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Collateralization of Descending Spinal Pathways from Red Nucleus and Other Brainstem Cell Groups in Rat, Cat and Monkey

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Collateralization of Descending Spinal Pathways from Red Nucleus and Other Brainstem Cell Groups in Rat, Cat and Monkey COLLATERALIZATION OF DESCENDING SPINAL PATHWAYS FROM RED NUCLEUS AND OTHER BRAINSTEM CELL GROUPS IN RAT, CAT AND MONKEY PROEFSCHRIFT TER VERKRIJGING VAN DE GRAAD VAN DOCTOR IN DE GENEESKUNDE AAN DE ERASMUS UNIVERSITEIT ROTTERDAM OP GEZAG VAN DE RECTOR MAGNIFICOS PROF. DR. J. SPERNA WEILAND EN VOLGENS BESLUIT VAN HET COLLEGE VAN DEKANEN. DE OPENBARE VERDEDIGING ZAL PLAATSVINDEN OP WOENSDAG 2 MAART 1983 DES NAMIDDAGS TE3.45 UUR DOOR ANNE-MARGRIET HUISMAN GEBOREN TE BREDA. ~------·---·- Med1scne emnom~eK. EU.R. druk: nkb-offscr bleiswiik-leiden Promotor : Prof. Dr. H.G.J.M. Kuypers Co-referenten: Prof. Dr. J. Voogd Prof. Dr. H.F.M. Busch aan Ale aan mijn ouders 5 Publications I. A.M. Huisman, H.G.J.M. Kuypers, C.A. Verburgh (1981) Quantitative diffe­ rences in collateralization of the descending spinal pathways from red nucleus and other brain stern cell groups in rat as demonstrated with the multiple fluorescent retrograde tracer technique. Brain Res. 209: 271-286. 2. A.M. Huisman, H.G.J.M. Kuypers, C.A. Verburgh (1982) Differences in col­ lateralization of the descending spinal pathways from red nucleus and other brain stern cell groups in cat and monkey. Progress in Brain Res. 57: 185-219. 3. A.M. Huisman, H.G.J.M. Kuypers, F. Conde, K. Keizer Collaterals of rubro­ spinal neurons to the cerebellum in rat. A retrograde fluorescent double labeling study. Brain Research (in press) 4. K. Keizer, H.G.J.M. Kuypers, A.M. Huisman Diarnidino Yellow (DY) a fluo­ rescent retrograde neuronal tracer, which migrates only very slowly out of the cell and can be used in combination with TB and FB in double labeling experiments. Submitted to Experimental Brain Research. 5. H.G.J.M. Kuypers, A.M. Huisman (1982) The new anatomy of the descending brain pathways. In 11 Brain Stern Control of Spinal Mechanisms" Fernstrom Foundation Series No. I New York-Oxford. 6. H.G.J.M. Kuypers, A.M. Huisman Fluorescent neuronal tracers. In 11 Advances in Cellular Neurobiology" Vol. 5: labeling methods applicable to the study of neuronal pathways (in press) The publications I, 2 and 3 are used in chapter III, IV and V of this thesis, with permission of Elsevier/North Holland Biomedical Press. Publication 6 is used in chapter II with permission of Academic Press, Ill Fifth Avenue, New York. 6 CONTENTS CHAPTER I: GENERAL INTRODUCTION I.!. red nucleus: anatomical aspects I. I.a. structure of the nucleus I. !.b. cytoarchitecture in rat I. I. c. cytoarchitecture ~n cat and monkey I. J.d. efferents of red nucleus I. I.e. afferents of red nucleus I.2. red nucleus: physiological aspects I.2.a. function of the rubrospinal pathway as one of the descending brainstem pathways I.2.b. physiology of the rubrospinal tract as the primary component of the laterally descending brainstem pathways I.3. aims and scope of the present investigations I. 4. references CHAPTER II: FLUORESCENT NEURONAL TRACERS CHAPTER III: QUANTITATIVE DIFFERENCES IN COLLATERALIZATION OF THE DESCENDING SPINAL PATHWAYS FROM RED NUCLEUS AND OTHER BRAIN STEM CELL GROUPS IN RAT AS DEMONSTRATED WITH THE MULTIPLE FLUORESCENT RETROGRADE TRACER TECHNIQUE. CHAPTER IV: DIFFERENCES IN COLLATERALIZATION OF THE DESCENDING SPINAL PATHWAYS FROM RED NUCLEUS AND OTHER BRAIN STEM CELL GROUPS IN CAT AND MONKEY. CHAPTER V: COLLATERALS OF RUBROSPINAL NEURONS TO THE CEREBELLUM IN RAT. A RETROGRADE FLUORESCENT DOUBLE LABELING STUDY. 7 CHAPTER VI: GENERAL DISCUSSlON VI. I . Technique VI.2. The rubrospinal tract in rat, cat and monkey VI.2.a. somatotopic organization of red nucleus VI.2.b. collateralization of the rubro­ spinal tract in rat, cat and monkey VI.2.c. collateralization of the rubro­ spinal tract compared with the collateralization of the raphe­ spinal and ventrolateral pontine tegmentum-spinal tracts in rat, cat and monkey VI.2.d. collateralization of the rubro­ spinal tract to the cerebellum. VI.3. references Summary Samenvatting voor leken List of abbreviations Dankwoord Curriculum vitae 8 CHAPTER I: GENERAL INTRODUCTION I.!. red nucleus: anatomical aspects I. I.a. structure of the nucleus I.l.b. cytoarchitecture ln rat I. I.e. cytoarchitecture ln cat and monkey I. I. d. efferents of red nucleus I. I.e. afferents of red nucleus I.2. red nucleus: physiological aspects I.2.a. function of the rubrospinal pathway as one of the descending brainstem pathways I.2.b. physiology of the rubrospinal tract as the primary component of the laterally descending brainstem pathways I.3. aims and scope of the present investigations I.4. references 9 I. I. Red Nucleus: anatomical aspects I.l.a. Structure of the· nucleus The red nucleus is located centrally in the mesencephalic tegmentu~ In the