Chapter 3 An anatomical model of cerebellar modules

Publisher Summary This chapter presents a view of cerebellar organization in which the entire cortex is subdivided into a reproducible array of very small modules. The working hypothesis is that bands of Purkinje cells plus their afferent climbing fibers, with a clear origin early in cerebellar embryology, are further subdivided into microzones/patches by the mossy fiber afferents. A predictable structural compartmentation down to the units of the order ∼102 Purkinje cells and associated interneurons implies that these modules may function as single processing units. The afferent topography of the cerebellum is complex and stereotyped, and multiple afferent pathways terminate in precise receiving areas, bands, and patches. The cerebellar cortex is subdivided parasagittally into bands, which may be further split; and orthogonal to the zebrin compartments is a second set of boundaries, revealed by the lobulation, developmental defects in mouse mutants and wrinkles in the granular layer. Each module receives a particular pattern of mossy fiber innervation and projects onto a topographically organized Purkinje cell layer above.

[1]  P Strata,et al.  Topographically Organized Climbing Fibre Sprouting in the Adult Rat Cerebellum , 1996, The European journal of neuroscience.

[2]  R. Hawkes,et al.  Parasagittal organization of the rat cerebellar cortex: Direct correlation between antigenic purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection , 1987, The Journal of comparative neurology.

[3]  C. Sotelo,et al.  Development of the olivocerebellar projection in the rat: I. Transient biochemical compartmentation of the inferior olive , 1992, The Journal of comparative neurology.

[4]  R. Hawkes,et al.  The development of molecular compartmentation in the cerebellar cortex. , 1994, Acta anatomica.

[5]  J. Altman,et al.  Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum , 1978, The Journal of comparative neurology.

[6]  M. Ross,et al.  Meander tail reveals a discrete developmental unit in the mouse cerebellum. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[7]  F. G. Worden,et al.  The neurosciences : fourth study program , 1979 .

[8]  R. Bronson,et al.  Rostral cerebellar malformation, (rcm): a new recessive mutation on chromosome 3 of the mouse. , 1992, The Journal of heredity.

[9]  G. Schoolnik,et al.  An inducible bundle-forming pilus of enteropathogenic Escherichia coli. , 1991, Science.

[10]  A. Parent,et al.  The compartmentalization of the monkey and rat cerebellar cortex: zebrin I and cytochrome oxidase , 1990, Brain Research.

[11]  S. Snyder,et al.  Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. Parent,et al.  Zonation in the rat cerebellar cortex: patches of high acetylcholinesterase activity in the granular layer are congruent with Purkinje cell compartments , 1988, Brain Research.

[13]  L. Garey,et al.  Parasagittal patches in the granular layer of the developing and adult rat cerebellum as demonstrated by NADPH-diaphorase histochemistry. , 1993, Neuroreport.

[14]  J. Voogd.  Comparative aspects of the structure and fibre connexions of the mammalian cerebellum. , 1967, Progress in brain research.

[15]  M E Hallonet,et al.  A new approach to the development of the cerebellum provided by the quail-chick marker system. , 1990, Development.

[16]  T. G. Scott,et al.  A Unique Pattern of Localization within the Cerebellum , 1963, Nature.

[17]  M L Johnson,et al.  Molecular compartmentation expressed in cerebellar cultures in the absence of neuronal activity and neuron‐glia interactions , 1995, The Journal of comparative neurology.

[18]  C. Sotelo,et al.  Expression of compartmentation antigen zebrin I in cerebellar transplants , 1990, The Journal of comparative neurology.

[19]  R. Hawkes,et al.  Distribution of zebrin II in the gigantocerebellum of the mormyrid fish Gnathonemus petersii compared with other teleosts , 1992, The Journal of comparative neurology.

[20]  W. Lange.  Regional Differences in the Cytoarchitecture of the Cerebellar Cortex , 1982 .

[21]  R. Hawkes.  Antigenic markers of cerebellar modules in the adult mouse. , 1992, Biochemical Society transactions.

[22]  H. Sakano,et al.  Detection of somatic DNA recombination in the transgenic mouse brain. , 1991, Science.

[23]  A. Joyner,et al.  Subtle cerebellar phenotype in mice homozygous for a targeted deletion of the En-2 homeobox. , 1991, Science.

[24]  O. Larsell,et al.  The comparative anatomy and histology of the cerebellum , 1967 .

