Parallel auditory pathways: projection patterns of the different neuronal populations in the dorsal and ventral cochlear nuclei

The cochlear nuclear complex gives rise to widespread projections to nuclei throughout the brainstem. The projections arise from separate, well-defined populations of cells. None of the cell populations in the cochlear nucleus projects to all brainstem targets, and none of the targets receives inputs from all cell types. The projections of nine distinguishable cell types in the cochlear nucleus—seven in the ventral cochlear nucleus and two in the dorsal cochlear nucleus—are described in this review. Globular bushy cells and two types of spherical bushy cells project to nuclei in the superior olivary complex that play roles in sound localization based on binaural cues. Octopus cells convey precisely timed information to nuclei in the superior olivary complex and lateral lemniscus that, in turn, send inhibitory input to the inferior colliculus. Cochlear root neurons send widespread projections to areas of the reticular formation involved in startle reflexes and autonomic functions. Type I multipolar cells may encode complex features of natural stimuli and send excitatory projections directly to the inferior colliculus. Type II multipolar cells send inhibitory projections to the contralateral cochlear nuclei. Fusiform cells in the dorsal cochlear nucleus appear to be important for the localization of sounds based on spectral cues and send direct excitatory projections to the inferior colliculus. Giant cells in the dorsal cochlear nucleus also project directly to the inferior colliculus; some of them may convey inhibitory inputs to the contralateral cochlear nucleus as well.     

Ventral nucleus of the lateral lemniscus in guinea pigs: Cytoarchitecture and inputs from the cochlear nucleus

Cytoarchitectonic criteria were used to distinguish three subdivisions of the ventral nucleus of the lateral lemniscus in guinea pigs. Axonal tracing techniques were used to examine the projections from the cochlear nucleus to each subdivision. Based on the cell types they contain and their patterns of input, we distinguished ventral, dorsal, and anterior subdivisions of the ventral nucleus of the lateral lemniscus. All three subdivisions receive bilateral inputs from the cochlear nucleus, with contralateral inputs greatly outnumbering ipsilateral inputs. However, the relative density of the inputs varies: the ventral subdivision receives the densest projection, whereas the anterior subdivision receives the sparsest projection. Further differences are apparent in the morphology of the afferent axons. Following an injection of Phaseolus vulgaris-leucoagglutinin into the ventral cochlear nucleus, most of the axons on the contralateral side and all of the axons on the ipsilateral side are thin. Thick axons are present only in the ventral subdivision contralateral to the injection site. The evidence from both anterograde and retrograde tracing studies suggests that the thick axons originate from octopus cells, whereas the thin axons arise from multipolar cells and spherical bushy cells. The differences in constituent cell types and in patterns of inputs suggest that each of the three subdivisions of the ventral nucleus of the lateral lemniscus makes a distinct contribution to the analysis of acoustic signals. J. Comp. Neurol. 379:363–385, 1997. © 1997 Wiley-Liss, Inc.     

Multiple topographically organized projections connect the central nucleus of the inferior colliculus to the ventral division of the medial geniculate nucleus in the gerbil, Meriones unguiculatus

The ventral division of the medial geniculate nucleus (MGv) receives almost all of its ascending input from the ipsilateral central nucleus of the inferior colliculus (CNIC). In a previous study (Cant and Benson [2006] J. Comp. Neurol. 495:511-528), we made injections of biotinylated dextran amine into the CNIC of the gerbil and demonstrated that it can be divided into two parts. One part (zone 1) receives almost all of its ascending input from the cochlear nuclei, the nuclei of the lateral lemniscus, and the main nuclei of the superior olivary complex; the other part (zone 2) receives inputs from the cochlear nuclei and nuclei of the lateral lemniscus but few or no inputs from the main olivary nuclei. Here we show that these two parts of the CNIC project differentially to the MGv. Axons labeled anterogradely by injections in zone 1 project throughout the rostral two-thirds of the MGv, whereas axons from zone 2 project to the caudal third of the MGv. Throughout much of their extent, the terminal fields do not appear to overlap, although both parts of the CNIC project to medial and dorsal parts of the MGv, and there may be overlap in the most ventral part as well. The results indicate that two parallel pathways arising in the CNIC remain largely separate in the medial geniculate nucleus of the gerbil. It seems most likely that the neurons in the two terminal zones in the MGv perform different functions in audition.     

GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pig

Retrograde transport of horseradish peroxidase was combined with immunocytochemistry to identify the origins of potential γ-aminobutyric acid (GABA) -ergic and glycinergic inputs to different subdivisions of the cochlear nucleus. Projection neurons in the inferior colliculus, superior olivary complex, and contralateral cochlear nucleus were examined, but only those from the superior olivary complex contained significant numbers of GABA- or glycine-immunoreactive neurons. The majority of these were in periolivary nuclei ipsilaterally, with a sizeable contribution from the contralateral ventral nucleus of the trapezoid body. Overall, 80% of olivary neurons projecting to the cochlear nucleus were immunoreactive for GABA, glycine, or both. Most glycine-immunoreactive projection neurons were located ipsilaterally, in the lateral and ventral nuclei of the trapezoid body and the dorsal periolivary nucleus. This suggests that glycine is the predominant neurotransmitter used by ipsilateral olivary projections. Most GABA-immunoreactive cells were located bilaterally in the ventral nuclei of the trapezoid body. The contralateral olivary projection was primarily GABA-immunoreactive and provided almost half the GABA-immunoreactive projections to the cochlear nucleus. This suggests that GABA is the predominant neurotransmitter used by contralateral olivary projections. The present results suggest that the superior olivary complex is the most important extrinsic source of inhibitory inputs to the cochlear nucleus. Individual periolivary nuclei differ in the strength and the transmitter content of their projections to the cochlear nucleus and may perform different roles in acoustic processing in the cochlear nucleus. J. Comp. Neurol. 381:500-512, 1997. © 1997 Wiley-Liss, Inc.     

Projections to the inferior colliculus from the anteroventral cochlear nucleus in the cat: possible substrates for binaural interaction

The projections to the inferior colliculus of the cat are shown in autoradiographs after injections of 3H-amino acids into the anteroventral cochlear nucleus and anterograde axonal transport. Labeled bands of axons are seen in the central nucleus of the inferior colliculus, parallel to the fibrodendritic laminae, and in layers 3 and 4 of the dorsal cortex. A bilateral projection to the lateral, low-frequency part of the inferior colliculus is observed. In contrast, the more ventromedial, mid- and high-frequency parts receive only a contralateral input. The projections from the cochlear nucleus to both the contralateral midbrain and bilaterally to the superior olivary complex appear to be tonotopically organized. After HRP injections in the inferior colliculus, small numbers of stellate neurons are labeled in the lateral and ventral low-frequency parts of the anteroventral cochlear nucleus on the ipsilateral side. EM autoradiographs show labeled axonal endings from both sides of the anteroventral cochlear nuclei are present in the same proportion in pars lateralis. Axonal endings from either cochlear nucleus have small, round synaptic vesicles and make asymmetric synaptic contacts on dendrites. Axons from the contralateral side also make axosomatic contacts on large disc-shaped or stellate cells. Neurons from the ipsilateral anteroventral cochlear nucleus apparently make more synaptic endings per cell as compared to neurons from the contralateral side. Together, bilateral inputs from the anteroventral cochlear nucleus can account for a third of the endings with round synaptic vesicles in pars lateralis of the central nucleus. Morphological similarities among the ascending inputs to the inferior colliculus are discussed. Both direct circuits from the cochlear nucleus to the inferior colliculus and indirect circuits via the superior olivary complex or lateral lemniscus may display banding patterns, nucleotopic organization, or differential synaptic organization. The direct inputs from the anteroventral cochlear nucleus to the colliculus may influence binaural interactions which occur in the superior olivary complex. In addition, direct inputs may create new binaural responses in the inferior colliculus that are independent of lower centers.     

Descending projections from the superior olivary complex to the cochlear nucleus of the cat

