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Descending Motor Pathways and the Spinal Motor System. Limbic and Non-Limbic Components

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Descending motor pathways and the spinal motor system. Limbic and non-limbic components Descenderende motorische baansystemen en het spinale motorische systeem. Limbische en niet limbische componenten Proefschrift Ter verkrijging van de graad van doctor aan de Erasmus Universiteit Rotterdam op gezag van de Rector Magnificus Prof. Dr. C.J. Rijnvos en volgens besluit van het College van Dekanen. De openbare verdediging zal plaats vinden op woensdag 19 september 1990 om 15.45 uur door Gerrit Holstege Geboren te Warnsveld PROMOTIECOMMISSIE Promotoren: Prof. Dr. H. Collewijn Prof. Dr. J. Voogd Overige leden: Prof. Dr. R. Nieuwenhuys Afd. Anatomie, Katholieke Universiteit . Nijmegen Prof. Dr. HJ. Ralston ill Dept. Anatomy, University of California San Francisco Het schrijven van dit proefschrift werd mede mogelijk gemaakt door een NASA Grant (NCC 2- 491) aan Gert Holstege. Ontwerp omslag: R.D.E. Oxenaar Aan Marianne Aan Henne, Floor en Gert Jan Dit proefschrift is identiek aan het laatste hoofdstuk van een in 1991 te verschijnen deel van Progress in Brain Research: "Role of the forebrain in sensation and behavior", (Ed. G. Holstege), Elsevier Science Publishers B.V. Amsterdam Nederland. Dit deel van Progress in Brain Research zal de voordrachten bevatten van de .sprekers op het congres, gehouden op 26 en 27 mei 1989 op NASA/Ames Research Center, Moffett Field California, ter gelegenheid van het afscheid van William R. Mehler als senior scientist op NASA/ Ames. De lay-out van dit proefschrift werd vervaardigd op een Apple Macintosh !lei computer met behulp van het programma Pagemaker en Adobe illus­ trator 88. Table of Contents 2. Local projections to motoneurons 13 A. Introduction 4 a. Recurrent motoneuronal axon collateral projections to motoneurons 13 B. Description of the spinal mo­ b. Muscle spindle afferent projections to tor system and the descend- motoneurons 14 ing motor pathways. 4 L Muscle spindle afferent projections to motoneurons in the spinal cord 14 2. Muscle spindle afferent projections 1 Somatic and autonomic motoneu- to motoneurons in the brainstem 15 . rons in spinal cord and brainstem 4 c. Propriospinal pathways 15 a. Somatic motoneurons in the L Projections from interneurons 15 spinal cord 4 2. Projections from propriospinal L Upper cervical cord 4 neurons 17 2. Phrenic nucleus 5 2a. Propriospinal neurons as rhythm 3. Cervical enlargement 6 generators 20 4. Thoracic and upper lumbar spinal 3. Long propriospinal projections 20 cord 7 4. Specific propriospinal projections 21 5. Lumbosacral enlargement 8 5. Absence of propriospinal projec- 6. Nucleus of Onuf 8 tions to certain motor nuclei 21 Sa. CTM motor nucleus 21 b. Autonomic motoneurons in the spinal Sb. Phrenic nucleus 22 cord 9 Sc. Onuf's nucleus 22 1. Sympathetic preganglionic mo- toneurons 9 d. Propriobulbar pathways 23 2. Parasympathetic preganglionic mo- L Interneuronal projections to the toneurons 10 motor trigeminal nucleus 24 2. Interneuronal projections to the c. Somatic motoneurons in the brainstem 10 hypoglossal nucleus 25 1. Extra-ocular muscle and retractor 3. Interneuronal projections to the bulbi motoneuronal cell groups 10 facial nucleus 25 2. Jaw closing and opening muscle 3a. Interneuronal projections to the motoneurons 11 ear- and platysma muscle mo­ 3. Facial muscle motoneurons 11 toneuronal cell groups 25 4. Middle ear muscle motoneurons 11 3b. Interneuronal projections to the 5. Somatic motoneurons belonging to orbicularis oculi and retractor bulbi the nucleus ambiguus 11 muscle motoneuronal cell groups 6. Tongue muscle motoneurons 12 and the neuronal organization of the blink reflex 25 d. Autonomic (parasympathetic) pregan­ 3c. Interneuronal projections to the glionic motoneurons in the brainstem 12 motoneurons of the peri-oral 1. Preganglionic motoneurons inner­ muscles 29 vating iris and lens via ciliary 4 Interneuronal projections to the ganglion 12 dorsal group of the nucleus 2. Preganglionic motoneurons inner­ ambiguus 29 vating salivatory and lacrimal glands 12 3. Bulbospinal intemeurons projecting to 3_ Preganglionic motoneurons inner­ motoneurons 31 vating the visceral organs 12 a. Pathways involved in respiratory control 31 2 1. Projections to the phrenic nucleus 31 lb. The rubro-olivary projections 58 la. Projections from the ventrolateral 2. The corticobulbar and corticospi- nucleus of the solitary tract 31 nal pathways 58 lb. Projections from the para-ambiguus nucleus/rostral nucleus retroam- 5. Descending pathways involved in biguus 32 limbic motor control systems 62 lc. Projections from the Botzinger complex 33 a. Introduction 62 ld. Projections from the ventrolateral parabrachial nuclei and nucleus b. Pathways projecting diffusely to the