, L. F. (1999). Ephrin-A binding and EphA receptor expression delineate the matrix compartment of the stria-tum. J. Neurosci. 19, 4962-4971.
35. Jollivet, C., Montero-Menei, C. N., Venier-Julienne, M. C., Sapin, A., Benoit, J. P., and Menei, P. (2004). Striatal tyrosine hydroxylase immu-noreactive neurons are induced by L-dihydroxyphenylalanine and nerve growth factor treatment in 6-hydroxy-dopamine lesioned rats. Neurosci. Lett. 362, 79-82.
36. Jongen-Relo, A., Groenewegen, H. J., and Voorn, P. (1993). Evidence for multi- compartmental histochemical organi-zation of the nucleus accumbens in the rat. J. Comp. Neurol. 337, 267-276.
37. Jongen-Relo, A. L., Voorn, P., and Groenewegen, H. J. (1994). Immunohistochemical characteriza-tion of the shell and core territories of the nucleus accumbens in the rat. Eur. J. Neurosci. 6, 1255-1264.
38. Kawaguchi, Y. (1992). Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J. Neurophysiol. 67, 1669-1682.
39. Kawaguchi, Y. (1993). Physiological, morphological and histochemical characterization of three classes of interneurons in the neostriatum. J. Neurosci. 13, 4908-4923.
40. Kawaguchi, Y., Wilson, C. J., Augood, S. J., and Emson, P. C. (1995). Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 18, 527-535.
41. Kawaguchi, Y., Wilson, C. J., and Emson, P. C. (1990). Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci. 10, 3421-3438.
42. Kita, H. (2001). Neostriatal and glo-bus pallidus stimulation induced inhibitory postsynaptic potentials in entopeduncular neurons in rat brain slice preparations. Neuroscience 105, 871-879.
43. Kita, H., Chiken, S., Tachibana, Y., and Nambu, A. (2006). Origins of GABA(A) and GABA(B) receptor- mediated responses of the globus pal-lidus induced after stimulation of the putamen in the monkey. J. Neurosci. 26, 6554-6562.
44. Kubota, Y., and Kawaguchi, Y. (1993). Spatial distributions of chemically identified intrinsic neurons in relation to patch and matrix compartments of rat neostriatum. J. Comp. Neurol. 332, 499-513.
45. Lawhorn, C., Smith, D. M., and Brown, L. L. (2008). Striosome-matrix pathol-ogy and motor deficits in the YAC 128 mouse model of Huntington's disease. Neurobiol. Dis. 32, 471-478.
46. Liao, L., Tsai, H., Wang, H., Chang, J., Lu, K., Wu, H., and Lee, Y. (2008). Modular patterning of structure and function of the striatum by retinoid receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 6765-6770.
47. Lopez-Real, A., Rodriguez-Pallares, J., Guerra, M. H., and Labandeira-Garcia, J. L. (2003). Localization and functional significance of striatal neurons immunoreactive to aromatic L-amino acid decarboxylase or tyros-ine hydroxylase in rat parkinsonian models. Brain Res. 969, 135-146.
48. Mao, L., Lau, Y. S., Petroske, E., and Wang, J. Q. (2001). Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration. Brain Res. Dev. Brain Res. 131, 57-65.
49. Martone, M. E., Young, S. J., Armstrong, D. M., and Groves, P. M. (1994). The dis-tribution of cholinergic perikarya with respect to enkephalin-rich patches in the caudate nucleus of the adult cat. J. Chem. Neuroanat. 8, 47-59.
50. Mason, H. A., Rakowiecki, S. M., Raftopoulou, M., Nery, S., Huang, Y., Gridley, T., and Fishell, G. (2005). Notch signaling coordinates the pattern of striatal compartments. Development 132, 4247-4258.
51. Mazloom, M., and Smith, Y. (2006). Synaptic microcircuitry of tyrosine hydroxylase-containing neurons and terminals in the striatum of 1-Methyl- 4-Phenyl-1,2,3,6-Tetrahydropyridine treated monkeys. J. Comp. Neurol. 495, 453-469.
