Compartmentalization of the deep cerebellar nuclei based on afferent projections and aldolase C expression

Cerebellum

Volumn 10, Issue 3, 2011, Pages 449-463

  Sugihara, Izumi ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Cerebellum; Climbing fiber; Purkinje cell; Topography; Zebrin; Zone

Indexed keywords

ALDOLASE C; LYASE; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL PHENOMENA AND FUNCTIONS; CEREBELLUM CORTEX; CEREBELLUM NUCLEUS; CLIMBING FIBER; HUMAN; NERVE FIBER; NERVE PROJECTION; NERVE TRACT; NONHUMAN; OLIVOCORTICONUCLEAR TRACT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PURKINJE CELL; SENSORY NERVE; SOMATOSENSORY SYSTEM; TISSUE COMPARTMENTALIZATION;

AFFERENT PATHWAYS; ANIMALS; CEREBELLAR NUCLEI; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE EXPRESSION; MODELS, ANATOMIC; MODELS, NEUROLOGICAL;

EID: 80455156092     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-010-0226-1     Document Type: Article

References (72)

1. Sugihara I, Shinoda Y. Molecular, topographic and functional organization of the cerebellar nuclei: analysis by threedimensional mapping of the olivonuclear projection and aldolase C labeling. J Neurosci. 2007;27:9696-710. (Pubitemid 47492186)
2. Voogd J, Ruigrok TJH. 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. 2004;33:5-21. (Pubitemid 38860216)
3. Pijpers A, Voogd J, Ruigrok TJH. Topography of olivo-corticonuclear modules in the intermediate cerebellum of the rat. J Comp Neurol. 2005;492:193-213. (Pubitemid 41443721)
4. Sugihara I, Fujita H, Na J, Quy PN, Li BY, Ikeda D. Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. J Comp Neurol. 2009;512:282-304.
5. Buisseret-Delmas C, Angaut P. The cerebellar olivocorticonuclear connections in the rat. Prog Neurobiol. 1993;40:63-87.
6. Eisenman LM. Organization of the olivocerebellar projection to the uvula in the rat. Brain Behav Evol. 1984;24:1-12. (Pubitemid 14136048)
7. Voogd J, Pardoe J, Ruigrok TJH, Apps R. 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. 2003;23:4645-56. (Pubitemid 36706193)
8. Sugihara I, Shinoda Y. Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J Neurosci. 2004;24:8771-85. (Pubitemid 39362972)
9. Groenewegen HJ, Voogd J. The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of the cat cerebellum. J Comp Neurol. 1977;174:417-88. (Pubitemid 8131168)
10. Voogd J, Bigaré F. 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; 1980. p. 207-34.
11. Sugihara I, Quy PN. Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. J Comp Neurol. 2007;500:1076-92. (Pubitemid 46106466)
12. Neudert F, Nuernberger KK, Redies C. Comparative analysis of cadherin expression and connectivity patterns in the cerebellar system of ferret and mouse. J Comp Neurol. 2008;511:736-52.
13. Brodal A. Neurological Anatomy in Relation to Clinical Medicine. 3rd ed. New York: Oxford University Press; 1981.
14. Voogd J. Cerebellum. In: Paxinos G, editor. The Rat Nervous System. 3rd ed. Amsterdam: Elsevier Academic; 2004. p. 205-42.
15. Buisseret-Delmas C, Angaut P, Compoint C, Diagne M, Buisseret P. Brainstem efferents from the interface between the nucleus medialis and the nucleus interpositus in the rat. J Comp Neurol. 1998;402:264-75. (Pubitemid 28533323)
16. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. 6th ed. Amsterdam: Elsevier Academic; 2007.
17. Hawkes R, Leclerc N. Antigenic map of the rat cerebellar cortex: the distribution of parasagittal bands as revealed by monoclonal anti-Purkinje cell antibody mabQ113. J Comp Neurol. 1987;256:29-41. (Pubitemid 17005342)
18. Brochu G, Maler L, Hawkes R. Zebrin II: a polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. J Comp Neurol. 1990;291:538-52. (Pubitemid 20047467)
19. Eisenman LM, Hawkes R. 5'-Nucleotidase and the mabQ113 antigen share a common distribution in the cerebellar cortex of the mouse. Neuroscience. 1989;31:231-5. (Pubitemid 19209713)
20. Mukai T, Yatsuki H, Masuko S, Arai Y, Joh K, Hori K. The structure of the brain-specific rat aldolase C gene and its regional expression. Biochem Biophys Res Commun. 1991;174:1035-42.
21. Stefanizzi I, Cañete-Soler R. Coregulation of light neurofilament mRNA by poly(A)-binding protein and aldolase C: implications for neurodegeneration. Mol Brain Res. 2007;1139:15-28. (Pubitemid 46335697)
22. Fortin M, Marchand R, Parent A. Calcium-binding proteins in primate cerebellum. Neurosci Res. 1998;30:155-68. (Pubitemid 28127836)