Kolliker-Fuse 33 spinal gray matter 63 2. Projections to the intercostal l. Projections from the nuclei raphe motoneurons 34 magnus [NRM), pallidus [NRP)and 3. Projections to the cutaneus trunci, obscurus and the ventral part of the bdominal muscle and pelvic floor caudal pontine and medullary motor nuclei 35 medial reticular formation 63 2. Projections from the dorsolateral b. Pathways involved in micturition pontine tegmental field (A7 cell control 37 group) 67 3. Projections from the pontine lateral c. Pathways specifically involved in tegmentum [paralemniscal reticu- cardiovascular control 41 lar formation) 68 4. Projections from the rostral mesen- 4. Descending pathways of somatic cephal on/caudal hypothalamus motor control systems 43 (All cell group) 69 a. The medial descending system 45 c. Projections from the mesencephalon to l. Pathways involved in regulating caudal brainstem and spinal cord 69 axial and proximal body move- l. Descending projections to the ments 45 NRM, NRP and ventral part of the 2. Pathways involved in regulating caudal pontine and medullary me- eye- and head movements 46 dial tegmentum 69 2a. Projections of Field H of Forel and la. Involvement of the descending interstitial nucleus of Cajal and mesencephalic projections in surrounding areas (INC-RF) 47 control of nociception 69 2b. Projections from the colliculus lb. Involvement of the descending superior 47 mesencephalic projections in the 2c. Spinal projections from the lateral lordosis reflex 72 periaqueductal gray (PAG) and lc. Involvement of the descending adjacent mesencephalic tegmen- mesencephalic projections in tum 49 locomotion 73 2d. Spinal projections from the pontine 2. Periaqueductal gray (PA G) projec- and medullary medial tegmental tions to the ventrolateral medulla; field 49 involvement in blood pressure 2e. Spinal projections from the vesti- control 74 bular nuclei 51 3. PAG projections to the nucleus 2f. Concluding remarks regarding the retroambiguus; involvement in vo- descending pathways involved in calization 74 regulating head movements 52 4. PAG projections to the spinal cord 75 b. The lateral descending system 53 d. Projections from the hypothalamus to 1. The rubrobulbar and rubrospinal caudal brainstem and spinal cord 76 system 53 1. Projections from the anterior la. The rubrobulbospinal projections 53 hypothalamus/preoptic area 76 3 2. Projections from the paraventricu- lar hypothalamic nucleus [PVN) 77 3. Projections from the medial part of the posterior hypothalamic area 81 4. Projections from the lateral hypothalamic area 81 e. Projections from amygdala and bed nu- deus of the stria terminalis to caudal brainstem and spinal cord 84 f. Projections from the prefrontal cortex to caudal brainstem and spinal cord 87 C. Conclusions 89 L The first motor system 89 2. The second motor system 89 3. The third motor system 91 D. Acknowledgements 92 E. Abbreviations 93 F. Conclusies 96 L Het eerste motorische systeem 96 2. Het tweede motorische systeem 97 3. Het derde motorische systeem 97 G. References 99 H. Verantwoording 118 I. Curriculum Vitae 119 4 A. Introduction For a thorough understanding of the descending concept the motoneurons will be considered to pathways of the motor system originating in the belong to the peripheral motor system, (motor forebrain, knowledge about the anatomy and func­ unit, which is the motoneuronal cell body-motor tion of the structures in the more caudally located axon-muscle). The first motor system consists of parts of the central nervous system is indispen­ the interneurons involved in motor reflex path­ sable. In this paper an overview will be presented ways. The second motor system contains the of these caudal structures in brainstem and spinal pathways of the so-called somatic motor system, cord as far as they concern the motor system, while the third motor system comprises the motor (sections 1 to 3). After that the descending path­ pathways related to the limbic system. The sec­ ways belonging to the so-called somatic motor ond and third motor systems act upon the neurons system are reviewed (section 4). Finally, a sum­ of the first motor system and to a limited extent mary of the many newly discovered pathways directly on motoneurons, but not on each other. related to the limbic system will be given (section The importance and strength of the third motor 5). In the Conclusions section a concept will be system, which, untill recendy, was virtually un­ presented, which subdivides the multitude of known, will be emphasized motor pathways into three motor systems. In this B. Description of the spinal motor system and the de­ scending motor pathways L Somatic and autonomic motoneurons in spinal cord and brainstem la. Somatic motoneurons in the spinal lumbosacral lateral column innervate the muscles cord of the fore- and hind-limbs respectively. The
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