Subdivisions of the cochlear nuclear complex give rise to a number of discrete projections to certain cell groups of the superior olivary complex and also received substantial descending projections from the periolivary nuclei. In the present study, we sought to determine by means of retrograde transport of horseradish peroxidase (HRP), and anterograde transport of radiolabeled protein, if the periolivary nuclei give rise to discrete projections to the various subdivisions of the cochlear nuclear complex. Following medium to large injections of HRP into the cochlear nucleus, irrespective of location, labeled cells were found in all periolivary nuclei bilaterally. In every case more than 40% of the labeled cells were found in the lateral nucleus of the trapezoid body on the same side and the ventral nucleus of the trapezoid body of both sides. Other periolivary nuclei contributing more than 5% of the total number of cells in individual cases were the contralateral lateral nucleus of the trapezoid body and the ipsilateral anterolateral and dorsal periolivary nuclei. Injections of tritiated leucine into periolivary nuclei gave rise to axonal labeling to the trapezoid body and the dorsal acoustic stria, usually bilaterally, and to terminal labeling that was widely distributed within the cochlear nuclear complex. In several cases with small injections, particularly in the lateral nucleus of the trapezoid body, the projections from the periolivary nuclei to the anteroventral and dorsal cochlear nuclei connected areas described as having similar best-frequency representation. The autoradiographic data corroborated the main results from the HRP experiments and provided additional information permitting these conclusions: the projections from the periolivary nuclei to the cochlear nuclear complex are organized tonotopically, at least in part; each periolivary nucleus (and perhaps individual cells), projects widely throughout the cochlear nuclear complex; the pattern of termination of projections from different periolivary nuclei to a given region of the cochlear nuclear complex are similar, as seen in autoradiograms, and the lateral and dorsal periolivary nuclei project mainly ipsilaterally, while the medial periolivary nuclei project bilaterally with a contralateral bias. The magnitude of these projections and their widespread distribution within the cochlear nuclear complex would suggest an important role for the descending projections in the normal functioning of the cochlear nucleus.     

Connections of the superior olivary complex in the rufous horseshoe bat Rhinolophus rouxi

In the rufous horseshoe bat (Rhinolophus rouxi), the superior olivary complex contains four main divisions. In comparison with other species, the most lateral division is clearly homologous to the lateral superior olive (LSO); the most medial division is homologous to the medial nucleus of the trapezoid body (MNTB). Lying between these landmarks, in approximately the position of the medial superior olive (MSO) of other mammals, are two additional divisions that are cytoarchitecturally distinct from one another yet do not greatly resemble the MSO of nonecholocating mammals such as the cat. We refer to these nuclei as the dorsal medial superior olive (DMSO) and the ventral medial superior olive (VMSO). We examined the afferent and efferent connections of all of these cell groups with retrograde and anterograde transport of WGA-HRP from the superior olivary complex. In the same animals we recorded the binaural response properties of single units in the superior olivary complex. Virtually all units recorded in LSO were excitatory to the ipsilateral ear and inhibitory to the contralateral ear (EI); all of the units sampled in the MNTB and most of those sampled in the VMSO responded only to the contralateral ear (OE). In DMSO the binaural properties of units were varied: the number of units that were inhibitory to the ipsilateral ear and excitatory to the contralateral ear (IE) was about equal to the number of units excitatory to both ears (EE); a few units had OE responses; no units had EI responses. Connectional correlates for these binaural response properties are seen in the patterns of retrograde transport from WGA-HRP injections in the divisions of the superior olive. The LSO receives projections from the ipsilateral cochlear nucleus and MNTB; MNTB receives projections from the contralateral cochlear nucleus. The DMSO and VMSO both receive bilateral projections from the cochlear nuclei. The results of retrograde and anterograde transport suggest that VMSO, in addition, receives projections from the ipsilateral MNTB. The LSO, DMSO, and VMSO all project to the ventral two-thirds of the central nucleus of the inferior colliculus, and their targets are approximately coextensive. However, the LSO projects bilaterally to the inferior colliculus, whereas the medial cell groups project mainly ipsilaterally.     

Functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats.

The ascending projections of the cochlear nucleus (CN) and the sources of descending inputs to the CN were investigated in horseshoe bats (Rhinolophus rouxi) by tracing the anterograde and retrograde transport of horseradish peroxidase (HRP or WGA-HRP) injected into the CN. The tracer was iontophoretically deposited into physiologically characterized regions of the cochlear nucleus (Feng and Vater, '85). We report the course and termination of pathways arising from the anteroventral (AVCN), posteroventral (PVCN), and dorsal (DCN) cochlear nucleus. The projection fields within the auditory brainstem centers (superior olivary complex [SOC]; lateral lemniscus complex [LLC]; and inferior colliculus [IC]) and their tonotopic organization according to the frequency representations at the injection sites are described. While the projection pattern is generally in accordance with other mammals, several species-characteristic features are noted: i) the lateral superior olive (LSO) receives tonotopically organized input from both the AVCN and PVCN; ii) the CN-projections to medial nuclear groups of the SOC located between the LSO and the medial nucleus of the trapezoid body do not support previously suggested homologies; iii) the ventral nucleus of the LLC can be subdivided into two divisions with distinct input patterns from the AVCN and PVCN, respectively.     

Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii

Ascending projections of the cochlear nuclei in the mustache bat were analyzed by anterograde transport of [3H]-leucine and by retrograde transport of HRP. We were particularly interested in pathways to two parts of the system: (1) to the medial superior olive, because this nucleus is missing in most echolocating bats, but appears to be present in the mustache bat, and (2) to the intermediate and ventral nuclei of the lateral lemniscus, because these nuclei are hypertrophied and highly differentiated in all echolocating bats that we have examined. The results show a highly systematic projection from the anteroventral cochlear nucleus to all of the auditory nuclei in the brain stem. After an injection of [3H]-leucine in the anterior and dorsal part of the anteroventral cochlear nucleus, presumably in a region sensitive to low frequencies, label is seen in the following locations: ipsilateral to the injection in the lateral part of the lateral superior olive; bilaterally in the dorsal part of the medial superior olive; contralateral to the injection in the dorsal parts of the intermediate and ventral nuclei of the lateral lemniscus; and in the anterolateral part of the central nucleus of the inferior colliculus. After an injection of [3H]-leucine in a posterior part of the anteroventral cochlear nucleus, presumably in a region sensitive to high frequencies, labeling is in the same set of nuclei, but within each nucleus the label is now in a different location: medially in the lateral superior olive, ventrally in the medial superior olive, ventrally in each division of the ventral and intermediate nuclei of the lateral lemniscus, and medially in the central nucleus of the inferior colliculus. Projections from the entire anteroventral cochlear nucleus to the inferior colliculus are confined to the ventral two-thirds of the central nucleus. The dorsal one-third of the central nucleus of the inferior colliculus is the principal target of the dorsal cochlear nucleus and may be a target of the posteroventral cochlear nucleus. Both of these nuclei appear to project sparsely to the ventral parts of the inferior colliculus. We conclude first that the bilateral input to the medial superior olive in the mustache bat is similar to the input seen in other mammals. Thus this bat has a neural structure which is associated with the analysis of binaural time differences and which usually is seen only in animals with heads large enough to create interaural time differences greater than those available to Pteronotus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Anatomical projections of the nuclei of the lateral lemniscus in the albino rat (rattus norvegicus)

The ascending projections to the lateral lemniscal nuclei and the inferior colliculus were investigated in the albino rat by using Fluoro‐Gold, either alone or in combination with other retrograde tract tracers. Injections were made into the central nucleus of the inferior colliculus (ICC), the dorsal nucleus of the lateral lemniscus (DNLL), the intermediate nucleus of the lateral lemniscus (INLL), or the ventral nucleus of the lateral lemniscus (VNLL). The ICC receives both ipsilateral and contralateral projections from the DNLL and the lateral superior olive, major ipsilateral projections from the INLL, VNLL, medial superior olive, and superior paraolivary nucleus, and major contralateral projections from both dorsal and ventral cochlear nucleus. The DNLL receives a similar pattern of projections from the auditory lower brainstem nuclei. The INLL, in contrast, receives its major projections from the ipsilateral VNLL, lateral superior olive, medial superior olive, superior paraolivary nucleus, and medial nucleus of the trapezoid body, but does not receive a heavy projection from the contralateral lateral superior olive. It receives a major contralateral projection from the ventral cochlear nucleus, but a much lighter projection from the contralateral dorsal cochlear nucleus. The VNLL receives projections from the ipsilateral medial nucleus of the trapezoid body and the contralateral ventral cochlear nucleus, but does not receive projections from the medial or lateral superior olives, the superior paraolivary nucleus, or the dorsal cochlear nucleus. Thus, the three primary subdivisions of the rat's lateral lemniscus can be distinguished from each other on the basis of their distinctive projection patterns. J. Comp. Neurol. 512:573–593, 2009. © 2008 Wiley‐Liss, Inc.     

Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats.

