Medial Superior Olivary Nucleus Research Articles

Auditory brainstem anomalies in albino cats: II. Neuronal atrophy in the superior olive.

In a previous paper (Brain Res., 260:1-9, 1983) we reported that albino cats show abnormal auditory brainstem evoked responses that appear to arise from structural defects in or near the superior olivary complex. In the present study, neuronal cross-sectional area in brainstem nuclei was compared in albino and normally pigmented adult cats. The albinos were true tyrosinase-negative (cc) and should not be confused with the deaf white cat (W); the albinos are not deaf. Neurons in the medial superior olivary nucleus (MSO) of albinos were, on average, 41% smaller than in pigmented animals; there was no overlap in the neuronal size distributions for the two groups of animals. Cell size in the lateral superior olive, medial nucleus of the trapezoid body, ventral nucleus of the lateral lemniscus, anteroventral cochlear nucleus, dorsal cochlear nucleus, and facial nucleus was also smaller (by 9-21%) in albinos than in pigmented animals but none of these differences was statistically reliable. In the abducens nucleus, neurons were 12% larger in albinos than in pigmented animals, demonstrating that neuronal size in the albinos is not uniformly smaller. Several lines of evidence suggest that the auditory system defects in albinos are related to abnormal pigmentation rather than to other gene effects. It is possible that a subtle pigment-related disruption of inner ear development in albinos results in a central cascade of atrophic changes along the auditory pathway.

Organization of the efferent projections of the medial superior olivary nucleus in the cat as revealed by HRP and autoradiographic tracing methods.

Features of the organization of the efferent axonal projections from the medial superior olivary nucleus (MSO) in the cat were studied. In order to determine the origin and distribution of projections from MSO, the retrograde horseradish peroxidase (HRP) and autoradiographic tracing methods were used. The results showed that (1) in both HRP and autoradiographic studies the projection to the inferior colliculus was largely ipsilateral, although a contralateral component was present; (2) the projection field of MSO was confined to the ventral division of the central nucleus of the inferior colliculus, and within this field the labeling was heavier in the rostral and dorsolateral parts of the ventral division; (3) the projection to the inferior colliculus was topographic with ventral parts of MSO projecting ventrally and dorsal parts of MSO projecting dorsolaterally; (4) the projection field in the central nucleus formed successive laminae oriented from ventrolateral to dorsomedial; (5) the axonal course was via the medial or internal segment of the lateral lemniscus; and (6) some fibers in this course ended additionally within the dorsal nucleus of the lateral lemniscus. This latter projection was also topographically organized. These observations supported previously described features of lamination and tonotopic order for afferents of the inferior colliculus, as well as recent suggestions that functional segregation of afferent connections exists within the laminated portion of the central nucleus of the inferior colliculus.

Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex.

An anterograde tracer (35S-methionine) was injected unilaterally in the superior olivary complex (SOC) at regions previously demonstrated by retrograde labeling to contain olivocochlear (OC) cell bodies. Quantitative analysis of cochlear autoradiographs from these cats demonstrates that there are two OC systems. The lateral OC system has cell bodies lateral to the medial superior olivary nucleus (MSO) and projects to the inner hair cell (IHC) region bilaterally (mostly ipsilaterally). The medial OC system has cell bodies medial, ventral, and anterior to the MSO and projects to the outer hair cell (OHC) region bilaterally (mostly contralaterally). A single medial OC neuron innervates many small patches of OHCs with substantial gaps between the patches. Medial OC neurons also appear to project to the IHC region to a small extent. A review of the literature with the medial-lateral division of OC efferents in mind reveals many differences between these two systems. In particular, lateral OC axons are unmyelinated and innervate the dendrites of radial afferent fibers under IHCs, whereas medial OC axons are myelinated and directly innervate OHCs. Although both systems appear to be cholinergic, the lateral OC system also shows met-enkephalin-like immunoreactivity. The synapses of the medial OC system are formed in development before those of the lateral OC system and they degenerate more slowly after the OC axons are cut. The many differences between these two OC systems suggest that they are functionally separate systems.

