Organization of the marmoset cerebellum in three-dimensional space: Lobulation, aldolase c compartmentalization and axonal projection

Journal of Comparative Neurology

Volumn 518, Issue 10, 2010, Pages 1764-1791

  Fujita, Hirofumi ^a   Oh Nishi, Arata ^b   Obayashi, Shigeru ^b   Sugihara, Izumi ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

Author keywords

Flocculus; Inferior olive; Primate; Purkinje cell; Topography; Zebrin

Indexed keywords

ALDOLASE C; FRUCTOSE BISPHOSPHATE ALDOLASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL COMPARTMENTALIZATION; CEREBELLUM; CEREBELLUM CORTEX; CEREBELLUM FLOCCULUS; CLIMBING FIBER; CONTROLLED STUDY; FEMALE; HYPOPHYSIS INTERMEDIATE LOBE; IMMUNOHISTOCHEMISTRY; MALE; MARMOSET; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES DIFFERENCE; WESTERN BLOTTING;

ANIMALS; AXONS; CALLITHRIX; CEREBELLUM; DENDRITES; FEMALE; FRUCTOSE-BISPHOSPHATE ALDOLASE; MALE; NEURAL PATHWAYS; RATS;

EID: 77952159445     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22301     Document Type: Article

References (70)

1. Akintunde A, Eisenman LM. 1994. External cuneocerebellar projection and Purkinje cell zebrin Il bands: a direct comparison of parasagittal banding in the mouse cerebellum. J Chem Neuroanat 7:75-86. (Pubitemid 24271596)
2. Azizi SA, Woodward DJ. 1987. Inferior olivary nuclear complex of the rat: morphology and comments on the principles of organization within the olivocerebellar system. J Comp Neurol 263:467-484.
3. Bowman JP, Sládek JR Jr. 1973. Morphology of the inferior olivary complex of the rhesus monkey (Macaca mulatta). J Comp Neurol 152:299-316.
4. 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. (Pubitemid 20047467)
5. Brodai A, Kawamura K. 1980. Olivocerebellar projection: a review. Adv Anat Embryol Cell Biol 64:1-140.
6. Brodai P, Brodai A. 1981. The olivocerebellar projection in the monkey. Experimental studies with the method of retrograde tracing of horseradish peroxidase. J Comp Neurol 201:375-393.
7. Brodai P, Brodai A. 1982. Further observations on the olivocerebellar projection in the monkey. Exp Brain Res 45:71-83.
8. Buisseret-Delmas C, Angaut P. 1993. The cerebellar olirvocorticonuclear connections in the rat. Prog Neurobiol 40:63-87.
9. Buisseret-Delmas C, Angaut P, Compoint C, Diagne M, Buisseret P. 1998. Brainstem efferents from the interface between the nucleus medialis and the nucleus interpositus in the rat. J Comp Neurol 402:264-275. (Pubitemid 28533323)
10. Courville J, Cooper CW. 1970. The cerebellar nuclei of Macaca mulatta: a morphological study. J Comp Neurol 140:241-254.
11. Doré L, Jacobson CD, Hawkes R. 1990. Organization and postnatal development of zebrin II antigenic compartmentation in the cerebellar vermis of the grey opossum, Monodelphis domestica. J Comp Neurol 291:431-449. (Pubitemid 20028781)
12. Ebner TJ, Johnson MT, Roitman A, Fu Q. 2002. What do complex spikes signal about limb movements? Ann N Y Acad Sei 978: 205-218.
13. Eisenman LM, Hawkes R. 1993. Antigenic compartmentation in the mouse cerebellar cortex: zebrin and HNK-1 reveal a complex, overlapping molecular topography. J Comp Neurol 335: 586-605. (Pubitemid 23254255)
14. Evrard HC, Craig AD. 2008. Retrograde analysis of the cerebellar projections to the posteroventral part of the ventral lateral thalamic nucleus in the macaque monkey. J Comp Neurol 508:286-314. (Pubitemid 351562038)
15. Gellman R, Gibson AR, Houk JC. 1985. Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol 54:40-60. (Pubitemid 15070470)
16. Gerrits NM, Voogd J. 1982. The climbing fiber projection to the flocculus and adjacent paraflocculus in the cat. Neuroscience 7:2971-2991. (Pubitemid 13168021)
17. 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. (Pubitemid 17160251)
18. Groenewegen HJ, Voogd J. 1977. The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of the cat cerebellum. J Comp Neurol 174:417-488. (Pubitemid 8131168)
