Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum

Frontiers in Neural Circuits

Volumn , Issue JUL, 2013, Pages

  Gangarossa, Giuseppe ^a,b   Espallergues, Julie ^a,b   Mailly, Philippe ^c   De Bundel, Dimitri ^a,b   de Kerchove d'Exaerde, Alban ^d   Hervé, Denis ^e,f   Girault, Jean Antoine ^e,f   Valjent, Emmanuel ^a,b   Krieger, Patrik ^g  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c CNRS   (France)

^d UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^e INSTITUT DU FER À MOULIN   (France)

^f SORBONNE UNIVERSITÉ   (France)

^g KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Adenosine a2a receptor; BAC transgenic mice; Dopamine D1 and D2 receptors; Medium sized spiny neurons

Indexed keywords

ADENOSINE A2 RECEPTOR; CALBINDIN; CALRETININ; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; IBOTENIC ACID; NEURON SPECIFIC NUCLEAR PROTEIN; PARVALBUMIN; PREPROENDOTHELIN; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL CELL; ARTICLE; BRAIN REGION; CELL DENSITY; CONTROLLED STUDY; CORPUS STRIATUM; CYTOARCHITECTURE; GABAERGIC SYSTEM; HEMISPHERE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; LATERAL GENICULATE BODY; MALE; MOUSE; NERVE CELL; NEUROCHEMISTRY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NORADRENERGIC NERVE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; ROSTRO CAUDAL AXIS; SPINY NERVE CELL; THALAMUS NUCLEUS; TISSUE PREPARATION;

EID: 84879963587     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2013.00124     Document Type: Article

References (69)

