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Topography of Cerebellar Nuclear Projections to the Brain Stem in the Rat

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Topography of Cerebellar Nuclear Projections to the Brain Stem in the Rat NM. Gerrits, T.J.H. Ruigrok and C.L De Zeeuw (Eds.) Progress in Brain Research, Vol 124 © 2000 Elsevier Science BV, All rights reserved. CHAPTER 11 Topography of cerebellar nuclear projections to the brain stem in the rat T.M. Teune, J. van der Burg, J. van der Moer, J. Voogd and T.J.H. Ruigrok* Department of Anatomy, Erasmus University Rotterdam, PO. Box 1738, 3000 DR Rotterdam, The Netherlands Introduction Steen et al., 1994 ). As such, it would be expected that the output of these modules will reflect this The cerebellum has been implicated to be involved functional heterogeneity. in motor control (Bloedel, 1992; Ito, 1984), However, to our knowledge, a detailed and cognition (Leiner et al., 1986; Schmahmann, 1996; comprehensive anterograde tracer study of the Thach, 1996), affection and visceral functions nucleobulbar projections in the rat is not available. (Bradley et al., 1987; Haines et al., 1990; Nisimaru Reports by Faull (1978) and Faull and Carman et al., 1991; Waldrop and Iwamoto, 1991). To exert (Faull and Carmen, 1978) provide profiles of the these different functions, the cerebellar cortical distribution of nucleo-fugal projections, based on output is directed, via the cerebellar nuclei (CN), lesions and subsequent degeneration of the axons onto a large number of different brain stem nuclei of the superior cerebellar peduncle. Other inves- (see Voogd, 1995) as has been studied in different tigations into the cerebellar nuclear efferents only species [rat: (Chan-Palay, 1977; Faull, 1978; Faull concerned parts of these projections, such as the and Carman, 1978; Voogd, 1995); cat: (Voogd, projections of the CN to the inferior olive (Ruigrok 1964); monkey: (Asanuma et al., 1983)]. and Voogd, 1990), the red nucleus (Angaut et al., The output profile of the cerebellum is organized 1987; Daniel et al., 1987), the nucleus reticularis according to a modular pattern (Voogd, 1964; tegmenti pontis (Cicirata et al., 1982; Angaut et al., Oscarsson, 1969; Tolbert et al., 1978; Buisseret- 1985a) or the thalamus (Haroian et al., 1981; Delmas and Angaut, 1993). A module consists of Angaut et al., 1985b). Only for the output of the one or more parasagittally arranged strips of lateral cerebellar nucleus an overview of all brain Purkinje cells that project onto a specific subdivi- stem projections based on radioactive methionine sion of the CN, both of which receive information tracing has been provided by Chan-Palay (1977). A from a specific part of the contralateral inferior survey of some of the main brain stem targets of the olive. These olivo-cortico-nuclear modules have interface between the medial and interposed cer- been suggested to represent functional cerebellar ebellar nuclei was recently given by units (Oscarsson, 1979; Ekerot et al., 1995). In this Buisseret-Delmas and colleagues (1998). way, different modules are thought to be involved This chapter aims to provide a comprehensive in different tasks (Godschalk et al., 1994; van der overview of the nucleo-fugal projections in the rat, resulting from anterograde tracer deposits in differ- ent parts of the CN, thereby verifying and *Corresponding author. Tel.: +31 I0 408 7296; Fax: complementing results from the previously men- + 31 10 408 9459; e-mail: [email protected] tioned studies. 142 Materials and methods nomenclature and the subdivision of the red nucleus and the medial region of the mesodience- In this overview, the results of thirteen anterograde phalic junction we have followed Ruigrok and tracer injections, all made in the CN of adult, Cella (1995). The nomenclature will be further purpose-bred, male Wistar rats, will be presented considered in the discussion. Delineation of the rat and discussed. They were carefully selected out of CN is slightly modified after Korneliussen (1968; a batch of 85 cases. The iontophoretic tracer see also: Ruigrok and Voogd, 1990; Buisseret- injections were made with a glass micropipette Delmas and Angaut, 1993; Voogd, 1995). containing either Phaseolus vulgaris Leucoag- glutinin (PhaL) or biotinylated dextran amine Results (BDA). Details of surgical and immunohistochem- For easy reference and comparison between ical procedures are detailed elsewhere (Ruigrok selected cases, the location of the injection sites and Voogd, 1990; Teune et al., 1998). was indicated in standardized transverse drawings Serially collected transverse sections were ana- of the CN (Fig. 1). Both BDA and PhaL injection lysed with a microscope equipped with a LucividTM sites appeared as rounded, well-defined deposits of miniature monitor and NeurolucidaTM software. tracer substance from which labeled fiber bundles Contours, brain stem nuclei and main fiber tracts of emerged. Within the brain stem these fiber bundles equally spaced sections (spacing 320 Ixm of levels collateralized and showed terminal arborizations rostral to the decussation of the superior cerebellar which carried many varicosities. The