[25]  R. Hawkes,et al.  Zebrins: Molecular Markers of Compartmentation in the Cerebellum , 1992 .

[26]  G. M. Shambes,et al.  Multiple tactile areas in cerebellar cortex: another patchy cutaneous projection to granule cell columns in rats , 1978, Brain Research.

[27]  J. Bower,et al.  Variability in tactile projection patterns to cerebellar folia crus IIa of the norway rat , 1990, The Journal of comparative neurology.

[28]  S. Palay,et al.  Sagittal cerebellar microbands of taurine neurons: immunocytochemical demonstration by using antibodies against the taurine-synthesizing enzyme cysteine sulfinic acid decarboxylase. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[29]  C. Sotelo,et al.  Development of the spinocerebellar system in the postnatal rat , 1985, The Journal of comparative neurology.

[30]  J. S. King,et al.  New concepts in cerebellar neurobiology , 1986 .

[31]  D. Tolbert,et al.  Lower thoracic-upper lumbar spinocerebellar projections in rats: A complex topography revealed in computer reconstructions of the unfolded anterior lobe , 1993, Neuroscience.

[32]  M. Surani,et al.  Segmental and developmental regulation of a presumptive T-cell oncogene in the central nervous system , 1990, Nature.

[33]  M. Capecchi,et al.  Swaying is a mutant allele of the proto-oncogene Wnt-1 , 1991, Cell.

[34]  G. M. Shambes,et al.  Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. , 1978, Brain, behavior and evolution.

[35]  D. Stainier,et al.  The monoclonal antibody B30 recognizes a specific neuronal cell surface antigen in the developing mesencephalic trigeminal nucleus of the mouse , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  R. Hawkes,et al.  Functional and antigenic maps in the rat cerebellum: Zebrin compartmentation and vibrissal receptive fields in lobule IXa , 1994, The Journal of comparative neurology.

[37]  C. Sotelo,et al.  Postnatal development of the inferior olivary complex in the rat. II. Topographic organization of the immature olivocerebellar projection , 1984, The Journal of comparative neurology.

[38]  C. Ekerot,et al.  Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. , 1973, Brain research.

[39]  J. Bower,et al.  Congruence of spatial organization of tactile projections to granule cell and Purkinje cell layers of cerebellar hemispheres of the albino rat: vertical organization of cerebellar cortex. , 1983, Journal of neurophysiology.

[40]  A. Brodal,et al.  The Inferior Olive. Notes on its Comparative Anatomy, Morphology, and Cytology , 1980 .

[41]  E. Hess,et al.  Tottering and leaner mutations perturb transient developmental expression of tyrosine hydroxylase in embryologically distinct purkinje cells , 1991, Neuron.

[42]  G. Paxinos.  The Rat nervous system , 1985 .

[43]  R. Hawkes,et al.  The modular cerebellum , 1991, Progress in Neurobiology.

[44]  J. W. Langelaan.  ON THE DEVELOPMENT OF THE EXTERNAL FORM OF THE HUMAN CEREBELLUM , 1919 .

[45]  R. Hawkes,et al.  Organization and postnatal development of zebrin II antigenic compartmentation in the cerebellar vermis of the grey opossum, monodelphis domestica , 1990, The Journal of comparative neurology.

[46]  C. Sotelo,et al.  Cerebellar development: afferent organization and Purkinje cell heterogeneity. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  R. Hawkes,et al.  Development of the cerebellum and its extracerebellar purkinje cell projection in teleost fishes as determined by zebrin II immunocytochemistry , 1991, Progress in Neurobiology.

[48]  J. Wu,et al.  Colocalization of taurine- and cysteine sulfinic acid decarboxylase- like immunoreactivity in the cerebellum of the rat with monoclonal antibodies against taurine , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Karl Schilling,et al.  Control of segment-like patterns of gene expression in the mouse cerebellum , 1993, Neuron.

[50]  S. Subtelny,et al.  Developmental order, its origin and regulation , 1982 .

[51]  R. Hawkes,et al.  Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells , 1988, The Journal of comparative neurology.

[52]  R. Hawkes,et al.  Zebrin II: A polypeptide antigen expressed selectively by purkinje cells reveals compartments in rat and fish cerebellum , 1990, The Journal of comparative neurology.

[53]  V. Mountcastle,et al.  An organizing principle for cerebral function : the unit module and the distributed system , 1978 .

