Patterned expression of a cocaine- and amphetamine-regulated transcript peptide reveals complex circuit topography in the rodent cerebellar cortex

Journal of Comparative Neurology

Volumn 519, Issue 9, 2011, Pages 1781-1796

  Reeber, Stacey L ^a   Sillitoe, Roy V ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Afferent fibers; Compartmentalization; Connectivity; HSP25; ZebrinII

Indexed keywords

ALDOLASE C; COCAINE AND AMPHETAMINE REGULATED TRANSCRIPT PEPTIDE; HEAT SHOCK PROTEIN 25; PEPTIDE; UNCLASSIFIED DRUG; ZEBRIN II;

ADULT ANIMAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CEREBELLAR MOSSY FIBER; CEREBELLUM CORTEX; CLIMBING FIBER; CONTROLLED STUDY; DENDRITE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; RAT; RODENT; SENSORIMOTOR CORTEX; SENSORY NERVE;

AFFERENT PATHWAYS; ANIMALS; AXONS; BODY PATTERNING; BRAIN MAPPING; CELL COMPARTMENTATION; CEREBELLAR CORTEX; FEMALE; MALE; MICE; NERVE FIBERS; NERVE TISSUE PROTEINS; RATS; SPECIES SPECIFICITY;

EID: 79955087436     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22601     Document Type: Article

References (67)