23. Chung SH, Marzban H, Hawkes R. Compartmentation of the cerebellar nuclei of the mouse. Neuroscience. 2009;161:123-38.
24. Chan-Palay V. Cerebellar Dentate Nucleus: Organization, Cytology, and Transmitters. Berlin: Springer; 1977.
25. Matsushita M, Xiong G. Projections from the cermical enlargement to the cerebellar nuclei in the rat, studied by anterograde axonal tracing. J Comp Neurol. 1997;377:251-61. (Pubitemid 27009832)
26. Wu HS, Sugihara I, Shinoda Y. Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei. J Comp Neurol. 1999;411:97-118. (Pubitemid 29343053)
27. Shinoda Y, Sugiuchi Y, Futami T, Izawa R. Axon collaterals of mossy fibers from the pontine nucleus in the cerebellar dentate nucleus. J Neurophysiol. 1992;67:547-60.
28. Parenti R, Zappalà A, Serapide MF, Pantò MR, Cicirata F. Projections of the basilar pontine nuclei and nucleus reticularis tegmenti pontis to the cerebellar nuclei of the rat. J Comp Neurol. 2002;452:115-27.
29. Shinoda Y, Sugiuchi Y, Futami T. Excitatory inputs to cerebellar dentate nucleus neurons from the cerebral cortex in the cat. Exp Brain Res. 1987;67:299-315. (Pubitemid 17105382)
30. Rowland NC, Jaeger D. Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways. J Neurophysiol. 2008;99:704-17. (Pubitemid 351253230)
31. Sugihara I, Wu H-S, Shinoda Y. Morphology of single olivocerebellar axons labeled with biotinylated dextran amine in the rat. J Comp Neurol. 1999;414:131-48. (Pubitemid 29489899)
32. Van der Want JJL, Wiklund L, Guegan M, Ruigrok TJH, Voogd J. Anterograde tracing of the rat olivocerebellar system with Phaseolus vulgaris leucoagglutinin (PHA-L). Demonstration of climbing fiber collateral innervation of the cerebellar nuclei. J Comp Neurol. 1989;288:1-18. (Pubitemid 19249470)
33. Ito M. Cerebellum and Neural Control. New York: Raven; 1984.
34. Sugihara I, Wu H-S, Shinoda Y. The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J Neurosci. 2001;21:7715-23. (Pubitemid 32904970)
35. Apps R, Garwicz M. Precise matching of olivo-cortical divergence and cortico-nuclear convergence between somatotopically corresponding areas in the medial C1 and medial C3 zones of the paravermal cerebellum. Eur J Neurosci. 2000;12:205-14. (Pubitemid 30068425)
36. Ruigrok TJ, Voogd J. Cerebellar nucleo-olivary projections in the rat: an anterograde tracing study with Phaseolus vulgarisleucoagglutinin (PHA-L). J Comp Neurol. 1990;298:315-33. (Pubitemid 20256544)
37. Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci. 2005;6:297-311. (Pubitemid 40469984)
38. Ruigrok TJH, Voogd J. Organization of projections from the inferior olive to the cerebellar nuclei in the rat. J Comp Neurol. 2000;426:209-28.
39. Sugihara I, Ebata S, Shinoda Y. Functional compartmentalization in the flocculus and the ventral dentate and dorsal group y nuclei: an analysis of single olivocerebellar axonal morphology. J Comp Neurol. 2004;470:113-33. (Pubitemid 38160687)
40. Ruigrok TJ, Pijpers A, Goedknegt-Sabel E, Coulon P. Multiple cerebellar zones are involved in the control of individual muscles: a retrograde transneuronal tracing study with rabies virus in the rat. Eur J Neurosci. 2008;28:181-200.
41. Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432-44. (Pubitemid 37129661)
42. Lu X, Miyachi S, Ito Y, Nambu A, Takada M. Topographic distribution of output neurons in cerebellar nuclei and cortex to somatotopic map of primary motor cortex. Eur J Neurosci. 2007;25:2374-82. (Pubitemid 46625916)
43. Haines DE, Koletar SL. Topography of cerebellar corticonuclear fibers of the albino rat. Vermis of anterior and posterior lobes. Brain Behav Evol. 1979;16:271-92. (Pubitemid 10202502)
44. Teune TM, van der Burg J, van der Moer J, Voogd J, Ruigrok TJH. Topography of cerebellar nuclear projections to the brain stem in the rat. Prog Brain Res. 2000;124:141-72. (Pubitemid 30604528)
45. Swenson RS, Castro AJ. The afferent connections of the inferior olivary complex in rats.An anterograde study using autoradiographic and axonal degeneration techniques. Neuroscience. 1983;8:259-75. (Pubitemid 13189497)
46. Onodera S. Olivary projections from the mesodiencephalic structures in the cat studied by means of axonal transport of horseradish peroxidase and tritiated amino acids. J Comp Neurol. 1984;227:37-49. (Pubitemid 14094640)
