Neuroanatomy of the oculomotor system. Preface.
Explore the source record for details and available documents.
Animals↗
Biomedical subjects
Jean A Büttner-Ennever
Publications and source records attributed to Jean A Büttner-Ennever.
Histochemical differences between motoneurons supplying multiply and singly innervated extraocular muscle fibers.
The extraocular muscle fibers of vertebrates can be classified into two categories: singly innervated fibers (SIFs) and multiply innervated fibers (MIFs). In monkeys, the motoneurons of SIFs lie within the oculomotor, trochlear, and abducens nucleus, whereas the motoneurons of MIFs appear in separate subgroups in the periphery of the classical nuclei borders. In the present study, we investigated the histochemical properties of SIF and MIF motoneurons by using combined tract-tracing and immunofluorescence techniques. In monkeys, SIF and MIF motoneurons of extraocular muscles were identified by tracer injections into the belly or the distal myotendinous junction of the medial or lateral rectus muscle. Alternatively, the motoneurons were identified by choline acetyltransferase immunostaining. These techniques were combined with the detection of histochemical markers for perineuronal nets, nonphosphorylated neurofilaments, parvalbumin, or cytochrome oxidase. The experiments revealed that the MIF motoneurons in the periphery of the motonuclei do not contain nonphosphorylated neurofilaments or parvalbumin and lack perineuronal nets. In contrast, SIF motoneurons express all markers at high intensity. Cytochrome oxidase immunostaining was found in both motoneuron populations. An additional population of motoneurons with "MIF properties" was identified within the boundaries of the abducens nucleus, which could represent the motoneurons innervating MIFs in the orbital layer of lateral rectus muscle. Our data provide evidence that SIF and MIF motoneurons, which can be correlated with twitch motoneurons and presumed non-twitch motoneurons, differ in their histochemical properties. The absence of perineuronal nets, nonphosphorylated neurofilaments, and parvalbumin may help to identify the homologous MIF motoneurons in other species, including humans.
Animals↗
Spatial properties of central vestibular neurons of monkeys after bilateral lateral canal nerve section.
Thirty-seven neurons were recorded in the superior vestibular nucleus (SVN) of two cynomolgus monkeys 1-2 yr after bilateral lateral canal nerve section to test whether the central neurons had spatially adapted for the loss of lateral canal input. The absence of lateral canal function was verified with eye movement recordings. The relation of unit activity to the vertical canals was determined by oscillating the animals about a horizontal axis with the head in various orientations relative to the axis of rotation. Animals were also oscillated about a vertical axis while upright or tilted in pitch. In the second test, the vertical canals are maximally activated when the animals are tilted back about -50 degrees from the spatial upright and the lateral canals when the animals are tilted forward about 30 degrees . We reasoned that if central compensation occurred, the head orientation at which the response of the vertical canal-related neurons was maximal should be shifted toward the plane of the lateral canals. No lateral canal-related units were found after nerve section, and vertical canal-related units were found only in SVN not in the rostral medial vestibular nucleus. SVN canal-related units were maximally activated when the head was tilted back at -47 +/- 17 and -50 +/- 12 degrees (means +/- SD) in the two animals, close to the predicted orientation of the vertical canals. This indicated that spatial adaptation of vertical canal-related vestibular neurons had not occurred. There were substantial neck and/or otolith-related inputs activating the vertical canal-related neurons in the nerve-sectioned animals, which could have contributed to oculomotor compensation after nerve section.
Action Potentials↗
Palisade endings in extraocular eye muscles revealed by SNAP-25 immunoreactivity.
Palisade endings form a cuff of nerve terminals around the tip of muscle fibres. They are found only in extraocular muscles, but no definite evidence for their role in eye movements has been established. Palisade endings have been reported in all species so far investigated except the rat. In this study we demonstrate that antibodies against SNAP-25, the synaptosomal associated protein of 25 kDa, reliably visualize the complete motor, sensory and autonomic innervation of the extraocular muscles in human, monkey and rat. The SNAP-25 antibody can be combined with other immunofluorescence procedures, and is used here to study properties of palisade endings. With SNAP-25 immunolabelling putative palisade endings are identified in the rat for the first time. They are not well branched, but fulfil several criteria of palisade endings, being associated with non-twitch fibres as shown by double labelling with 'myosin heavy chain slow-twitch' antibodies. The putative palisade endings of the rat lack alpha-bungarotoxin binding, which implies that these synapses are sensory. If palisade endings are sensory then they could function as an eye muscle proprioceptor. They seem to be a general feature of all vertebrate eye muscles, unlike the other two extraocular proprioceptors, muscle spindles and Golgi tendon organs, the presence of which varies widely between species.
Animals↗
Proprioception and palisade endings in extraocular eye muscles.
Palisade endings occur only in extraocular muscles, and their function is unknown. They form a cuff of nerve terminals around the tips of muscle fibers. We describe here the advantages of using antibodies to a synaptosomal-associated protein (SNAP-25) to study properties of palisade endings in man, monkey, and rat. The stain can be combined readily with other immunofluorescence procedures, and results suggest that the synapses of palisade endings do not bind alpha-bungarotoxin (i.e., are not motor), nor do they contain substance P. These double-labeling data support the hypothesis that palisade endings are non-nociceptive sensory receptors, and could serve a proprioceptive function. With SNAP-25 immunolabeling, palisade endings were identified in the rat for the first time. Thus, palisade endings appear to be present in all vertebrate extraocular muscles studied to date. Their apparent universality, which contrasts with the more variable manifestation of extraocular muscle spindles and Golgi tendon organs, would be expected if proprioceptive feedback is necessary to the function of the ocular motor system, and if palisade endings are the critical proprioceptive structure.
Animals↗
Twitch and nontwitch motoneuron subgroups in the oculomotor nucleus of monkeys receive different afferent projections.
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.
Afferent Pathways↗
The neuroanatomical basis of oculomotor disorders: the dual motor control of extraocular muscles and its possible role in proprioception.
Current investigations show that two separate sets of motoneurons control the extraocular eye muscles, and that is there is a dual final common pathway. We propose that one set of motoneurons are the major source of tension generating eye movements, whereas the other may participate in a proprioceptive system concerned more with the exact alignment and stabilization of the eyes. In this article we discuss the structures that may participate in the proprioceptive circuits; and consider several recent publications in the light of this sensory feedback hypothesis, emphasizing the relevance to eye movement disorders.
Animals↗