The auditory brainstem nuclei and some of their projections to the inferior colliculus in the North American opossum

Afferent projections to the inferior colliculus in the North American opossum have been examined using the retrograde transport of horseradish peroxidase. Projections to primarily the contralateral inferior colliculus arise in the dorsal and ventral cochlear nuclei, the auditory nerve nucleus and the spinal trigeminal nucleus pars caudalis, while ipsilateral projections arise in the superior paraolivary nucleus, the ventral nucleus of the trapezoid body, the ventral nucleus of the lateral lemniscus, the paralemniscal nucleus, the deep layer of the superior colliculus and the parabrachial nucleus. Bilateral projections to the inferior colliculus originate within the dorsal column nuclei, the nucleus reticularis gigantocellularis pars ventralis, the lateral and medial superior olivary nuclei, the dorsal nucleus of the lateral lemniscus and the auditory cortex. Nissl, fiber and Golgi-stained preparations were used to study the neuronal organization of those auditory nuclei with projections to the inferior colliculus. Anterograde axonal degeneration and transport techniques revealed that the inferior colliculus is innervated differentially by the dorsal and ventral cochlear nucleus, the superior olivary complex and the auditory neocortex. Axons from the contralateral dorsal cochlear nucleus and the ipsilateral superior olivary complex innervate both the central nucleus and external cortex, whereas those from ventral cochlear nucleus and contralateral, superior olivary complex project to only the central nucleus. Projections from auditory cortex form the complement of those from the cochlear nuclei and superior olivary complex, that is, they terminate in a thin band overlying the dorsal cortex and the superficial layer of external cortex. Our results have been compared with those obtained from eutherian mammals and it is clear that there are striking similarities in neuronal organization and connectivity. Since the opossum is born 12 days after conception and has an extended development in an external pouch, it may be suited for developmental studies of the mammalian auditory connections and the behaviors dependent of them.

Neuron morphology and synaptic architecture in the medial superior olivary nucleus. Light- and electron microscope studies in the cat.

Dendritic arborization pattern, spatial and synaptic relations of various neuron types and the terminal distribution of afferent axons of various origin were studied in the medial superior olivary nucleus of the cat using Golgi, degeneration, electron microscope and horseradish peroxidase techniques. Three types of neurons clearly different in morphological features, distribution, neighbourhood relations, input and output characteristics were distinguished: (1) fusiform cells having specific dendritic orientations and arborization patterns and synaptic relations to various types of terminal axon arborizations (2) multipolar neurons with wavy dendrites bearing spine-like appendages, receiving relatively few synaptic contacts and having a locally arborizing axon, and (3) elongated marginal cells, largely restricted to the fibrous capsule of the nucleus. The fusiform and marginal neurons were identified by retrograde peroxidase labeling as the olivo-collicular projection cells. Ultrastructural analysis of normal and experimental material revealed the presence of four distinct kinds of axon terminals differing in size, synaptic vesicles type, relation to postsynaptic targets and in origin: (i) large terminals with multiple extended asymmetric synaptic membrane specializations and containing round, clear vesicles arise from the spherical cells of the ipsilateral anteroventral cochlear nucleus, (ii) most of the small axon terminal profiles - engaged in asymmetric synaptic contacts - originated from the trapezoid nucleus, (iii) terminal boutons containing pleomorphic vesicles belong to fibers descending from the ipsilateral multipolar neurons in the central nucleus of the inferior colliculus and from the nuclei of the lateral lemniscus while (iv) boutons containing exclusively ovoid vesicles and remaining intact after complete deafferentation of the nucleus were considered to be of local origin.

Frequency-specific projections of individual neurons in chick brainstem auditory nuclei

Nucleus magnocellularis and nucleus laminaris in the avian brainstem contain second- and third-order auditory neurons thought to be homologous to the mammalian anteroventral cochlear nucleus and medial superior olivary nucleus, respectively. Nucleus laminaris in the chicken is a tonotopically organized sheet of bipolar neurons; each of these neurons receives spatially segregated bilateral innervation from the two magnocellular nuclei. In the present study, this projection was studied at the single cell level by analyzing the pattern of terminal arborizations of individual horseradish peroxidase-filled axons. Reconstruction of the terminal arborizations of nucleus magnocellularis axons revealed that each axon forms an elongated band of endings, the long axis of which is parallel to the physiologically defined isofrequency bands. Within a band, the individual terminal collaterals form distinct patches separated by areas without endings. We suggest that the elongated terminal fields provide the basis of the tonotopic organization observed in nucleus laminaris and that the trajectories of the ipsilateral and contralateral axons may provide differential conduction delays that are important for binaural integration of acoustic information.