52. Meredith, G. E., Farrell, T., Kellaghan, P., Tan, Y., Zahm, D. S., and Toterdell, S. (1999). Immunocytochemical char-acterization of catecholaminergic neurons in the rat striatum following dopamine-depleting lesions. Eur. J. Neurosci. 11, 3583-3596.
53. Mikula, S., Parrish, S. K., Trimmer, J. S., and Jones, E. G. (2009). Complete 3D visualization of primate striosomes by KChIP1 immunostaining. J. Comp. Neurol. 514, 507-517.
54. Miura, M., Masada, M., and Aosaki, T. (2008). Roles of micro-opioid recep-tors in GABAergic synaptic trans-mission in the striosome and matrix compartments of the striatum. Mol. Neurobiol. 37, 104-115.
55. Miura, M., Saino-Saito, S., Masuda, M., Kobayashi, K., and Aosaki, T. (2007). Compartment-specific modulation of GABAergic synaptic transmission by μ-opioid receptor in the mouse striatum with green fluorescent protein-expressing dopamine islands. J. Neurosci. 27, 9721-9728.
56. Mura, A., Jackson, D., Manley, M. S., Young, S. J., and Groves, P. M. (1995). Aromatic L-amino acid decarboxylase immunoreactive cells in the rat stria-tum: a possible site for the conversion of exogenous L-DOPA to dopamine. Brain Res. 704, 51-60.
57. Mura, A., Linder, J. C., Young, S. J., and Groves, P. M. (2000). Striatal cells containing aromatic L-amino acid decarboxylase: an immunohistochem-ical comparison with other classes of striatal neurons. Neuroscience 98, 501-511.
58. Oorschot, D. E. (2010). "Cell types in the different nuclei of the basal ganglia," in Handbook of Basal Ganglia Structure and Function, eds H. Steiner and K. Y. Tseng (San Diego, CA: Academic Press), 63-91.
59. Palfi, S., Leventhal, L., Chu, Y., Ma, S. Y., Emborg, M., Bakay, R., Deglon, N., Hantraye, P., Aebischer, P., and Kordower, J. H. (2002). Lentivirally delivered glial cell line-derived neuro-trophic factor increases the number of striatal dopaminergic neurons in pri-mate models of nigrostriatal degenera-tion. J. Neurosci. 22, 4942-4954.
60. Prasad, K., and Richfield, E. K. (2010). Number and nuclear morphology of TH+ and TH- neurons in the mouse ventral midbrain using epifluores-cence stereology. Exp. Neurol. 225, 328-340.
61. Ragsdale, C. W., and Graybiel, A. M. (1981). The fronto-striatal projec-tion in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry. Brain Res. 208, 259-266.
62. Redies, C., Kovjanic, D., Heyers, D., Medina, L., Hirano, S., Suzuki, S. T., and Puelles, L. (2002). Patch/matrix patterns of gray matter differentia-tion in telencephalon of chicken and mouse. Brain Res. Bull. 57, 489-493.
63. Rivera, A., Cuellar, B., Giron, F. J., Grandy, D. K., de la Calle, A., and Moratalla, R. (2002). Dopamine D4 receptors are heterogeneously distributed in the stri-osomes/matrix compartments of the striatum. J. Neurochem. 80, 219-229.
64. Rodriguez, M., Morales, I., Gomez, I., Gonzalez, S., Gonzalez-Hernandez, T., and Gonzalez-Mora, J. L. (2006). Heterogeneous dopamine neu-rochemistry in the striatum: the fountain-drain matrix. J. Pharmacol. Exp. Ther. 19, 31-43.
65. Rymar, V. V., Sasseville, R., Luk, K. C., and Sadikot, A. F. (2004). Neurogenesis and stereological morphometry of cal-retinin immunoreactive GABAergic interneurons of the neostriatum. J. Comp. Neurol. 469, 325-339.
