The sources of monosynaptic input to "fast" and "slow" abducens motoneurons (MNs) were revealed in primates by retrograde transneuronal tracing with rabies virus after injection either into the distal or central portions of the lateral rectus (LR) muscle, containing, respectively, "en grappe" endplates innervating slow muscle fibers or "en plaque" motor endplates innervating fast fibers. Rabies uptake involved exclusively motor endplates within the injected portion of the muscle. At 2.5 days after injections, remarkable differences of innervation of slow and fast MNs were demonstrated. Premotor connectivity of slow MNs, revealed here for the first time, involves mainly the supraoculomotor area, central mesencephalic reticular formation, and portions of medial vestibular and prepositus hypoglossi nuclei carrying eye position and smooth pursuit signals. Results suggest that slow MNs are involved exclusively in slow eye movements (vergence and possibly smooth pursuit), muscle length stabilization and gaze holding (fixation), and rule out their participation in fast eye movements (saccades, vestibulo-ocular reflex). By contrast, all known monosynaptic pathways to LR MNs innervate fast MNs, showing their participation in the entire horizontal eye movements repertoire. Hitherto unknown monosynaptic connections were also revealed, such as those derived from the central mesencephalic reticular formation and vertical eye movements pathways (Y group, interstitial nucleus of Cajal, rostral interstitial nucleus of the medial longitudinal fasciculus). The different connectivity of fast and slow MNs parallel differences in properties of muscle fibers that they innervate, suggesting that muscle fibers properties, rather than being self-determined, are the result of differences of their premotor innervation.
Eye muscle fibers can be divided into two categories: nontwitch, multiply innervated muscle fibers (MIFs), and twitch, singly innervated muscle fibers (SIFs). We investigated the location of motoneurons supplying SIFs and MIFs in the six extraocular muscles of monkeys. Injections of retrograde tracers into eye muscles were placed either centrally, within the central SIF endplate zone; in an intermediate zone, outside the SIF endplate zone, targeting MIF endplates along the length of muscle fiber; or distally, into the myotendinous junction containing palisade endings. Central injections labeled large motoneurons within the abducens, trochlear or oculomotor nucleus, and smaller motoneurons lying mainly around the periphery of the motor nuclei. Intermediate injections labeled some large motoneurons within the motor nuclei but also labeled many peripheral motoneurons. Distal injections labeled small and medium-large peripheral neurons strongly and almost exclusively. The peripheral neurons labeled from the lateral rectus muscle surround the medial half of the abducens nucleus: from superior oblique, they form a cap over the dorsal trochlear nucleus; from inferior oblique and superior rectus, they are scattered bilaterally around the midline, between the oculomotor nucleus; from both medial and inferior rectus, they lie mainly in the C-group, on the dorsomedial border of oculomotor nucleus. In the medial rectus distal injections, a "C-group extension" extended up to the Edinger-Westphal nucleus and labeled dendrites within the supraoculomotor area. We conclude that large motoneurons within the motor nuclei innervate twitch fibers, whereas smaller motoneurons around the periphery innervate nontwitch, MIF fibers. The peripheral subgroups also contain medium-large neurons which may be associated with the palisade endings of global MIFs. The role of MIFs in eye movements is unclear, but the concept of a final common pathway must now be reconsidered.
No abstract
Physiological experiments show that the abducens internuclear pathway is involved in the activation of only the medial rectus (MR) eye muscle. Previous anatomical experiments have shown that this pathway terminates in multiple foci within the oculomotor nucleus (OMN) of the monkey, and not only over the classical motoneuron subgroup. In this study the location of MR motoneurons in the monkey OMN is reinvestigated, and compared with the detailed pattern of terminations of the abducens internuclear pathway. The motoneurons were labelled by injections of retrograde tracer substances, HRP and [125I] wheat germ agglutinin (WGA), into extraocular muscles. Labelled MR motoneurons were found in three main divisions, called subgroup A, B, and C. Subgroup A corresponds mainly to the classical ventral MR subgroup. Subgroup B lies dorsal and caudal in OMN, occupying an area classically reserved for inferior rectus (IR). However, the representation of IR is shown to be further rostral in the dorsal OMN. Subgroup C is on the dorsomedial border of OMN. Its cells are significantly smaller than those of Group A and B. In addition C could be labelled independently of the other subgroups by small injections into the outer (orbital) layer of MR muscle. This indicates a functional difference between the subgroups. It is suggested that subgroup C may be important for the tonic component of MR activity, possibly convergence. The location of abducens internuclear terminals, labelled by the injection of tritiated amino acids into the abducens nucleus, corresponds exactly to the position of MR motoneurons. These experiments provide a new picture of the internal OMN organization, and support the physiological findings that the abducens internuclear pathway activates only MR motoneurons.