Auditory neuronal sizes after a unilateral conductive hearing loss

The left external auditory meatus was removed in 4-day-old CBA J mice; after killing at 45 days, serial sections of the cochleae and brain stem were prepared. From these, the cross-sectional areas of spiral ganglion neurons and of 14 auditory brain stem neuronal types were measured, using a total of 210 neurons of each of the 15 types from both the right and left sides. Nine neuronal types were significantly ( P < 0.01) on the left side: spiral ganglion neurons; globular, small spherical, large spherical, octopus, multipolar, and granule cells of the ventral cochlear nucleus; Purkinje-like cells of the dorsal cochlear nucleus; and spindle cells of the lateral superior olivary nucleus. Two neuronal types were significantly smaller ( P < 0.01) on the right: principal cells of the medial nucleus of the trapezoid body (superior olivary complex), and spindle-shape principal neurons of the central nucleus of the inferior colliculus. The left ventral cochlear nucleus had significantly smaller volume ( P < 0.01) than the right but right and left dorsal cochlear nuclear volumes did not differ significantly ( P > 0.05). Right and left sides were not significantly different ( P > 0.05) for the following neuronal types: fusiform cells and coarse- and fine-Nissl deep cells of the dorsal cochlear nucleus, and rostral bipolar cells of the medial superior olivary nucleus. Neurons affected by unilateral conductive loss were not significantly different ( P > 0.05) from the same cells in mice with bilateral conductive losses; neurons not affected by unilateral conductive loss were not significantly diferent ( P > 0.05) from the same cells in normal mice.

Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: A light and electron microscope study

This report presents the major structural features of neurons and their afferent input in nucleus magnocellularis, the avian homologue of the mammalian anteroventral cochlear nucleus. Results of light-microscope observations, as seen in Golgi, Nissl, and normal fiber preparations, as well as ultrastructural morphology are reported. In addition, cells and axons in nucleus laminaris, the presumed homologue of the mammalian medial superior olivary nucleus, are also described. In Golgi-impregnated material, the mature principal cell in nucleus magnocellularis has an ovoid soma encrusted with somatic spines. A dendrite, when present, emerges from the cell soma, travels for a short distance and breaks into a tuft of stubby terminal branches. Foremost among the afferents to nucleus magnocellularis are auditory nerve axons that terminate in large, axosomatic endings, or endbulbs, covering a large portion of the somatic surface. Other afferents, which also end in relation to the perikaryon, are of undetermined and perhaps multiple origins. The neurons resemble the bushy cells of the mammalian anteroventral cochlear nucleus. Evidence is presented that individual axons from the nucleus magnocellularis bifurcate and send branches to the nucleus laminaris bilaterally, thus placing constraints on the binaural interactions possibly involved in lateralization functions. In electron micrographs, the end-bulbs appear as large, elongate structures which can cover a third of the cell soma. Multiple sites of synaptic specialization occur along these terminals. The synaptic membrane complexes may form directly on the cell body or on the sides or crests of somatic spines. These complexes are characterized by asymmetric membrane densities with a cluster of clear, spherical vesicles on the axonal side. Other small terminal profiles are also present on the somata receiving the end-bulbs. Dendritic profiles are scarce, in agreement with observations in Golgi impregnations. The structural findings indicate that the medial part of the nucleus magnocellularis is homologous to the anterior part of the mammalian anteroventral cochlear nucleus in that the neurons of nucleus magnocellularis are homologous to the bushy cells of the cat. On this basis, the cells in nucleus magnocellularis could faithfully preserve the acoustic response patterns generated in the auditory nerve. This should, in turn, allow a secure relay of bilateral latency differences essential for binaural interactions in the nucleus laminaris.

Correlated studies of the ear and brainstem in the deaf white cat: changes in the spiral ganglion and the medial superior olivary nucleus.