66. Sadikot, A. F., and Sasseville, R. (1997). Neurogenesis in the mammalian neostriatum and nucleus accum-bens: parvalbumin-immunoreactive GABAergic interneurons. J. Comp. Neurol. 389, 193-211.
67. Saka, E., Iadarola, M., Fitzgerald, D. J., and Graybiel, A. M. (2002). Local cir-cuit neurons in the striatum regulate neural and behavioral responses to dopaminergic stimulation. Proc. Natl. Acad. Sci. U.S.A. 99, 9004-9009.
68. Sako, W., Morigaki, R., Nagahiro, S., Kaji, R., and Goto, S. (2010). Olfactory type G protein alpha subunit in striosome- matrix dopamine systems in adult mice. Neuroscience 170, 497-502.
69. Sato, K., Sumi-Ichinose, C., Kaji, R., Ikemoto, K., Nomura, T., Nagatsu, I., Ichinose, H., Ito, M., Sako, W., Nagahiro, S., Graybiel, A. M., and Goto, S. (2008). Differential involve-ment of striosome and matrix dopa-mine systems in a transgenic model of dopa-responsive dystonia. Proc. Natl. Acad. Sci. U.S.A. 105, 12551-12556.
70. Schatzmiller, R. A., Goldman, J. S., Simard-Emond, L., Rymar, V., Manitt, C., Sadikot, A. F., and Kennedy, T. E. (2008). Graded expression of netrin-1 by specific neuronal subtypes in the adult mammalian striatum. Neuroscience 157, 621-636.
71. Tande, D., Hoglinger, G., Debeir, T., Freundlieb, N., Hirsch, E. C., and Francois, C. (2006). New striatal dopamine neu-rons in MPTP-treated macaques result from a phenotypic shift and not neuro-genesis. Brain 129, 1194-1200.
72. Tashiro, Y., Sugimoto, T., Hattori, T., Uemura, Y., Nagatsu, I., Kikuchi, H., and Mizuno, N. (1989a). Tyrosine hydroxylase-like immunoreactive neurons in the striatum of the rat. Neurosci. Lett. 97, 6-10.
73. Tashiro, Y., Kaneko, T., Sugimoto, T., Nagatsu, I., Kikuchi, H., and Mizuno, N. (1989b). Striatal neurons with aro-matic L-amino acid decarboxylase-like immunoreactivity in the rat. Neurosci. Lett. 100, 29-34.
74. Tepper, J. M. (2010). "GABAergic interneurons of the striatum," in Handbook of Basal Ganglia Structure and Function, eds H. Steiner and K. Y. Tseng (San Diego, CA: Academic Press), 151-163.
75. van Vulpen, E. H., and van der Kooy, D. (1998). Striatal cholinergic interneu-rons: birthdates predict compartmen-tal localization. Brain Res. Dev. Brain Res. 109, 51-58.
76. Voorn, P., Gerfen, C. R., and Groenewegen, H. J. (1989). Compartmental organi-zation of the ventral striatum of the rat: immunohistochemical distribu-tion of enkephalin, substance P, dopa-mine and calcium binding protein. J. Comp. Neurol. 289, 189-201.
77. Voorn, P., Vanderschuren, L. E., and Groenewegen, H. J. (2004). Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 27, 468-474.
78. Wightman, R. M., Heien, M. L., Wassum, K. M., Sombers, L. A., Aragona, B. J., Khan, A. S., Ariansen, J. L., Cheer, J. F., Phillips, P. E., and Carelli, R. M. (2007). Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens. Eur. J. Neurosci. 26, 2046-2054
79. Wu, Y., and Parent, A. (2000). Striatal interneurons expressing calretinin, parvalbumin and NADPH-diaphorase: a comparative study in the rat, monkey and human. Brain Res. 863, 182-191.
80. Zaborszky, L., Alheid, G. F., Beinfeld, M. C., Eiden, L. E., Heimer, L., and Palkovita, M. (1985). Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunolog-ical study. Neuroscience 14, 427-453.