19. Gwyn DG, Nicholson GP, Flumerfelt BA. 1977. The inferior olivary nucleus of the rat: a light and electron microscopic study. J Comp Neurol 174:489-520.
20. Hallem JS, Thompson JH, Gundappa-Sulur G, Hawkes R, Bjaalie JG, Bower JM. 1999. Spatial correspondence between tactile projection patterns and the distribution of the antigenic Purkinje cell markers antt-zebrin I and anti-zebrin II in the cerebellar folium crus IIA of the rat. Neuroscience 93:1083-1094. (Pubitemid 29341655)
21. Hashimoto M, Mikoshiba K. 2003. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J Neurosci 23:11342-11351.
22. Hawkes R, Leclerc N. 1987. Antigenic map of the rat cerebellar cortex: the distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mobA113. J Comp Neurol 256:29-41. (Pubitemid 17005342)
23. Hess DT, Voogd J. 1986. Chemoarchitectonic zonation of the monkey cerebellum. Brain Res 369:383-387.
24. Ikeda Y, Noda H, Sugita S. 1989. Olivocerebellar and cerebellool'rvary connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 284:463-488. (Pubitemid 19173272)
25. Larsell O. 1952. The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J Comp Neurol 97:281-356.
26. Larsell O. 1953. The cerebellum of the cat and the monkey. J Comp Neurol 99:135-199.
27. Larsell O. 1970. The comparative anatomy and histology of the cerebellum from monotremes through apes. Minneapolis, MN: The University of Minnesota Press.
28. Leonard CS, Simpson Jl, Graf W. 1988. Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Topology of inferior olive neurons of the dorsal cap of Kooy. J Neurophysiol 60:2073-2090. (Pubitemid 19017466)
29. Madigan JC Jr, Carpenter MB. 1971. Cerebellum of the rhesus monkey, atlas of lobules, laminae, and folia, in sections. Baltimore, MD: University Park Press.
30. Matsushita M, Ragnarson B, Grant G. 1991. Topographic relationship between sagittal Purkinje cell bands revealed by monoclonal antibody to zebrin I and spinocerebellar projections arising from the central cervical nucleus in the rat. Exp Brain Res 84:133-141.
31. Millen KJ, Hui CC, Joyner AL. 1995. A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development 121:3935-3945.
32. Nagao S, Kitamura T, Nakamura N, Hiramatsu T, Yamada J. 1997. Differences of the primate flocculus and ventral paraflocculus in the mossy and climbing fiber input organization. J Comp Neurol 382:480-498. (Pubitemid 27250808)
33. Neudert F, Redies C. 2008. Neural circuits revealed by axon tracing and mapping Cadherin expression in the embryonic chicken cerebellum. J Comp Neurol 509:283-301.
34. Neudert F, Nuernberger KK, Redies C. 2008. Comparative analysis of Cadherin expression and connectivity patterns in the cerebellar system of ferret and mouse. J Comp Neurol 511: 736-752.
35. Nieuwenhuys R., Voogd J, van Huijzen C. 2008. The human central nervous system. Berlin: Springer.
36. Ozol K, Hayden JM, Oberdick J, Hawkes R. 1999. Transverse zones in the vermis of the mouse cerebellum. J Comp Neurol 412:95-111. (Pubitemid 29380327)
37. 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 Iivia). J Comp Neurol 501:619-630. (Pubitemid 46622499)
38. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates, 4th ed. San Diego, CA: Academic Press.
39. Pijpers A, Apps R, Pardoe J, Voogd J, Ruigrok TJH. 2006. Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. J Neurosci 26:12067-12080. (Pubitemid 44772117)
40. Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG. 2002. Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J Neurophysiol 87:912-924. (Pubitemid 34670854)
41. Ruigrok TJH, Cella F. 2004. Precerebellar nuclei and red nucleus. In: Paxinos G, editor. The rat nervous system, 3rd ed. Amsterdam: Elsevier Academic Press, p 167-204.
42. 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.
43. Sanchez M, Sillitoe RV, Attwell PJ, Ivarsson M, Rahman S, Yeo CH, Hawkes R. 2002. Compartmentation of the rabbit cerebellar cortex. J Comp Neurol 444:159-173.
44. Sillitoe RV, Hulliger M, Dyck R, Hawkes R. 2003. Antigenic compartmentation of the cat cerebellar cortex. Brain Res 977:1-15. (Pubitemid 36644164)