Correlated studies of the ear and brainstem in deaf and hearing white cats have demonstrated early and progressive changes both peripherally and centrally, including organ of Corti degeneration, loss of spiral ganglion cells and auditory nerve fibers and decrease of neuronal size in the medial superior olivary nucleus (MSO). Loss of synaptic appositions on MSO neuronal perikarya is already pronounced in the youngest deaf animal, a time before the spiral ganglion cell population has decreased significantly. Thus, spiral ganglion cell populations alone cannot be used as a reliable indicator of the integrity of the central auditory pathways.

The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum).

The connections of the inferior colliculus, the mammalian mid-brain auditory center, were determined in the greater horseshoe bat (Rhinolophus ferrumequinum), using the horseradish peroxidase method. In order to localize the auditory centers of this bat, brains were investigated with the aid of cell and fiber-stained material. The results show that most auditory centers are highly developed in this echolocating bat. However, the organization of the central auditory system does not generally differ from the mammalian scheme. This holds also for the organization of the superior olivary complex where a well-developed medial superior olivary nucleus was found. In addition to the ventral and dorsal nuclei of the lateral lemniscus a third well-developed nucleus has been defined which projects ipsilaterally to the inferior colliculus and which was called the intermediate nucleus of the lateral leminiscus. All nuclei of the central auditory pathway project ipsi-, contra-, or bilaterally to the central nucleus of the inferior colliculus with the exception of the medial nucleus of the trapezoid body and the medial geniculate body. The tonotopic organization of these projections and their possible functions are discussed in context with neurophysiological investigations.

The origins of the cochlear efferent bundle of Rasmussen in primates

The spatial distribution of neurons emitting fibers of the olivocochlear bundle was determined by injecting horseradish peroxidase into the round window in a series of new and old world monkeys. Animals were perfused 24–28 h later. Sections through the pons and medulla were reacted with tetramethyl benzidine and counterstained with thionin and/or neutral red. Perikarya containing reaction product numbered over 800 in one case. The greatest concentration of labeled cells was located in the dorsal periolivary area intermediate between the dorsal margins of the lateral and medial superior olivary nuclei. Approximately 400 cells were ipsilateral to the injection, opposed to 100 contralaterally. The dorsolateral periolivary area contained over 100 labeled cells ipsilaterally, and only about one-third as many contralaterally. While 95 labeled cells occupied the region of the contralateral medial preolivary nucleus, about two-thirds as many labeled cells were found in the comparable ipsilateral nucleus. Although a few labeled neurons were present bilaterally in the lateral preolive and the lateral superior olivary nucleus, no labeled cells were found in the region of the dorsomedial or ventromedial periolivary nuclei (medial to the medial superior olive). [Work supported by the Deafness Research Foundation.]

Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat

Binaural response properties of single neurons in the medial superior olivary nucleus (MSO) were investigated in the anesthetized rat. Stimulus parameters studied included interaural time difference and interaural intensity difference. In the present study, of the two cell types observed in the rat MSO nucleus, EE and EI, variations in the binaural response properties of the MSO neurons permitted further subclassifications, which may be related to the dendritic dominance of the MSO neurons.

Normal postnatal development of medial superior olivary neurons in the albino rat: a Golgi and Nissl study.

Bipolar neurons in the medial superior olivary (MSO) nucleus of albino rats were studied at various ages (0-75 days) during development in order to elucidate normal neuronal growth patterns. Neurons, visualized in celloidin embedded Golgi/Nissl- and frozen Nissl-stained sections, were analyzed quantitatively for cell size and extent of dendritic arborization. These parameters, from both sets of data, showed a consistent developmental trend with the existence of two major stages in the ontogenetic process: a rapid developmental and a stabilization stage. The first stage, encompassing postnatal days 0 through approximately 14, was characterized by a rapidly increasing cell size, as observed in frozen sections. At the peak of this rapid growth, Golgi-stained neurons possessed thick dendrites with many appendages, growth cones, and filopodia. The peak in neuronal development coincided with the initiation of ear opening. Morphological features attained a more mature form in the second, stabilizing stage of development, which began at approximately postnatal day 14. This phase was distinguished by a decrement in cell size and dendritic branching. Also, dendrites possessed more regularly distributed varicosities and fewer appendages, growth cones, and filopodia in this period. It was observed that dendritic branching trends paralleled those of cell diameter growth.

Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla.

Groups of pregnant rats were injected with two successive daily doses of 3H-thymidine from gestational days 12 and 13 (E12 + 13) until the day before parturition (E21 + 22). In adult progeny of the injected rats the proportion of neurons generated on specific embryonic days was determined quantitatively in the vestibular and auditory nuclei of the upper medulla. In the vestibular nuclei, neurons are generated between days E11 and E15 in an overlapping sequential order, yielding a lateral-to-medial and a rostral-to-caudal internuclear gradient. In the lateral vestibular nucleus peak production time is day E12; in the superior nucleus, E13; in the inferior nucleus, E13 and E14; and in the medial nucleus, E14. The early generation of neurons of the lateral vestibular nucleus may reflect the early differentiation of the circuit from the gravity receptors (utricle) to neurons of the spinal cord controlling postural balance. The later production of neurons of the superior vestibular nucleus may reflect the subsequent differentiation of the circuit from the rotational receptors (semicircular canals) to the neurons of the brain stem controlling eye movements. The generation time of neurons of the nucleus prepositus hypoglossi overlaps with that of the medial vestibular nucleus. The neurons of the anteroventral and posteroventral cochlear nuclei are produced from days E13 to E17, with no temporal differences between the two nuclei. The neurons of the dorsal cochlear nucleus are generated over a very long time span, beginning on day E12 and extending into the postnatal period. There is a sequence in the production of neurons forming the different layers of the dorsal cochlear nucleus in the following order: pyramidal cells, cells of the inner layer, cells of the outer layer and, finally, cells of the granular layer. There is also a sequential production of neurons in four nuclei of the superior olivary complex. In the lateral trapezoid nucleus peak production time is day E12; in the medial superior olivary nucleus, day E13; in the medial trapezoid nucleus, day E15; and in the lateral superior olivary nucleus, day E16. This order yields a medial-to-lateral gradient in the dorsal aspect of the superior olivary complex, and a lateral-to-medial gradient ventrally. These mirror-image gradients were also seen intranuclearly in the lateral superior olivary nucleus and the medial trapezoid nucleus. The cytogenetic gradients could not be related to tonotopic representation; however, they could be related to the lateral location of ipsilateral cochlear nucleus input to the lateral superior olivary nucleus and the medial location of the contralateral cochlear nucleus input to the medial trapezoid nucleus.

The differential distribution of synaptic terminal on marginal and central cells in the cat medial superior olivary nucleus.

Electron microscopic analysis of the perikaryal surfaces of central and marginal cells in the cat medial superior olivary nucleus has revealed three differences in their relationships with synaptic terminals. Marginal cells have a smaller percentage of their surface covered by synaptic terminals; synaptic endings on marginal cells tend to be smaller in size; and a higher proportion of synaptic terminals on marginal cells contain small vesicles. These differences suggest that central and marginal cells differ in the information which they receive, as well as in the cells to which they pass their information.

Effects of monaural and binaural occlusion on the morphology of neurons in the medial superior olivary nucleus of the rat

Effects of monaural and binaural occlusion on the morphology of neurons in the medial superior olivary nucleus of the rat

Transport of radioactivity from primary auditory neurons beyond the cochlear nuclei