1. Ballion, B., Mallet, N., Bezard, E., Lanciego, J.L., and Gonon, F. (2008). Intratelencephalic corticostriatal neurons equally excite striatonigral and striatopallidal neurons and their discharge activity is selectively reduced in experimental parkinsonism. Eur J Neurosci 27, 2313-2321.
2. Bertran-Gonzalez, J., Bosch, C., Maroteaux, M., Matamales, M., Hervé, D., Valjent, E., and Girault, J.A. (2008). Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28, 5671-5685.
3. Bertran-Gonzalez, J., Hervé, D., Girault, J.A., and Valjent, E. (2010). What is the degree of segregation between striatonigral and striatopallidal projections? Front Neuroanat 4, 136.
4. Bolam, J.P., Hanley, J.J., Booth, P.A., and Bevan, M.D. (2000). Synaptic organisation of the basal ganglia. J Anat 196 (Pt 4), 527-542.
5. Crittenden, J.R., and Graybiel A.M. (2011). Basal Ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front Neuroanat 5, 59.
6. Davis, M.I., and Puhl H. L. 3rd (2011). Nr4a1-eGFP is a marker of striosome-matrix architecture, development and activity in the extended striatum. PLoS One 6,e16619.
7. Diggle, P.J. (2003). Statistical Analysis of Spatial Point Patterns. Hodder Education Publishers, London.
8. Durieux, P.F., Bearzatto, B., Guiducci, S., Buch, T., Waisman, A., Zoli, M., Schiffmann, S.N., and De Kerchove D'exaerde, A. (2009). D2R striatopallidal neurons inhibit both locomotor and drug reward processes. Nat Neurosci 12, 393-395.
9. Durieux, P.F., Schiffmann, S.N., and De Kerchove D'exaerde, A. (2011). Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J 31, 640-653.
10. Eglen, S.J., Diggle, P.J., and Troy, J.B. (2005). Homotypic constraints dominate positioning of on- and off-center beta retinal ganglion cells. Vis Neurosci 22, 859-871.
11. Eglen, S.J., and Wong, J.C. (2008). Spatial constraints underlying the retinal mosaics of two types of horizontal cells in cat and macaque. Vis Neurosci 25, 209-214.
12. Ena, S.L., De Backer J.F., Schiffmann, S.N., and de Kerchove D'exaerde, A. (2013). FACS Array Profiling Identifies Ecto-5' Nucleotidase as a Striatopallidal Neuron-Specific Gene Involved in Striatal-Dependent Learning. J Neurosci. 33, 8794-8809.
13. Franklin, K., and Paxinos, G. (2007). The Mouse Brain in Stereotaxic Coordinates. 360.
14. Frazer, A. (2000). Norepinephrine involvement in antidepressant action. J Clin Psychiatry. 61, 25-30.
15. Fremeau, R.T. Jr., Voglmaier, S., Seal, R.P. and Edwards, R.H. (2004). VGlUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27, 98-103.
16. Fulceri, F., Biagioni, F., Lenzi, P., Falleni, A., Gesi, M., Ruggieri, S., Fornai, F. (2006). Nigrostriatal damage with 6-OHDA: validation of routinely applied procedures. Ann N Y Acad Sci. 1074, 344-348.
17. Gangarossa, G., Perroy, J., and Valjent, E. (2013a). Combinatorial topography and cell-type specific regulation of the ERK pathway by dopaminergic agonists in the mouse striatum. Brain Struct Funct. 218,405-419.
18. Gangarossa, G., Espallergues, J., de Kerchove d'Exaerde, A., El Mestikawy, S., Gerfen, C.R., Hervé, D., Girault, J.A., and Valjent, E. (2013b). Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens. Front Neural Circuits 7, 22.
19. Gerfen, C.R. (1989). The neostriatal mosaic: striatal patch-matrix organization is related to cortical lamination. Science 246, 385-388.
20. 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.
21. Gerfen, C.R., and Surmeier, D.J. (2011). Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34, 441-466.
22. Gerfen, C.R., and Young, W.S., 3rd (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.
23. Gertler, T.S., Chan, C.S., and Surmeier, D.J. (2008). Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 28, 10814-10824.
24. Gittis, A.H., and Kreitzer, A.C. (2012). Striatal microcircuitry and movement disorders. Trends Neurosci 9,557-564.
25. Goldman-Rakic, P.S. (1982). Cytoarchitectonic heterogeneity of the primate neostriatum: subdivision into Island and Matrix cellular compartments. J Comp Neurol 205, 398-413.
26. Gong, S., Doughty, M.L., Harbaugh, C.R., Cummins, A., Hatten, M.E., Heintz, N., and Gerfen, C.R. (2007). Targeting CRE recombinase to specific neurons populations with bacterial Artificial Chromosome constructs. J Neurosci 27, 9817-9823.
27. Graybiel, A.M. (1984). Neurochemically specified subsystems in the basal ganglia. Ciba Found Symp 107, 114-149.
28. Graybiel, A.M., and Chesselet, M.F. (1984). Compartmental distribution of striatal cell bodies expressing [Met]enkephalin-like immunoreactivity. Proc Natl Acad Sci U S A 81, 7980-7984.
29. Graybiel, A.M. (2004). Network-level neuroplasticity in cortico-basal ganglia pathways. Parkinsonism Relat Disord 10, 293-296.
30. Groh, A., Meyer, H.S., Schmidt, E.F., Heintz, N., Skamann, B., and Krieger, P. (2010). Celltype specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb Cortex 20, 826-836.
31. Haber, S.N., Kim, K.S., Mailly, P., and Calzavara, R. (2006). Reward-related cortical inputs define a large striatal region in primates that interface with associative cortical connections, providing a substrate for incentive-based learning. J Neurosci 26, 8368-8376.
32. Hansson, K., Jafari-Mamaghani, M., and Krieger, P. (2013). RipleyGUI:software for analyzing spatial patterns in 3D cell distribution. Front Neuroinform 7, 5.
33. Hardman, C.D., Henderson, J.M., Finkelstein, D.I., Horne, M.K., Paxinos, G., and Halliday, G.M. (2002). Comparison of the basal ganglia in rats, marmosets, macaques, baboons, and humans: volume and neuronal number for the output, internal relay, and striatal modulating nuclei. J Comp Neurol 445, 238-255.
34. Heiman, M., Schaefer, A., Gong, S., Peterson, J.D., Day, M., Ramsey, K.E., Suàrez-Fariña, M., Schwarz, C., Stephan, D.A., Surmeier, D.J., Greengard, P., and Heintz, N. (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748.