In this study we present direct evidence of axonal projections from both the medial and lateral nuclei of the trapezoid body to the medial superior olive. Projections were traced by intracellularly labeling cells and axons in a tissue slice preparation of two rodent species, Mus musculus and Meriones unguiculatus and two bat species, Eptesicus fuscus and Pteronotus parnellii. The main axon of most principal cells in the medial nucleus of the trapezoid body gives off one or more collateral branches which arborize within the medial superior olive. These collateral axons form small bouton-like swellings which primarily contact somata within the central cell column in the medial superior olive. Likewise, labeled elongate and multipolar cells of the lateral nucleus of the trapezoid body send axons to both the medial and lateral superior olives. These axons also form perisomatic contacts in both target nuclei. These two sets of projections may relay ascending input to the medial superior olive and the lateral superior olive; the medial nucleus of the trapezoid body is known to relay input from the contralateral ventral cochlear nucleus, and the lateral nucleus of the trapezoid body may relay input from the ipsilateral ventral cochlear nucleus. These projections offer two routes for indirect, possibly inhibitory input to reach the medial superior olive from both cochlear nuclei. These indirect, inhibitory pathways may parallel the direct excitatory projections the medial superior olive receives from each cochlear nucleus.     

Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat,Eptesicus fuscus

The nuclei of the lateral lemniscus in the echolocating bat, Eptesicus fuscus, are large and highly differentiated. In each nucleus, different characteristic response properties predominate. To determine whether the dissimilar response properties are due in part to dfferential ascending input, we examined the retrograde transport from small deposits of horseradish peroxidase (HRP) or HRP conjugated with wheat germ agglutinin (WGA-HRP) in the nuclei of the lateral lemniscus. The intermediate nucleus (INLL) and the two divisions of the ventral nucleus (VNLL) receive almost exclusively monaural input from the anteroventral and posteroventral cochlear nuclei and from the medial nucleus of the trapezoid body. Lesser inputs originate in the lateral nucleus of the trapezoid body and the ventral periolivary area. Although the three monaural nuclei of the lateral lemniscus all receive input from the same set of nuclei, and from the same identified cell types in the cochlear nucleus, there is a difference in the relative proportions of input from these sources. The dorsal nucleus (DNLL) receives input mostly from binaural structures, the lateral and medial superior olives and the contralateral DNLL, with only a minor projection from the coc hlear nucleus. The lateral and medial superior olives project bilaterally; the bilateral projection from the medial superior olive is unusual in that it is found in only a few mammalian species. The results show a segregated pattern of binaural projections to DNLL and monaural projections to INLL and VNLL that is consistent with the binaural response properties found in DNLL and the exclusively monaural response properties found in INLL and VNLL. The differences in response properties between monaural nuclei, however, are not due to input from different nuclei or cell types but may be influenced by differing magnitudes of the constituent ascending projections. © 1995 Wiley-Liss, Inc.     

Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat

Anterior thalamic afferents from the mamillary body and the limbic cortex were studied by using single and double retrograde transport methods in the rat. The medial mamillary nucleus was divided on the basis of the cytoarchitecture into four subnuclei: the pars medialis centralis, pars medialis dorsalis, pars lateralis, and pars basalis. Extensive connections were seen between each of these subdivisions of the mamillary body and the anterior thalamic nuclei, topographically organized so that the anteromedial thalamic nucleus receives projections exclusively from the pars medialis centralis, while the anteroventral thalamic nucleus receives projections from the pars medialis dorsalis and pars lateralis. Nuclei in the dorsal half of these two mamillary subdivisions project predominantly to the medial half of the anteroventral thalamic nucleus, and those in the ventral half to the lateral half of the nucleus. The pars basalis was found to have numerous projections to the magnocellular part of the anteroventral nucleus. All limbic cortical areas send projections bilaterally to all regions of the anteromedial nucleus as well as to the parvicellular parts of the anteroventral thalamic nucleus, while the anterodorsal nucleus receives ipsilateral projections originating exclusively from the preagranular, anterior limbic, and cingular regions. The magnocellular part of the anteroventral nucleus, however, receives only ipsilateral projections from all of the limbic cortex. Some neurons in the infralimbic region also project bilaterally to all of the anterior thalamic nuclei except the anterodorsal nucleus. All of these cortical projections to the anterior thalamus originate in layers V and VI of the limbic cortex.     