45. Sillitoe RV, Malz CR, Rockland K, Hawkes R. 2004. Antigenic compartmentation of the primate and tree shrew cerebellum: a common topography of zebrin Il in Macaca mulatta and Tupaia belangeri. J Anat 204:257-269. (Pubitemid 38515143)
46. 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. (Pubitemid 40127312)
47. Strick PL, Dum RP, Fiez JA. 2009. Cerebellum and nonmotor function. Annu Rev Neurosci 32:413-434.
48. Sudarov A, Joyner AL. 2007. Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev 2:26.
49. Sugihara I. 2005. Microzonal projection and climbing fiber remodeling in single olivocerebellar axons of newborn rats at postnatal days 4-7. J Comp Neurol 487:93-106. (Pubitemid 40646954)
50. Sugihara I, Quy PN. 2007. Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol 500:1076-1092. (Pubitemid 46106466)
51. 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. (Pubitemid 39362972)
52. Sugihara I, Shinoda Y. 2007. Molecular, topographic, and functional organization of the cerebellar nuclei: analysis by threedimensional mapping of the olivonuclear projection and aldolase C labeling. J Neurosci 27:9696-9710. (Pubitemid 47492186)
53. Sugihara I, Lang EJ, Llinás R. 1995. Serotonin modulation of inferior olivary oscillations and synchronicity: a multipleelectrode study in the rat cerebellum. Eur J Neurosci 7:521-534.
54. Sugihara I, Bailly Y, Mariani J. 2000. Olivocerebellar climbing fibers in the granuloprival cerebellum: morphological study of individual axonal projections in the X-irradiated rat J Neurosci 20:3745-3760.
55. Sugihara I, Wu H-S, Shinoda Y. 2001. The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci 21:7715-7723. (Pubitemid 32904970)
56. 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. (Pubitemid 38160687)
57. Sugihara I, Marshall SP, Lang EJ. 2007. Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus lla of the rat cerebellar cortex. J Comp Neurol 501:13-29. (Pubitemid 46155870)
58. 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.
59. Swanson LW. 1998. Brain maps: structure of the rat brain. Amsterdam, Elsevier.
60. Tan J, Gerrits NM, Nanhoe R, Simpson JI, Voogd J. 1995. Zonal organization of the climbing fiber projection to the flocculus and nodulus of the rabbit a combined axonal tracing and acetylcholinesterase histochemical study. J Comp Neurol 356:23-50.
61. Voogd, J. 1998. Cerebellum and precerebellar nuclei. In: Dubbeldam JL, Van Dongen PAM, Voogd J, editors. The central nervous system of vertebrates. Berlin: Springer, p 1724-1753.
62. Voogd, J. 2004. Cerebellum. In: Paxinos G, editor. The rat nervous system, 3rd ed. Amsterdam: Elsevier Academic Press, p 205-242.
63. Voogd J, Bigaré F. 1980. Topographical distribution of olivary and corticonuclear fibers in the cerebellum. A review. In: Courville J, de Montigny C, Lamarre Y, editors. The inferior olivary nucleus: anatomy and physiology. New York: Raven Press, p 207-234.
64. Voogd J, Ruigrok TJH. 1997. Transverse and longitudinal patterns in the mammalian cerebellum. Prog Brain Res 114:21-37. (Pubitemid 27244963)
65. Voogd J, Ruigrok TJH. 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. (Pubitemid 38860216)
66. Voogd J, Gerrits NM, Ruigrok TJ. 1996. Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553-579.
67. Voogd J, Pardoe J, Ruigrok TJH, 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. (Pubitemid 36706193)
68. Wadiche JI, Jahr CE. 2005. Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci 8:1329-1334.
69. Wassef M, Cholley B, Heizmann CW, Sotelo C. 1992. Development of the olivocerebellar projection in the rat: II. Matching of the developmental compartmentations of the cerebellum and inferior olive through the projection map. J Comp Neurol 323:537-550.
70. Welsh JP, Yuen G, Placantonakis DG, Vu TQ, Haiss F, O'Hearn E, Molliver ME, Aicher SA. 2002. Why do Purkinje cells the so easily after global brain ischemia? Aldolase C, EAAT4, and the cerebellar contribution to posthypoxic myoclonus. Adv Neurol 89:331-359.