The rostral interstitial nucleus of the medial longitudinal fasciculus in known to participate in the generation of fast vertical eye movements in the monkey. A cell group homologous to this nucleus has been identified in the human brain. In man the nucleus lies dorsomedial to the anterior pole of the red nucleus, rostral to the interstitial nucleus of Cajal, and lateral to the nucleus of Darkschewitsch. Reconstructions of lesions in patients with different types of vertical gaze paralysis show that destruction of the rostral interstitial nucleus of the MLF bilaterally leads to an impairment of fast vertical eye movements. We propose that the nucleus participates in the production of vertical saccades and quick phases of nystagmus in man. Preservation of its integrity is not necessary for the production of vestibular compensatory eye movements in the vertical plane.
This article is dedicated with great respect to Parviz Mehraein, Professor of Neuropathology, University of Munich, on the occasion of his 60th birthday. INTRODUCTIONThere have been several recent reviews on the neuroanatomy of the vestibular nuclei, describing their cytoarchitecture, location, nomenclature, and connections.'-' But it is still very difficult to relate the anatomy to the functions of the vestibular nuclei, such as their role in smooth pursuit eye movements, the velocity storage mcchanism, adaptation of the vestibuloocular reflex (VOR), the common neural integrator, and the role in optokinetic responses.' The reason is that the information available to do this is meager, and widely scattered. Any attempt to localize function reveals only a few consistent patterns, and these unfortunately do not conform to any ncuroanatomical borders. In this review the more basic patterns of connectivity in the vestibular nuclei will be described. These relate almost exclusively to labyrinthine canal sinals since there is very little information on otolith pathways.The diagramatic outlines of the vestibular nuclei in the horizontal plane that are used in many of the following diagrams roughly represent the arrangement in mammals. The ventromedial border of the lateral vestibular nucleus (Iv) has been drawn so that the smaller-celled region containing many secondary vestibular neurons [the ventrolateral nucleus, or the magnocellular subdivision of the medial vestibular nucleus (mv)] lies within the boundaries of the mv. VESTIBULAR NERVE AFFERENTSThe primary (1") vestibular afferents in the VIIIth nerve enter the medulla at the level of the lateral vestibular nucleus. Nearly every fiber divides at this point and sends one descending branch to terminate in the medial and inferior vestibular nuclei (mv and iv), and an ascending branch to the superior vestibular nucleus (sv) where it gives off branches before continuing on to the cerebellum. These fibers project to the anterior and posterior vermis bilaterally, the major input being to the nodulus (lobe X) and the lobule IXd of the uvula. There are conflicting reports of the input to the flocculus; if it is present it is very sma1L6 FIGURE 1 represents a generalized summary of the termination sites of primary afferents found in several studies,'-' including the terminal branches of a single "This work was supported by the Deutsche Forschungsgemeinschaft SFB 220/D8. 'Address all correspondence to the Institute of Physiology, University of Munich, Pettenkofferstr. 12, D-8000 Munich 2, Germany. 363 364 ANNALS NEW YORK ACADEMY OF SCIENCES 1 AFFERENTS FIGURE 1. The pattern of vestibular nerve termination in the vestibular nuclei, generalized from studies that disagree on several points." The canal projections are represented by stripes (HC and AC) and dots (PC), the utricular input by open circles, and sacculus by triangles. Only one area (zone I) receives inputs from all canals and otoliths.In sv the canal afferents each have individual sites of termination, and project to ...
Motoneurons in the primate oculomotor nucleus can be divided into two categories, those supplying twitch muscle fibers and those supplying nontwitch muscle fibers. Recent studies have shown that twitch motoneurons lie within the classical oculomotor nucleus (nIII), and nontwitch motoneurons lie around the borders. Nontwitch motoneurons of medial and inferior rectus are in the C group dorsomedial to nIII, whereas those of inferior oblique and superior rectus lie near the midline are in the S group. In this anatomical study, afferents to the twitch and nontwitch subgroups of nIII have been anterogradely labeled by injections of tritiated leucine into three areas and compared. 1) Abducens nucleus injections gave rise to silver grain deposits over all medial rectus subgroups, both twitch and nontwitch. 2) Laterally placed vestibular complex injections that included the central superior vestibular nucleus labeled projections only in twitch motoneuron subgroups. However, injections into the parvocellular medial vestibular nucleus (mvp), or Y group, resulted in labeled terminals over both twitch and nontwitch motoneurons. 3) Pretectal injections that included the nucleus of the optic tract (NOT), and the olivary pretectal nucleus (OLN), labeled terminals only over nontwitch motoneurons, in the contralateral C group and in the S group. Our study demonstrates that twitch and nontwitch motoneuron subgroups do not receive identical afferent inputs. They can be controlled either in parallel, or independently, suggesting that they have basically different functions. We propose that twitch motoneurons primarily drive eye movements and nontwitch motoneurons the tonic muscle activity, as in gaze holding and vergence, possibly involving a proprioceptive feedback system.
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