Organization of the inferior colliculus of the gerbil (Meriones unguiculatus): differences in distribution of projections from the cochlear nuclei and the superior olivary complex

The inferior colliculus (IC) receives its major ascending input from the cochlear nuclei, the superior olivary complex, and the nuclei of the lateral lemniscus. To understand better the terminal distribution of the inputs from these sources relative to one another, we made focal injections of a retrograde tracer, biotinylated dextran amine, in different parts of the IC in 74 gerbils (Meriones unguiculatus). The cases could be divided into three groups based on counts of labeled cells in brainstem auditory nuclei. Group 1 cases had labeled cells in both the cochlear nuclei and the lateral and medial superior olivary nuclei. Group 2 cases had labeled cells in the cochlear nuclei but few or none in the lateral and medial superior olivary nuclei. Both groups had labeled cells in the nuclei of the lateral lemniscus and the superior paraolivary nucleus. Group 3 cases had few labeled cells in any of the ascending auditory pathways. The group to which a case belonged was strongly related to the location of the injection site in the IC. The injection sites for both group 1 and group 2 were located in the central nucleus, but those for group 1 tended to be located laterally relative to those for group 2, which were located more medially and caudally. The injection sites for group 3 cases lay outside the central nucleus of the IC. The two regions of the central nucleus of the IC, distinguished on the basis of connectivity, are likely to subserve different functions.     

Ascending auditory afferents to the nuclei of the lateral leminscus

Afferents from the hindbrain auditory system to the nuclei of the lateral lemniscus were analyzed by the use of orthograde and retrograde axontracing techniques. Three divisions of the nuclei of the lateral lemniscus, a dorsal, an intermediate, and a ventral division are discussed. The dorsal nucleus of the lateral lemniscus is a recipient of afferents from cells located mainly in the superior olivary complex and the contralateral dorsal nucleus of the lateral lemniscus. It receives direct afferents from only a few cells in the cochlear nuclei. In sharp contrast, the ventral nucleus of the lateral lemniscus is the recipient of afferents from many cells in the contralateral ventral cochlear nucleus and from only a few cells in the superior olivary complex. Further, it receives no afferents from cells in the contralateral nuclei of the lateral lemniscus. The intermediate nucleus of the lateral lemniscus receives afferents from some cells in the cochlear nucleus and the superior olivary complex. It is unique among the three nuclei of the lateral lemniscus in that it receives a substantial projection from the medial nucleus of the trapezoid body.     

Axonal projections from the lateral and medial superior olive to the inferior colliculus of the cat: A study using electron microscopic autoradiography

The superior olivary complex is the first site in the central auditory system where binaural interactions occur. The output of these nuclei is direct to the central nucleus of the inferior colliculus, where binaural inputs synapse with monaural afferents such as those from the cochlear nuclei. Despite the importance of the olivary pathways for binaural information processing, little is known about their synaptic organization ir the colliculus. The present study investigates the structure of the projections from the lateral and medial superior olivary nuclei to the inferior colliculus at the electron microscopic level. Stereotaxic placement and electrophysi ological responses to binaural sounds were used to locate the superior olive. Anterograde axonal transport of 3H-leucine was combined with light and electron microscopic autoradiography to reveal the location and morphology of the olivary axonal endings. The results show that the superior olivary complex contributes different patterns of synaptic input to the central nucleus of the inferior colliculus. Each projection from the superior olivary complex to the colliculus differs in the number and combinations of endings. Axonal endings from the ipsilateral medial superior olive were exclusively the round (R) type that contain round synaptic vesicles and make asymmetrical synaptic junctions. This morpholo is usually associated with excitatory synapses and neurotransmitters such as glutamate. Endings from medial superior olive terminate densely in the central nucleus. The projection from the contralateral lateral superior olive also terminates primarily as R endings. This projection also includes small numbers of pleomorphic (PL) endings that contain pleomorphic synaptic vesicles and usually make symmetrical synaptic junctions. The PL morpholo is associated with inhibitory synapses and transmitters such as gamma-aminobutyric acid and glycine. All endings from the contralateral lateral superior olive terminate much less densely than endings from the medial olive. In contrast, the projection from the ipsilateral lateral superior olive contributes both R and PL endings in roughly equal proportions. These ipsilateral afferents are heterogeneous in density and can terminate in lower or higher concentrations than endings from the contralateral side. These data show that the superior olive is a major contributor to the synaptic organization of the centr nucleus of the inferior colliculus. The ipsilateral projections of the medial and lateral superior olive may produce higher concentrations of R endings than other inputs to the central nucleus. Such endings may participate in excitatory synapses. The highest concentra tions of PL endings come from the ipsilateral lateral superior olive. In combination with inputs from the contralateral dorsal nucleus of the lateral lemniscus, PL endings from the superior olive may participate in many inhibitory synapses found in the central nucleus. These different patterns of synaptic input from the superior olivary complex will influence how binaural information is transmitted to the inferior colliculus. © 1995 Wiley-Liss, Inc.     