human brain the most conspicious gross feature of the red nucleus is its pinkish-red color in fresh sections. This is due to the high vascularity of the nucleus (Hough and Wolff, 1939) which distinguishes it from the surrounding structures. Its 11 capsule" is formed by fibers of the superior cerebellar peduncle, which sur­ round and traverse the nucleus and by the oculomotor nerve which runs along the medial aspect of the nucleus (Carpenter, 1956). Using the Golgi and Nissl techniques, Cajal (1952) described three types of neurons in the red nucleus based on their size: large neurons, medium sized neurons and small neurons. Hatschek was the first who recognized that the red nucleus was divided in a magna­ and parvicellular part (Hatschek, 1907). In humans the red nucleus is mainly composed of small neurons with only relatively few magna­ cellular neurons, the latter of which are located at the caudal pole of the nucleus (Ariens-Kappers et al., 1960; de Lange, 1912; Ten Donkelaar, 1976a; Masion, 1967). In monkey the red nucleus can readily be subdivided into a caudal magnocellular portion and a rostral parvicellular portion. At the meso-diencephalic junction the latter is located lateral to the fasciculus retroflexus. How­ ever, in lower mammals no such a strict distinction between a magna­ cellular and a parvicellular portion can be made, although also in these species large neurons are more numerous in the caudal parts of the nucleus and small neurons predominate in its rostral parts. In birds and reptiles the red nucleus consists of large cells only. Rats, cats, monkeys, apes and humans have a magna- and parvicellu­ lar part. From rat to cat, from cat to monkey and from monkey to human the relative size of the magnocellular part decreases, and the relative size of the parvicellular part increases. These t'vo principal subdivisions of the red nucleus have their own efferent pathways. Thus the caudal magnocellular part gives rise to projections to the cerebellum, the lower brainstem and the spinal cord, while the rostral parvicellular part projects to the inferior olive and possibly the thalamus. However, the segregation in a caudal red nucleus projecting to the cerebellum, the lower 10 brainstem and the spinal cord and a rostral red nucleus projecting to the inferior olive is a relative one, such that for the rubro­ spinal and rubrocerebellar neurons only a rostrocaudal gradient exists. This was shown by the fact that in cat rubrospinal and rubrocerebellar neurons are located throughout the rostrocaudal extent of the nucleus but that they are concentrated in the caudal half (Brodal and Gogstad, 1954; Pompeiano and Brodal, 1957), and that both sets of neurons comprise large as well as medium and small sized cells. I.l.b. cytoarchitecture in rat In cross-sections the caudal half of the nucleus is egg shaped and consists of large (soma diameter 40 ym, giant neurons) and medium sized (soma diameter 25-40 ym) neurons. The medium sized neurons are most numerous, but a considerable number of large neurons is also present, particularly in the caudal pole of the nucleus, where they are more numerous than in any other part (Reid et al., 1975). The rostral half of the nucleus is composed of predominantly small neurons (soma diameter 25 ym) with a scattering of medium sized ones and caudally in this rostral part also some large ones. In the most caudal part of this rostral half a population of neurons, designated the lateral horn (Reid et al., 1975) extends from the ventral surface of the nucleus dorsally along its lateral aspect. This subgroup contains predominantly small and medium sized neurons, but also some large ones. This lateral horn in rat is not analogous to the nucleus minimus of Von Monakow (1910) in cat, which sub­ nucleus is located dorsolateral to the red nucleus and consists of very small neurons (soma diameter 6-8 ym) (Massion, 1967). The portion of the red nucleus which contains large neurons and there­ fore is designated the magnocellular portion, occupies the caudal three fourth of the nucleus. The rostral pole of the nucleus in rat blends imperceptively with the prerubral field and this part of the nucleus is cytoarchitectonically difficult to demarcate (Reid et al., 1975). I.l.c. cytoarchitecture in cat and monkey In cat the caudal magnocellular part of the red nucleus occupies the caudal two thirds of the nucleus but ln monkey it seems relatively smaller and occupies only the caudal half. In both species the 11 caudal portion of the magnocellular part of the red nucleus is round in cross-section and contains large neurons which are dispersed between the tegmental fiber bundles. The rostral portion of the magnocellular red nucleus in monkey is also round in cross-section but contains mainly medium sized neurons. In cat this rostral portion of the magnocellular part as seen Ln cross-section has the shape of a flattened disc and contains both large and small neurons.
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