[54]  Wally Welker,et al.  Fractured cutaneous projections to the granule cell layer of the posterior cerebellar hemisphere of the domestic cat , 1984, The Journal of comparative neurology.

[55]  J M Bower,et al.  Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats. , 1981, Brain, behavior and evolution.

[56]  S. Martinez,et al.  Rostral Cerebellum Originates from the Caudal Portion of the So‐Called ‘Mesencephalic’ Vesicle: A Study Using Chick/Quail Chimeras , 1989, The European journal of neuroscience.

[57]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[58]  J. M. Gibson,et al.  Trigeminocerebellar mossy fiber branching to granule cell layer patches in the rat cerebellum , 1981, Brain Research.

[59]  S. Zackson,et al.  A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. , 1990, Science.

[60]  R. Llinás,et al.  General Discussion: Radial Connectivity in the Cerebellar Cortex: A Novel View Regarding the Functional Organization of the Molecular Layer , 1982 .

[61]  R. Hawkes,et al.  Zebrin II immunoreactivity in the rat and in the weakly electric teleost Eigenmannia (gymnotiformes) reveals three modes of purkinje cell development , 1991, The Journal of comparative neurology.

[62]  Richard Hawkes,et al.  Monoclonal antibodies reveal sagittal banding in the rodent cerebellar cortex , 1985, Brain Research.

[63]  H. Richard,et al.  Structural and Molecular Compartmentation in the Cerebellum , 1993, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[64]  S. Vincent,et al.  Neuronal NADPH diaphorase is a nitric oxide synthase. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[65]  G. M. Shambes,et al.  Tactile projections to granule cells in caudal vermis of the rat's cerebellum. , 1978, Brain, behavior and evolution.

[66]  J. Kassel,et al.  Superior colliculus projections to tactile areas of rat cerebellar hemispheres , 1980, Brain Research.

[67]  R. Hawkes,et al.  Differential Distribution of MAP1a and Aldolase c in Adult Mouse Cerebellum , 1996, The European journal of neuroscience.

[68]  R. Hawkes,et al.  Expression of monoclonal antibody Q113 immunoreactivity in the rat cerebral cortex: Unique differential sublayering of layer I. Staining of radial glia , 1988, Journal of neuroscience research.

[69]  G. M. Shambes,et al.  Tactile cutaneous representation in cerebellar granule cell layer of the opossum, Didelphis virginiana. , 1985, Brain, behavior and evolution.

[70]  R. Hawkes,et al.  Compartmentation of NADPH‐diaphorase activity in the mouse cerebellar cortex , 1994, The Journal of comparative neurology.

[71]  R. Hawkes,et al.  Compartmentation of the granular layer of the cerebellum. , 1997, Histology and histopathology.

[72]  J. Voogd,et al.  Chemoarchitectonic zonation of the monkey cerebellum , 1986, Brain Research.

[73]  R. Hawkes,et al.  Compartmentation in mammalian cerebellum: Zebrin II and P-path antibodies define three classes of sagittally organized bands of Purkinje cells. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[74]  D. Tolbert,et al.  Chronic NMDA receptor blockade or muscimol inhibition of cerebellar cortical neuronal activity alters the development of spinocerebellar afferent topography. , 1994, Brain research. Developmental brain research.

[75]  S. Rabacchi,et al.  Involvement of the N-methyl D-aspartate (NMDA) receptor in synapse elimination during cerebellar development. , 1992, Science.

[76]  R. Snider.  Neurobiology of cerebellar evolution and development , 1971 .

[77]  R. Hawkes,et al.  5'-Nucleotidase and the MABQ113 antigen share a common distribution in the cerebellar cortex of the mouse , 1989, Neuroscience.

[78]  5'-Nucleotidase of cerebellar molecular layer: reduction in Purkinje cell-deficient mutant mice. , 1986, Brain research.

[79]  K. Schilling,et al.  Nitric oxide synthase expression reveals compartments of cerebellar granule cells and suggests a role for mossy fibers in their development , 1994, Neuroscience.

[80]  C. Sotelo,et al.  Organization of spinocerebellar projection map in three types of agranular cerebellum: Purkinje cells vs. granule cells as organizer element , 1988, The Journal of comparative neurology.

[81]  C. Sotelo,et al.  Parasagittal compartmentation of adult rat purkinje cells expressing the low-affinity nerve growth factor receptor: Changes of pattern expression after a traumatic lesion , 1994, Neuroscience.