47. Holstege G, Tan J. Projections from the red nucleus and surrounding areas to the brainstem and spinal cord in the cat. An HRP and autoradiographical tracing study. Behav Brain Res. 1988;28:33-57.
48. de Zeeuw CI, Holstege JC, Ruigrok TJ, Voogd J. Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry. J Comp Neurol. 1989;284:12-35. (Pubitemid 19186008)
49. Matsushita M, Ragnarson B, Grant G. 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. 1991;84:133-41.
50. Brown JT, Chan-Palay V, Palay SL. A study of afferent input to the inferior olivary complex in the rat by retrograde axonal transport of horseradish peroxidase. J Comp Neurol. 1977;176:1-22. (Pubitemid 8209579)
51. Gerrits NM, Voogd J, Magras IN. Vestibular afferents of the inferior olive and the vestibulo-olivo-cerebellar climbing fiber pathway to the flocculus in the cat. Brain Res. 1985;332:325-36. (Pubitemid 15108003)
52. Akaike T. The tectorecipient zone in the inferior olivary nucleus in the rat. J Comp Neurol. 1992;320:398-414.
53. Boesten AJ, Voogd J. Projections of the dorsal column nuclei and the spinal cord on the inferior olive in the cat. J Comp Neurol. 1975;161:215-37.
54. Berkley KJ, Hand PJ. Projections to the inferior olive of the cat. II. Comparisons of input from the gracile, cuneate and the spinal trigeminal nuclei. J Comp Neurol. 1978;180:253-64. (Pubitemid 8345055)
55. Matsushita M, Yaginuma H, Tanami T. Somatotopic termination of the spino-olivary fibers in the cat, studied with the wheat germ agglutinin-horseradish peroxidase technique. Exp Brain Res. 1992;89:397-407.
56. Molinari HH, Schultze KE, Strominger NL. Gracile, cuneate, and spinal trigeminal projections to inferior olive in rat and monkey. J Comp Neurol. 1996;375:467-80. (Pubitemid 26374785)
57. Büttner U, Fuchs AF, Markert-Schwab G, Buckmaster P. Fastigial nucleus activity in the alert monkey during slow eye and head movements. J Neurophysiol. 1991;65:1360-71.
58. Mori S, Matsui T, Kuze B, Asanome M, Nakajima K, Matsuyama K. Stimulation of a restricted region in the midline cerebellar white matter evokes coordinated quadrupedal locomotion in the decerebrate cat. J Neurophysiol. 1999;82:290-300. (Pubitemid 29330084)
59. Huerta MF, Hashikawa T, Gayoso MJ, Harting JK. The trigeminoolivary projection in the cat: contributions of individual subnuclei. J Comp Neurol. 1985;241:180-90. (Pubitemid 16202811)
60. Gellman R, Houk JC, Gibson AR. Somatosensory properties of the inferior olive of the cat. J Comp Neurol. 1983;215:228-43. (Pubitemid 13089753)
61. Van Ham JJ, Yeo CH. Somatosensory trigeminal projections to the inferior olive, cerebellum and other precerebellar nuclei in rabbits. Eur J Neurosci. 1992;4:302-17.
62. Attwell PJ, Rahman S, Ivarsson M, Yeo CH. Cerebellar cortical AMPA-kainate receptor blockade prevents performance of classically conditioned nictitating membrane responses. J Neurosci. 1999;19(RC45):1-6.
63. Mostofi A, Holtzman T, Grout AS, Yeo CH, Edgley SA. Electrophysiological localization of eyeblink-related microzones in rabbit cerebellar cortex. J Neurosci. 2010;30:8920-34.
64. Ruigrok TJ. Ins and outs of cerebellar modules. Cerebellum 2010 (in press) doi:10.1007/s12311-010-0164-y.
65. Leonard CS, Simpson JI, Graf W. 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. 1988;60:2073-90. (Pubitemid 19017466)
66. Kuypers HG. The descending pathways to the spinal cord, their anatomy and function. Prog Brain Res. 1964;11:178-202.
67. Fuchs AF, Robinson FR, Straube A. Participation of the caudal fastigial nucleus in smooth-pursuit eye movements. I. Neuronal activity. J Neurophysiol. 1994;72:2714-28. (Pubitemid 24382101)
68. Ohtsuka K, Noda H. Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys. J Neurophysiol. 1991;65:1422-34.
69. Oulad Ben Taib N, Manto M. Effects of trains of high-frequency stimulation of the premotor/supplementary motor area on conditioned corticomotor responses in hemicerebellectomized rats. Exp Neurol. 2008;212:157-65.
70. Gruart A, Delgado-García JM. Discharge of identified deep cerebellar nuclei neurons related to eye blinks in the alert cat. Neuroscience. 1994;61:665-81. (Pubitemid 24240313)
71. Thach WT, Kane SA, Mink JW, Goodkin HP. Cerebellar output: multiple maps and motor modes in movement coordination. In: Llinas R, Sotelo C, editors. The cerebellum revisited. New York: Springer; 1992. p. 283-300.
72. Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413-34.