1. Abbott LC, Sotelo C. 2000. Ultrastructural analysis of catecholaminergic innervation in weaver and normal mouse cerebellar cortices. J Comp Neurol 426: 316-329.
2. Ahn AH, Dziennis S, Hawkes R, Herrup K. 1994. The cloning of zebrin II reveals its identity with aldolase C. Development 120: 2081-2090.
3. Akintunde A, Eisenman LM. 1994. External cuneocerebellar projection and Purkinje cell zebrin II bands: a direct comparison of parasagittal banding in the mouse cerebellum. J Chem Neuroanat 7: 75-86.
4. Apps R, Hawkes R. 2009. Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci 10: 670-681.
5. Armstrong CL, Hawkes R. 2000. Pattern formation in the cerebellar cortex. Biochem Cell Biol 78: 551-562.
6. Armstrong CL, Krueger-Naug AM, Currie RW, Hawkes R. 2000. Constitutive expression of the 25-kDa heat shock protein Hsp25 reveals novel parasagittal bands of purkinje cells in the adult mouse cerebellar cortex. J Comp Neurol 416: 383-397.
7. Armstrong CL, Krueger-Naug AM, Currie RW, Hawkes R. 2001. Constitutive expression of heat shock protein HSP25 in the central nervous system of the developing and adult mouse. J Comp Neurol 434: 262-274.
8. Armstrong CL, Chung SH, Armstrong JN, Hochgeschwender U, Jeong YG, Hawkes R. 2009. A novel somatostatin-immunoreactive mossy fiber pathway associated with HSP25-immunoreactive purkinje cell stripes in the mouse cerebellum. J Comp Neurol 517: 524-538.
9. Barmack NH, Baughman RW, Eckenstein FP. 1992. Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J Comp Neurol 317: 233-249.
10. Berretta S, Perciavalle V, Poppele RE. 1991. Origin of spinal projections to the anterior and posterior lobes of the rat cerebellum. J Comp Neurol 305: 273-281.
11. Brochu G, Maler L, Hawkes R. 1990. Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol 291: 538-552.
12. 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.
13. Demilly A, Reeber SL, Gebre SA, Sillitoe RV. 2010. Neurofilament heavy chain expression reveals a unique parasagittal stripe topography in the mouse cerebellum. Cerebellum (in press).
14. Dietrichs E. 1984. Cerebellar autonomic function: direct hypothalamocerebellar pathway. Science 223: 591-593.
15. Dominguez G, del Giudice EM, Kuhar MJ. 2004. CART peptide levels are altered by a mutation associated with obesity at codon 34. Mol Psychiatry 9: 1065-1066.
16. Douglass J, McKinzie AA, Couceyro P. 1995. PCR differential display identifies a rat brain mRNA that is transcriptionally regulated by cocaine and amphetamine. J Neurosci 15: 2471-2481.
17. Fujita H, Oh-Nishi A, Obayashi S, Sugihara I. 2010. Organization of the marmoset cerebellum in three-dimensional space: lobulation, aldolase C compartmentalization and axonal projection. J Comp Neurol 518: 1764-1791.
18. Gravel C, Hawkes R. 1990. Parasagittal organization of the rat cerebellar cortex: direct comparison of Purkinje cell compartments and the organization of the spinocerebellar projection. J Comp Neurol 291: 79-102.
19. Gravel C, Eisenman LM, Sasseville R, Hawkes R. 1987. Parasagittal organization of the rat cerebellar cortex: direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. J Comp Neurol 265: 294-310.
20. Hioki H, Fujiyama F, Taki K, Tomioka R, Furuta T, Tamamaki N, Kaneko T. 2003. Differential distribution of vesicular glutamate transporters in the rat cerebellar cortex. Neuroscience 117: 1-6.
21. Hisano S, Sawada K, Kawano M, Kanemoto M, Xiong G, Mogi K, Sakata-Haga H, Takeda J, Fukui Y, Nogami H. 2002. Expression of inorganic phosphate/vesicular glutamate transporters (BNPI/VGLUT1 and DNPI/VGLUT2) in the cerebellum and precerebellar nuclei of the rat. Brain Res Mol Brain Res 107: 23-31.
22. Iwaniuk AN, Marzban H, Pakan JM, Watanabe M, Hawkes R, Wylie DR. 2009. Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase C beta 4. J Chem Neuroanat 37: 55-63.
23. Jaarsma D, Ruigrok TJ, Caffe R, Cozzari C, Levey AI, Mugnaini E, Voogd J. 1997. Cholinergic innervation and receptors in the cerebellum. Prog Brain Res 114: 67-96.
24. Kim JY, Marzban H, Chung SH, Watanabe M, Eisenman LM, Hawkes R. 2009. Purkinje cell compartmentation of the cerebellum of microchiropteran bats. J Comp Neurol 517: 193-209.
25. Kimmel HL, Gong W, Vechia SD, Hunter RG, Kuhar MJ. 2000. Intra-ventral tegmental area injection of rat cocaine and amphetamine-regulated transcript peptide 55-102 induces locomotor activity and promotes conditioned place preference. J Pharmacol Exp Ther 294: 784-792.
26. Kimmel HL, Thim L, Kuhar MJ. 2002. Activity of various CART peptides in changing locomotor activity in the rat. Neuropeptides 36: 9-12.
27. Kitzman PH, Bishop GA. 1994. The origin of serotoninergic afferents to the cat's cerebellar nuclei. J Comp Neurol 340: 541-550.
28. 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.
29. Koylu EO, Balkan B, Kuhar MJ, Pogun S. 2006. Cocaine and amphetamine regulated transcript (CART) and the stress response. Peptides 27: 1956-1969.
30. Kuhar MJ, Yoho LL. 1999. CART peptide analysis by Western blotting. Synapse 33: 163-171.
31. Lannoo MJ, Brochu G, Maler L, Hawkes R. 1991. Zebrin II immunoreactivity in the rat and in the weakly electric teleost Eigenmannia (gymnotiformes) reveals three modes of Purkinje cell development. J Comp Neurol 310: 215-233.
32. Larouche M, Hawkes R. 2006. From clusters to stripes: the developmental origins of adult cerebellar compartmentation. Cerebellum 5: 77-88.
33. Marzban H, Hawkes R. 2010. On the architecture of the posterior zone of the cerebellum. Cerebellum (in press).
34. Marzban H, Kim CT, Doorn D, Chung SH, Hawkes R. 2008. A novel transverse expression domain in the mouse cerebellum revealed by a neurofilament-associated antigen. Neuroscience 153: 1190-1201.