Transneuronal degeneration in secondary brainstem auditory nuclei has been described following cochlear lesions, and Marchi studies have revealed degeneration in the trapezoid body after such lesions. These findings support the view of some early neuroanatomists that primary auditory afferents project beyond the cochlear nuclei. Silver impregnation studies of degenerating cochlear afferents have failed to support this claim, leaving the question unresolved. Using [3H] amino acids auditory projections in the monkey were traced autoradiographically from labeled ganglion cells: (1) in all portions of the spiral ganglion, (2) in apical and middle turns of the cochlea and (3) primarily in the basal turn of the cochlea. Labeling of the entire spiral ganglion resulted in profuse transport of isotope to parts of all cochlear nuclei [anteroventral (AVCN), posteroventral (PVCN), and dorsal (DCN) cochlear nuclei]. Labeled axons entering the trapezoid body (TB) projected ipsilaterally to: (1) the lateral trapezoid nuclei (LTN), (2) the lateral superior olivary nucleus (LSO), (3) the dorsal dendritic zone of the medial superior olivary nucleus (MSO), and (4) the pericollicular or cortical nucleus of the inferior colliculus (IC). Auditory fibers crossing the midline in the TB projected contralaterally to: (1) the medial trapezoid nucleus (MTN), (2) the ventral dendritic zone of the MSO, (3) the ventral nucleus of the lateral lemniscus (VNLL), and (4) the central nucleus of the inferior colliculus (CNIC). Selective labeling of cells in the apical and middle ganglionic turns ofthe cochlea resulted in a similar pattern of centripetal transport. Selective [3H] uptake primarily by ganglion cells in the basal turn of the cochlea resulted in: (1) labeling of restricted parts of all cochlear nuclei, and (2) a considerable reduction of isotope transported beyond the cochlear nuclei. Labeled fibers in the TB were distributed sparsely in the ipsilateral LTN, LSO and dorsal dendritic zone of the MSO. Fibers in the TB were not labeled contralaterally in these animals. Interpretation of these data considers the possibility of transneuronal isotope transport. The pattern of isotope transported beyond the cochlear nuclei does not correspond to the secondary projections of any individual cochlear nucleus, although it bears some resemblance to that of the AVCN. The current study suggests that some primary auditory afferents project beyond the cochlear nuclei.

Ascending and intrinsic projections of the superior olivary complex in the cat.

The ascending and intrinsic projections of the superior olivary complex (SO) in the cat were investigated by injection of 3H-leucine and horseradish peroxidase (HRP) in SO and the inferior colliculus (IC), respectively. A topically arranged projection was demonstrated from the nucleus of the trapezoid body (NTB) to the ipsilateral lateral superior olivary nucleus (LSO) wiht a lesser connection in the opposite direction. The medial superior olivary nucleus (MSO) has a strictly ipsilateral projection, whilst LSO projects symmetrically through the lateral lemniscus (LL) of both sides, to end with topically arranged terminals in the ventrolateral part of the central nucleus of the inferior colliculus (CNIC). Terminal labelling found in the ventral and dorsal nuclei of LL (VNLL and DNLL) probably represents collaterals from bypassing fibres originating in MSO and LSO, respectively. These results were demonstrated by both techniques, whilst in addition the HRP method revealed an ipsilateral and contralateral projection to IC from VNLL and DNLL, respectively.

Afferent projections to the central nucleus of the inferior colliculus in the rat

The afferent projections to the inferior colliculus of the rat were studied using the method of retrograde transport of horseradish peroxidase (HRP). Following large injections of HRP into the central nucleus, cells within the cochlear nuclei, superior olivary complex and auditory cortex were stained. Within the contralateral dorsal cochlear nucleus, fusiform cells were heavily labeled. Giant cells were also labeled in deeper layers. In the contralateral ventral cochlear nucleus, virtually all major cell types were labeled, with some types being labeled in greater numbers than others. Octopus cells of posteroventral division of ventral cochlear nucleus (PVCN) were never labeled. HRP-positive cells were found in ipsilateral and contralateral lateral superior olivary nucleus (LSO), ipsilateral medial superior olivary nucleus (MSO), ipsilateral and contralateral lateral nucleus of the trapezoid body (LTB), ipsilateral ventral nucleus of the trapezoid body (VTB), and ipsilateral superior paraolivary nucleus (SPN). Pyramidal cells of layer V of auditory cortex were heavily labeled. Small injections of HRP into the central nucleus resulted in labeled cells within restricted regions of the cochlear nuclei, superior olivary complex and auditory cortex. Injections into dorsal regions of the central nucleus resulted in cells labeled in ventral regions of the dorsal and ventral cochlear nuclei, and in lateral regions of LSO. These regions contain neurons which are considered to have low best frequencies. Injections placed in more ventral regions of the central nucleus led to labeling of cells in more dorsal regions of the cochlear nuclei and more medial regions of LSO in agreement with the tonotopical progressions within these structures.

Plasticity of binaural interaction. I. Effect of early auditory deprivation

Plasticity of binaural interaction. I. Effect of early auditory deprivation