35. Herkenham, M., and Pert, C.B (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature. 291, 415-418.
36. Hervé, D., Le Moine, C., Corvol, J.C., Belluscio, L., Ledent, C., Fienberg, A.A., Jaber, M., Studler, J.M., and Girault, J.A. (2001). Galpha(olf) levels are regulated by receptor usage and control dopamine and adenosine action in the striatum. J Neurosci 21, 4390-4399.
37. Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D.R., and Arber, S. (2005). A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3, e159.
38. Jafari-Mamaghani, M., Andersson, M., and Krieger, P. (2010). Spatial Point Pattern Analysis of Neurons Using Ripley's K-Function in 3D. Front Neuroinform 4, 9.
39. Kawaguchi, Y. (1993). Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13, 4908-4923.
40. Kawaguchi, Y. (1997). Neostriatal cell subtypes and their functional roles. Neurosci Res 1,1-8.
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. Koshimizu, Y., Wu, S.X., Unzai, T., Hioki, H., Sonomura, T., Nakamura, K.C., Fujiyama, F., Kaneko, T. (2008). Paucity of enkephalin production in neostriatal striosomal neurons: analysis with preproenkephalin-green fluorescent protein transgenic mice. Eur J Neurosci 28, 2053-2064.
43. Kravitz, A.V., Freeze, B.S., Parker, P.R., Kay, K., Thwin, M.T., Deisseroth, K., and Kreitzer, A.C. (2010). Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466, 622-626.
44. Kremer, J.R., Mastronarde, D.N., and Mcintosh, J.R. (1996). Computer visualization of threedimensional image data using IMOD. J Struct Biol 116, 71-76.
45. Lanca, A.J., Boyd, S., Kolb, B.E., and Van Der Kooy, D. (1986). The development of a patchy organization of the rat striatum. Brain Res 392, 1-10.
46. Ledoux, J.E., Farb, C.R., and Romanski, L.M. (1991). Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci Lett 134, 139-144.
47. Lee, K.S., Schubert, P., Reddington, M., and Kreutzberg, G.W. (1986). The distribution of adenosine A1 receptors and 5'-nucleotidase in the hippocampal formation of several mammalian species. J Comp Neurol 246, 427-434.
48. Lei, W., Jiao, Y., Del Mar, N., and Reiner, A. (2004). Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci 24, 8289-8299.
49. Levesque, M., Bedard, A., Cossette, M., and Parent, A. (2003). Novel aspects of the chemical anatomy of the striatum and its efferents projections. J Chem Neuroanat 26, 271-281.
50. Liu, F.C., and Graybiel, A.M. (1992) Heterogeneous development of calbindin-D28K expression in the striatal matrix. J Comp Neurol 320, 304-322.
51. Mailly, P., Haber, S.N., Groenewegen, H.J., and Deniau, J.M. (2009). A 3D multi-modal and multi-dimensional digital brain model as a framework for data sharing. J Neurosci Methods 194, 56-63.
52. Mailly, P., Haber, S.N., Groenewegen, H.J., and Deniau, J.M. (2010). A 3D multi-modal and multi-dimensional digital brain model as a framework for data sharing. J Neurosci Methods 194, 56-63.
53. Matamales, M., Bertran-Gonzalez, J., Salomon, L., Degos, B., Deniau, J.M., Valjent, E., Hervé, D., and Girault, J.A. (2009). Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS One 4, e4770.
54. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V.H., Butt, S.J., Battiste, J., Johnson, J.E., Machold, R.P., and Fishell, G. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30, 1582-1594.
55. Nicola, S.M. (2007). The nucleus accumbens as part of a basal ganglia action selection circuit. Psychopharmacology (Berl) 191, 521-550.
56. Reiner, A., Hart, N.M., Lei, W., and Deng, Y. (2010). Corticostriatal projection neurons - dichotomous types and dichotomous functions. Front Neuroanat 4, 142.
57. Reiner, A., Jiao, Y., Del Mar, N., Laverghetta, A.V., and Lei, W.L. (2003). Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457, 420-440.
58. Ripley, B.D. (1988). Statistical Interference for Spatial Processes. Cambridge University Press, Cambridge.
59. Sako, W., Morigaki, R., Nagahiro, S., Kaji, R., and Goto, S. (2010). Olfactory type G-protein α subunit in striosome-matrix dopamine systems in adult mice. Neuroscience 170,497-502.
60. Schoen, S.W., and Graybiel, A.M. (1993). Species-specific patterns of glycoprotein expression in the developing rodent caudoputamen: association of 5'-nucleotidase activity with dopamine islands and striosomes in rat, but with extrastriosomal matrix in mouse. J Comp Neurol 333, 578-596.
61. Selemon, L.D., and Goldman-Rakic, P.S. (1985). Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5, 776-794.
62. Shepherd, G.M. (2013). Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 14, 278-291.
63. Shu, S.Y., Bao, X., Li S., Niu D., Xu Z., and Li Y. (1999). A new subdivision of mammalian neostriatum with functional implications to learning and memory. J Neurosci Res 58, 242-253.
64. Shu, S.Y., McGinty, J.F., and Peterson, G.M. (1990). High density of zinc-containing and dynorphin B- and substance P-immunoreactive terminals in the marginal division of the rat striatum. Brain Res Bull 24, 201-205.
65. Shu, S.Y., Penny, G.R., and Peterson, G.M. (1988). The 'marginal division': a new subdivision in the neostriatum of the rat. J Chem Neuroanat 1, 147-163.
66. Srinivas, S., Watanabe, T., Lin, C.S., William, C.M., Tanabe, Y., Jessell, T.M., and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1, 4.
67. Tepper, J.M., Tecuapetla, F., Koos T., Ibanez-Sandoval, O. (2010). Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4,150.
68. Valjent, E., Bertran-Gonzalez, J., Hervé, D., Fisone, G., and Girault, J.A. (2009). Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci 32, 538-547.
69. Wu, Y., Richard, S., and Parent, A. (2000). The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci Res 38, 49-62.