[82]  R. Hawkes,et al.  The cloning of zebrin II reveals its identity with aldolase C. , 1994, Development.

[83]  P. Strata,et al.  Reestablishment of the olivocerebellar projection map by compensatory transcommissural reinnervation following unilateral transection of the inferior cerebellar peduncle in the newborn rat , 1997 .

[84]  T. G. Scott.  A unique pattern of localization within the cerebellum of the mouse , 1964 .

[85]  E. Mugnaini,et al.  Dynamic organization of developing Purkinje cells revealed by transgene expression. , 1991, Science.

[86]  D. Hillman,et al.  Compartmentation of the cerebellar cortex by protein kinase C delta , 1993, Neuroscience.

[87]  J. Voogd,et al.  The parasagittal zonation within the olivocerebellar projection. II. Climbing fiber distribution in the intermediate and hemispheric parts of cat cerebellum , 1979, The Journal of comparative neurology.

[88]  R. Hawkes,et al.  The development of differential mabQ113-immunoreactivity in the rat habenular complex , 1987, Brain Research Bulletin.

[89]  M. Taussig.  The Nervous System , 1991 .

[90]  R. Hawkes,et al.  Novel developmental boundary in the cerebellum revealed by zebrin expression in the Lurcher (Lc/+) mutant mouse , 1992, The Journal of comparative neurology.

[91]  R. Llinás,et al.  The Cerebellum Revisited , 1992, Springer US.

[92]  S. Palay,et al.  The Cerebellum—New Vistas , 1982 .

[93]  R. Hawkes,et al.  Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK‐1 reveal a complex, overlapping molecular topography , 1993, The Journal of comparative neurology.

[94]  S. Palay,et al.  Chemical heterogeneity in cerebellar Purkinje cells: existence and coexistence of glutamic acid decarboxylase-like and motilin-like immunoreactivities. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[95]  A. Brodal,et al.  Olivocerebellar projection: a review. , 1980, Advances in anatomy, embryology, and cell biology.

[96]  R. Hawkes,et al.  Developing mossy fiber terminal fields in the rat cerebellar cortex may segregate because of Purkinje cell compartmentation and not competition , 1995, The Journal of comparative neurology.

[97]  O. Oscarsson.  Functional units of the cerebellum - sagittal zones and microzones , 1979, Trends in Neurosciences.

[98]  R. Hawkes,et al.  A survey of MabQ113 immunoreactivity in the adult rat brain: Differential staining of the lateral and medial habenular nuclei , 1986, Brain Research.

[99]  C. Sotelo,et al.  Transient biochemical compartmentalization of Purkinje cells during early cerebellar development. , 1985, Developmental biology.

[100]  N. Leclerc,et al.  Antigenic map of the rat cerebellar cortex: The distribution of parasagittal bands as revealed by monoclonal anti‐purkinje cell antibody mabQ113 , 1987, The Journal of comparative neurology.

[101]  R. Hawkes,et al.  Topography of purkinje cell compartments and mossy fiber terminal fields in lobules ii and iii of the rat cerebellar cortex: Spinocerebellar and cuneocerebellar projections , 1994, Neuroscience.

[102]  J. Voogd,et al.  An acetylcholinesterase band-pattern in the molecular layer of the cat cerebellum. , 1977, Journal of anatomy.

[103]  L. Eisenman,et al.  Parasagittal organization of mossy fiber collaterals in the cerebellum of the mouse , 1988, The Journal of comparative neurology.

[104]  R. Hawkes,et al.  Selective staining of a subset of Purkinje cells in the human cerebellum with monoclonal antibody mabQ113 , 1985, Journal of the Neurological Sciences.

[105]  R. Hawkes,et al.  Parasagittal organization of the rat cerebellar cortex: Direct comparison of purkinje cell compartments and the organization of the spinocerebellar projection , 1990, The Journal of comparative neurology.

[106]  B. B. Owens,et al.  Diversity among Purkinje cells in the monkey cerebellum. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[107]  O. Oscarsson.  Functional Organization of Spinocerebellar Paths , 1973 .

[108]  C. Sotelo,et al.  Asynchrony in the expression of guanosine 3′:5′-phosphate-dependent protein kinase by clusters of purkinje cells during the perinatal development of rat cerebellum , 1984, Neuroscience.