35. Marzban H, Chung SH, Pezhouh MK, Feirabend H, Watanabe M, Voogd J, Hawkes R. 2010. Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticus). J Comp Neurol 518: 2221-2239.
36. Meek J, Hafmans TG, Maler L, Hawkes R. 1992. Distribution of zebrin II in the gigantocerebellum of the mormyrid fish Gnathonemus petersii compared with other teleosts. J Comp Neurol 316: 17-31.
37. Nelson TE, King JS, Bishop GA. 1997. Distribution of tyrosine hydroxylase-immunoreactive afferents to the cerebellum differs between species. J Comp Neurol 379: 443-454.
38. Olson L, Fuxe K. 1971. On the projections from the locus coeruleus noradrealine neurons: the cerebellar innervation. Brain Res 28: 165-171.
39. Ozol K, Hayden JM, Oberdick J, Hawkes R. 1999. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412: 95-111.
40. Pakan JM, Wylie DR. 2008. Congruence of zebrin II expression and functional zones defined by climbing fiber topography in the flocculus. Neuroscience 157: 57-69.
41. Pakan JM, Iwaniuk AN, Wylie DR, Hawkes R, Marzban H. 2007. Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia). J Comp Neurol 501: 619-630.
42. Pakan JM, Graham DJ, Wylie DR. 2010. Organization of visual mossy fiber projections and zebrin expression in the pigeon vestibulocerebellum. J Comp Neurol 518: 175-198.
43. Pijpers A, Apps R, Pardoe J, Voogd J, Ruigrok TJ. 2006. Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. J Neurosci 26: 12067-12080.
44. Press DA, Wall MJ. 2008. Expression of cocaine- and amphetamine-regulated transcript (CART) peptides at climbing fibre-Purkinje cell synapses in the rat vestibular cerebellum. Neuropeptides 42: 39-46.
45. Ramon y Cajal. 1911. Histologie du systeme nerveux de l'homme et des vertebres, Vols I and II. Paris: Maloine.
46. Ruigrok TJ, Osse RJ, Voogd J. 1992. Organization of inferior olivary projections to the flocculus and ventral paraflocculus of the rat cerebellum. J Comp Neurol 316: 129-150.
47. Sarna JR, Marzban H, Watanabe M, Hawkes R. 2006. Complementary stripes of phospholipase Cbeta3 and Cbeta4 expression by Purkinje cell subsets in the mouse cerebellum. J Comp Neurol 496: 303-313.
48. Sawada K, Fukui Y, Hawkes R. 2008. Spatial distribution of corticotropin-releasing factor immunopositive climbing fibers in the mouse cerebellum: analysis by whole mount immunohistochemistry. Brain Res 1222: 106-117.
49. Sillitoe RV, Hawkes R. 2002. Whole-mount immunohistochemistry: a high-throughput screen for patterning defects in the mouse cerebellum. J Histochem Cytochem 50: 235-244.
50. Sillitoe RV, Benson MA, Blake DJ, Hawkes R. 2003a. Abnormal dysbindin expression in cerebellar mossy fiber synapses in the mdx mouse model of Duchenne muscular dystrophy. J Neurosci 23: 6576-6585.
51. Sillitoe RV, Kunzle H, Hawkes R. 2003b. Zebrin II compartmentation of the cerebellum in a basal insectivore, the Madagascan hedgehog tenrec Echinops telfairi. J Anat 203: 283-296.
52. Sillitoe RV, Marzban H, Larouche M, Zahedi S, Affanni J, Hawkes R. 2005. Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species. Prog Brain Res 148: 283-297.
53. Sillitoe RV, Stephen D, Lao Z, Joyner AL. 2008. Engrailed homeobox genes determine the organization of Purkinje cell sagittal stripe gene expression in the adult cerebellum. J Neurosci 28: 12150-12162.
54. Sillitoe RV, Vogel MW, Joyner AL. 2010. Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J Neurosci 30: 10015-10024.
55. Stanek LM. 2006. Cocaine- and amphetamine-related transcript (CART) and anxiety. Peptides 27: 2005-2011.
56. Sugihara I, Quy PN. 2007. Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol 500: 1076-1092.
57. Sugihara I, Shinoda Y. 2004. Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci 24: 8771-8785.
58. Sugihara I, Ebata S, Shinoda Y. 2004. Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei: an analysis of single olivocerebellar axonal morphology. J Comp Neurol 470: 113-133.
59. Sugihara I, Fujita H, Na J, Quy PN, Li BY, Ikeda D. 2009. Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J Comp Neurol 512: 282-304.
60. Vicentic A, Jones DC. 2007. The CART (cocaine- and amphetamine-regulated transcript) system in appetite and drug addiction. J Pharmacol Exp Ther 320: 499-506.
61. Vogel MW, Ji Z, Millen K, Joyner AL. 1996. The Engrailed-2 homeobox gene and patterning of spinocerebellar mossy fiber afferents. Brain Res Dev Brain Res 96: 210-218.
62. Voogd J, Ruigrok TJ. 1997. Transverse and longitudinal patterns in the mammalian cerebellum. Prog Brain Res 114: 21-37.
63. Voogd J, Ruigrok TJ. 2004. The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: the congruence of projection zones and the zebrin pattern. J Neurocytol 33: 5-21.
64. Voogd J, Pardoe J, Ruigrok TJ, Apps R. 2003. The distribution of climbing and mossy fiber collateral branches from the copula pyramidis and the paramedian lobule: congruence of climbing fiber cortical zones and the pattern of zebrin banding within the rat cerebellum. J Neurosci 23: 4645-4656.
65. Walther EU, Dichgans M, Maricich SM, Romito RR, Yang F, Dziennis S, Zackson S, Hawkes R, Herrup K. 1998. Genomic sequences of aldolase C (zebrin II) direct lacZ expression exclusively in non-neuronal cells of transgenic mice. Proc Natl Acad Sci U S A 95: 2615-2620.
66. Zagrebelsky M, Rossi F, Hawkes R, Strata P. 1996. Topographically organized climbing fibre sprouting in the adult rat cerebellum. Eur J Neurosci 8: 1051-1054.
67. Zagrebelsky M, Strata P, Hawkes R, Rossi F. 1997. Reestablishment of the olivocerebellar projection map by compensatory transcommissural reinnervation following unilateral transection of the inferior cerebellar peduncle in the newborn rat. J Comp Neurol 379: 283-299.