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Development and Developmental Disorders of the Human Cerebellum

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Development and Developmental Disorders of the Human Cerebellum Chapter 8 Development and Developmental Disorders of the Human Cerebellum Hans J.ten Donkelaar,Martin Lammens,Pieter Wesseling and Akira Hori 8.1 Introduction the human cerebellum. In this chapter the morpho- genesis and histogenesis of the cerebellum and the The cerebellum is one of the best studied parts of the precerebellar nuclei, the mechanisms involved, and brain. Its three-layered cortex and well-defined affer- the more frequent developmental disorders of the ent and efferent fibre connections make the cerebel- cerebellum, such as the Dandy–Walker anomaly and lum a favourite field for research on development and pontocerebellar hypoplasias, are discussed and illus- fibre connections of the central nervous system trated with MRI data and autopsy cases. (Voogd et al. 1996). The cerebellar cortex is com- posed of four main types of neurons: granule cells, Purkinje cells and two types of inhibitory interneu- 8.2 Some Notes on the Anatomy rons, the Golgi cells and the stellate/basket cells. The of the Cerebellum cortex receives three kinds of input: the mossy fibres (most afferent systems), the climbing fibres from the 8.2.1 Subdivision inferior olive, and diffusely organized monoaminer- gic and cholinergic fibres.The cerebellum plays a role Transverse fissures divide the cerebellum into lobes, not only in motor control but also in motor learning lobules and folia, whereas paramedian sulci separate and cognition (Middleton and Strick 1998; Marien et the median vermis from the hemispheres (Fig. 8.1). al.2001).The cerebellum develops over a long period, The flocculus and the nodule form the caudal floccu- extending from the early embryonic period until the first postnatal years. The main cell types of the cere- bellum arise at different times of development and at different locations. The Purkinje cells and the deep cerebellar nuclei arise from the ventricular zone of the metencephalic alar plate, whereas the granule cells are added from the rostral part of the rhombic lip, known as the upper rhombic lip. The caudal part of the rhombic lip (the lower rhombic lip) gives rise to the precerebellar nuclei, which include the pontine nuclei, the inferior olivary nucleus and some smaller nuclei with projections largely aimed at the cerebel- lum. Its protracted development makes the cerebellum vulnerable to a broad scala of developmental disor- ders, ranging from the Dandy–Walker and related malformations to medulloblastoma, a neoplasia of granule precursor cells (Friede 1989; Norman et al. 1995; Ramaeckers et al. 1997; Ramaeckers 2000; ten Donkelaar et al. 2003; Boltshauser 2004). Ultrasound and MRI allow detection of cerebellar malformations at an early stage of development (Kollias and Ball 1997; Barkovich 2000). Cerebellar anomalies, of the vermis in particular, have also been found in neu- robehavioural disorders such as autism and develop- mental dyslexia (Chap. 10). In mice, the molecular mechanisms of cerebellar development are rapidly being unravelled (Hatten et al. 1997; Goldowitz and Hamre 1998; Oberdick et al. 1998; Millen et al. 1999; Wang and Zoghbi 2001;Wingate 2001).Similar mech- Fig. 8.1 Median section (a) and detail (b) of human cerebel- anisms are likely to be involved in the development of lum (courtesy Gerard van Noort, Enschede) 310 Chapter 8 Normal and Abnormal Development of the Cerebellum intermediate zone consists of three C-zones, project- ing to the nucleus emboliformis (C1 and C3) and the nucleus globosus (C2). The large lateral zone (D- zone) innervates the nucleus dentatus. The lobus flocculonodularis innervates the vestibular nuclear complex. 8.2.2 Compartmentalization A modular organization of the cerebellar cortex is found in mammals and birds (Voogd 1967; Oscarsson 1980;Voogd and Bigaré 1980; Marani 1982; Feirabend 1983; Ito 1984; Feirabend and Voogd 1986; Voogd et al. 1990, 1996). Purkinje cells of a zone project to a particular cerebellar or vestibular target nucleus. Zones can extend across one or more lobules; some span the entire rostrocaudal length of the cerebellum (Fig. 8.2). The olivocerebellar projection is arranged in a similar way. Subnuclei of the inferior olive pro- ject to a single Purkinje-cell zone or to a pair of zones Fig. 8.2 Subdivision of the cerebellum. At the left, the spin- sharing the same target nucleus. These longitudinal ocerebellum is shown in light red and the vestibulocerebellum zones are not evident on the outside of the cerebel- in red.The remaining,non-coloured part forms the pontocere- lum.However,a system of compartments in the white bellum.A,B,C1,C2,C3,D longitudinal zones, De declive, DE den- matter, which contains the axons of the Purkinje cells tate nucleus, E emboliform nucleus, F fastigial nucleus, Fl floc- and the climbing fibres, can be visualized. Moreover, culus, Fol folium, G globose nucleus,LV lateral vestibular (Deit- a strong heterogeneity has been found in the expres- ers) nucleus, Nod nodulus, pf primary fissure, Pyr pyramis, Tub sion of certain proteins by subpopulations of Purkin- tuber, Uv