Auditory projections from the cochlear nucleus to pontine and mesencephalic reticular nuclei in the rat.

We investigated projections from the cochlear nucleus in the rat using the anterograde tracer Phaseolus vulgaris-leucoagglutinin. We focused on nuclei in the brainstem which are not considered to be part of the classical auditory pathway. In addition to labeling in auditory nuclei, we found presumed terminal fibers in 4 pontine and mesencephalic areas: (1) the pontine nucleus (PN), which receives bilateral projections from the antero- and posteroventral cochlear nuclei; (2) the ventrolateral tegmental nucleus (VLTg), which receives a contralateral projection from the rostral portion of the anteroventral cochlear nucleus; (3) the caudal pontine reticular nucleus (PnC), which receives bilateral input originating predominantly in the dorsal cochlear nucleus; and (4) the lateral paragigantocellular nucleus (LPGi), which receives projections from all subdivisions of the cochlear nuclei. In the VLTg and PnC, anterogradely labeled varicose axons were often found in close apposition to the primary dendrites and somata of large reticular neurons. Injections of the retrograde fluorescent tracer Fluoro-Gold into the VLTg demonstrated that the neurons of origin are mainly located contralaterally in the rostral anteroventral cochlear nucleus and in the cochlear root nucleus. The relevance of these auditory projections for short-latency audio-motor behaviors and acoustically elicited autonomic responses is discussed.     

Projections from the superior olivary complex to the cochlear nucleus in the tree shrew

The origins and targets of projections from the superior olivary complex to the cochlear nuclei were studied in the tree shrew by placing small injections of horseradish peroxidase (HRP) in the cochlear nucleus and small injections of ³H-leucine in the superior olivary complex. The results show that the descending pathways originate in periolivary cell groups surrounding the medial and lateral superior olives and that the periolivary nuclei differ from one another in their patterns of projections to the cochlear nucleus. For example, cell groups may project either ipsilaterally or bilaterally. Cells in the lateral nucleus of the trapezoid body project only to the ipsilateral cochlear nucleus. Other periolivary cell groups project bilaterally, although some of these may project more heavily to one side than the other. Some pathways have widespread targets in the cochlear nucleus whereas others have relatively specific targets. Diffuse projections to all divisions of the cochlear nucleus arise from the lateral nucleus of the trapezoid body ipsilaterally and from the medial perioliviary nucleus bilaterally. The targets of other descending pathways are more restricted. The anterolateral, dorsal, and dorsolateral periolivary nuclei project mainly to the anteroventral cochlear nucleus; the ventral nucleus of the trapezoid body and the posterior periolivary nucleus project mainly to the dorsal and posteroventral cochlear nuclei. All of these specific projections are bilateral. These results suggest that projections from the periolivary cell groups to the cochlear nucleus consist of multiple components with different degrees of specificity.     

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 form 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 form 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.     

Thalamic afferents to the limbic cortex in the cat studied with the method of retrograde axonal transport of horseradish peroxidase

Thalamic afferents to the limbic cortex in the cat were studied with the method of retrograde axonal transport of horseradish peroxidase. The anterior limbic region receives fibers largely from the anteromedial nucleus and partly from the anterodorsal and anteroventral nuclei. There appears to be a dorsoventral organization of cortical projections of the anteromedial nucleus to the anterior limbic region. The cingular area has its main input from the anteroventral and anteromedial nuclei. The lower bank and fundus of the splenial sulcus receive fibers from the anteroventral nucleus, particularly its parvocellular part. The retrosplenial area receives projections from the naterodorsal, anteroventral and anteromedial nuclei. The agranular retrosplenial area (area 30) recieves hardly any fibers from the anterior thalamic nuclei. The postsubicular and presubicular areas receive cortical afferents from the anterodorsal, anteroventral (both magnocellular and parvocellular parts) and anteromedial nuclei. In addition, the limbic cortex receives many fibers from the dorsal lateral, medial pulvinar and lateral pulvinar nuclei, and few fibers from the intralaminar and midline nuclei.