location of peduncle and 640 Ixm of levels caudal to this point) the varicosities was indicated in the plots. In were plotted at low magnification (objective 2.5 × ). accordance with a report on the similarity of BDA Subsequently, at high magnification (objective and PhaL-tracing (Wouterlood and Jorritsma- 20x ), the sections were systematically scanned Byham, 1993), we noted no obvious differences in and the positions of all labeled varicosities were staining characteristics. However, based on the digitized by mouse clicks. Varicosities in both PhaL amount of labeled varicosities, BDA usually and BDA labeled fibers have been shown to reflect resulted in a smaller number of labeled terminal synaptic boutons (Wouterlood and Groenewegen, structures which most likely is related to the 1985; Wouterlood and Jorritsma-Byham, 1993) and somewhat smaller appearance of the injection site. thus represent the most likely sites where informa- The results presented below will be illustrated with tion is transmitted to postsynaptic structures. In this serial plots of actual sections and with the projec- way, for every plotted section, both the positions tion profiles which indicate the rostrocaudal levels and number of plotted terminals was determined of the brain stem that receive most prominent with reasonable accuracy. Only in areas with a very projections. An overview of the bulbar projections dense labeling such as occurring in the CN of all analysed cases is shown in Table 1. projections to the inferior olive or red nucleus is it likely that the number of plotted terminals repre- Bulbar projections from the medial cerebellar sents an underestimate of the actual number of nucleus labeled varicosities. The number of plotted varicos- ities and the analysed surface area of the section Three cases were selected with injections that were were used to design a bulbar projection profile of a confined to various parts of the medial cerebellar particular case. This profile indicates the relative nucleus (MCN: Fig. 1). The injection in case T195 amount of labeling along the rostrocaudal axis of (BDA) was restricted to its rostral half whereas the brain stem. Table 1, representing a survey of the case R100 (PhaL) centered on the caudal part of the results of all presented cases, was based on the nucleus. In an additional case (R127: PhaL) the computerized plots as well as on a supplement of injection was placed in the lateral aspect of the the actual sections. dorsolateral protuberance (DLP). Together, these Nomenclature of brain stem structures is mostly cases provide an impression of the targets of the based on Paxinos and Watson (1986). For the entire nucleus. 143 TABLE 1 Overview of all described cases indicating in which brain stem regions labeled varicosities were found. Large dot denotes dense labeling, small dot indicates only a minor projection, intermediate dot represents a fair projection. Question mark indicated that the area was not available for analysis; i indicates that the labeling was found ipsilateral to the injection site, otherwise the labeling was observed contralaterally MCN PIN AIN LCN T195 R127 R100 T82 T79 T108 R89 R98 1"77 T98 R178 T94 Medulla oblongata Inferior olive • • • • • O • O/'i O/.i O/'i Lateral reticular nucl. • i "i Nucl. of the solitary tract "i Parasolitary nucl. O/,i • • Medullary reticular nucl O/Oi • • Paramedian nucl Parr•celL retic nucL • i Oi • /Oi oi Gigantocell retic nucl O/Oi • • • • O/.i Lat paragigantocelL nucl O/.i Spinal trigem nucl, oral part • i -i Oi O/el ,i Spinal trigem nucl, interpolar part • i •i Oi oi .i Spinal tdgem nucl, caudal part .i Oi • i .i Superior vestibular nucl • /oi ./oi -/'i .i Lateral vestibular nucl • /el .i,i .i • i ,i Medial vestibular nucl rostral • /.i .i ./.i .i Medial vestibular nucl., caudal • /.i ./-i .i Spinal vestibular nucl. o/oi • "/,i oi NucL prep•situs hypoglossi Ol,i Metencephalon Basal pontine nuclei • D • • • Nucl. retic, tegm. pontis • • • • • A5 noradrenergic group (?) -i Oi oi ,i Principal sens. trig. nucl. Caud. pont retic, nucL • Otoi Oral pont. retic, nucL • o/,i O/.i Central gray pons O/.i • • Pedunculopentine tegm. nucl. .i • i • • Parabrachial nucL O/-i .[.i -i ,i Mesencephalon Red nucL, parvicellular Red nucl magnocelnular • O/.i Pararubral area Deep mesenceph nucl • • • • • Superior col/iculus, superficial Superior colliculus, intermediate • • Superior colliculus, deep o/.i • Ventral tegmental area Dorsal raphe nucleus Ventral tegm relay zone Medial access oculomot nucl • • • O/-i O/,i • • Interstitial nucl of Cajal • • o/,i Nucl of Darkschewitsch • • D Nucl parafasciculads prerubr • • O/,i Periaquaductal gray • • • • Nucl of post commissure • O/-i Anterior pretectal nucl • OI.i • Posterior pretectal nucl • •/.i • 144 TABLE 1--Continued MCN PIN AIN DLH LCN T195 R127 RIO0 T82 T79 T108 R89 R98 R138 T77 TU R178 T94 Diencephalon Mammillary nuclei Lateral hypothal, area O/•i • Dorsal hypothal, area O/.i • Zona incerta • • • • • • Ol'i O/•i Nucl. fields of Forel • • O/'i O/'i Ventral lat. geniculate nucl. Parafascicular thalam, nucl. • • O/'i • Central medial thalam, nucl, Laterodorsal thalam, nucl.
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