uvula. (After Voogd 1995;Voogd et al. 1996) je cells, distributed in alternating longitudinal zones. This pattern, described by Scott (1964) and Marani lonodular lobe that is also known as the vestibulo- (1982) for the 5’-nucleotidase pattern (Fig. 8.3), and cerebellum or archicerebellum. This lobe receives pri- subsequently by Hawkes and Leclerc (1987) for the mary (from the vestibular organs) and secondary ‘zebrin’ epitope on the rat cerebellum, is shared by (from the vestibular nuclei) vestibular projections. the expression of several other proteins in Purkinje The corpus cerebelli, i.e. the vermis and the hemi- cells and in Bergmann glia (Voogd et al.1996; Herrup spheres, consists of the spinocerebellum (or paleo- and Kuemerle 1997). The antibodies zebrins I and II cerebellum) medially, and the pontocerebellum (or specifically stain a subset of Purkinje cells, distrib- neocerebellum) laterally. The spinocerebellum re- uted into multiple longitudinal zones and separated ceives projections from the spinal cord and trigemi- by zebrin-negative areas in rodents (Hawkes et al. nal system, whereas the pontocerebellum is innervat- 1985; Hawkes and Leclerc 1987), but not in macaque ed by pontocerebellar fibres. The fissura prima di- monkeys, where antibodies against zebrin stain all vides the cerebellar hemispheres into anterior and posterior lobes.The cerebellum is organized as longi- tudinal zones of Purkinje cells (A-, B-, C- and D- zones), each projecting to its own cerebellar nucleus (Fig. 8.2) and receiving input from different parts of the inferior olive (Voogd 1967, 1995, 2003, 2004; Voogd et al. 1996; Voogd and Glickstein 1998). The central cerebellar nuclei are the medial nucleus fastigii,the intermediate nucleus globosus and the nu- cleus emboliformis (together also known as the nucle- us interpositus), and the laterally situated, large nucleus dentatus. The vermis contains a medial zone (A-zone), projecting to the nucleus fastigii, and a small B-zone that innervates the lateral vestibular nucleus of Deiters. The cerebellar hemispheres can Fig. 8.3 5´-Nucleotidase pattern in the rat cerebellar cortex be divided into intermediate and lateral zones. The (from Marani 1982; courtesy Enrico Marani, Leiden) 8.2 Some Notes on the Anatomy of the Cerebellum 311 Fig. 8.4 Transverse, acetylcholinesterase-stained section of Fig. 8.5 Connections of the dentate and interposed nuclei.bc the anterior cerebellar lobe of the macaque monkey,showing brachium conjunctivum, cosp corticospinal tract, C1, C2, C3, D the modular organization of the cerebellum. A, B, C1, C2, C3, D1, longitudinal zones,DE dentate nucleus,E emboliform nucleus, D2, X longitudinal zones, bc brachium conjunctivum, cr corpus G globose nucleus, NRTP nucleus reticularis tegmenti pontis, restiforme,IntA nucleus interpositus anterior,m midline.(Kind- Rm magnocellular part of red nucleus,Rp parvocellular part of ly provided by Jan Voogd, Oegstgeest) red nucleus, rusp rubrospinal tract, thal thalamus, vm vermis, 4 primary motor cortex,6 premotor cortex.(After Voogd 1995) Purkinje cells (Leclerc et al.1990).In the human cere- bellaris medius or brachium pontis is formed by the bellum, no clear arrangement of zebrin I-stained massive pontocerebellar system. The pontine nuclei Purkinje cells was found (Plioplys et al. 1985).Acetyl- are innervated by the cerebral cortex via two tracts: cholinesterase (AChE) histochemistry is a useful the frontopontine tract from the frontal lobe, motor marker for the delineation of parasagittal compart- and premotor areas in particular,and the parietotem- ments in the cerebellum of adult mammals (Marani poro-occipitopontine tract, particularly arising in the and Voogd 1977; Hess and Voogd 1986; The borders somatosensory areas and the adjacent area 5. The pe- between compartments are selectively stained with dunculus cerebellaris superior contains the tractus AChE and this staining is especially distinct in mon- spinocerebellaris anterior and the main efferent sys- keys (Fig. 8.4). tem of the cerebellum, i.e. the brachium conjunc- tivum. The cerebellar nuclei are the output centres of the cerebellum. The targets of these nuclei differ con- 8.2.3 Major Fibre Connections siderably. The dentate and interposed nuclei mainly innervate the thalamus and the red nucleus, and Afferent and efferent fibre connections of the cere- control corticospinal and rubrospinal projections bellum pass through the cerebellar peduncles. The (Fig. 8.5). The fastigial nucleus and the nucleus of pedunculus cerebellaris inferior or corpus resti- Deiters control the reticulospinal and vestibulospinal forme contains cerebellar afferents: the tractus spin- projections (Fig. 8.6). The subdivision of descending ocerebellaris posterior and the fibrae cuneocerebel- supraspinal pathways into lateral and medial systems lares from the spinal cord, trigeminocerebellar fibres (Chap. 6) is therefore also found in the cerebellar from sensory trigeminal nuclei, olivocerebellar fibres control system. The dentate nucleus also has impor- and vestibulocerebellar fibres. The pedunculus cere- tant feedback loops to the cerebellum through the 312 Chapter 8 Normal and Abnormal Development of the Cerebellum Fig.
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