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.     

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.     

Convergence of ascending pathways at the inferior colliculus of the mustache bat, Pteronotus parnellii

To compare patterns of projections to the inferior colliculus from different sources, injections of [3H]-leucine were placed in the cochlear nuclei, superior olivary complex, and nuclei of the lateral lemniscus of Pteronotus parnellii. The results show that the target of the anteroventral cochlear nucleus (AVCN) is the ventral and lateral two thirds of the central nucleus of the inferior colliculus. The binaural pathways from the medial and lateral superior olives (MSO and LSO) project to the same target. The dorsal cochlear nucleus (DCN) projects to the entire central nucleus of the inferior colliculus and does so in a more diffuse manner than does the AVCN. The DCN also sends sparse projections beyond the central nucleus into dorsal parts of the pericentral area. The intermediate (INLL) and ventral (VNLL) nuclei of the lateral lemniscus are relays in pathways that originate in the cochlear nucleus and terminate in the contralateral inferior colliculus. These nuclei also receive indirect input from the contralateral AVCN via the medial nucleus of the trapezoid body. Although nuclei of the lateral lemniscus project most densely to those areas of the inferior colliculus that are also the targets of the AVCN, MSO, and LSO, the nuclei of the lateral lemniscus also send spare projections outside these areas. Many of the pathways just described project in bands, a finding that raises the possibility that the projections parallel the orientation of disk-shaped cells in the inferior colliculus and raises the question of whether the bands from one source overlap or interdigitate with the bands from another source.     

Auditory brainstem of the ferret: sources of projections to the inferior colliculus

The organization of the auditory brainstem in adult, darkly pigmented ferrets was studied by using the retrograde transport of the lectin wheat germ agglutinin-horseradish peroxidase injected into one inferior colliculus. Retrogradely labelled neurons were found bilaterally in every nucleus of the auditory brainstem. The greatest number of labelled neurons was found in the cochlear nuclei contralateral to the injection site, the ipsilateral medial superior olivary nucleus, both lateral superior olivary nuclei, the ipsilateral ventral nucleus of the lateral lemniscus, both dorsal nuclei of the lateral lemniscus, and the contralateral inferior colliculus. Quantitative assessment of the projections from the cochlear nuclei showed that the number of contralaterally projecting neurons exceeded the number of ipsilaterally projecting neurons by about 50 to one. This ratio remained relatively stable over a wide range of volumes of injected lectin, whereas the absolute number of labelled neurons on each side varied by at least twofold for a constant volume of lectin. These results provide basic data on the ferret auditory system and demonstrate quantitatively some properties of the projections between the cochlear nucleus and the inferior colliculus.     

Ascending projections of the primary cochlear nuclei and nucleus laminaris in the pigeon

Auditory projections were studied, by the Nauta method, from medullary to mesencephalic levels following lesions in nuclei magnocellularis, angularis and laminaris and transection of the dorsal cochlear decussation and trapezoid body in the midline of the medulla. Fragmented axons project bilaterally to nucleus laminaris from the medial part of nucleus magnocellularis. Degenerated fibers from the lateral part of nucleus magnocellularis, medial part of nucleus angularis. and nucleus laminaris projects to the homolateral superior olivary nucleus. cross the raphé in the trapezoid body, ascend in the contralateral lateral lemniscus, distribute to the ventral and lateroventral nuclei of the lateral lemniscus and, at least third order axons from nucleus laminaris. terminate in nucleus mesencephali lateralis pars dorsalis. No ascending auditory neurons project, even following midventral section of the trapezoid body, to nucleus isthmi, nucleus semilunaris nor. with certainty, to the dorsal nucleus of the lateral lemniscus. This study supports the homology of the avian nucleus mesencephali lateralis pars dorsalis and nucleus laminaris with the mammalian central nucleus of the inferior colliculus and medial superior olivary nucleus respectively. Furthermore, on the basis of fiber projections and cellular organization. nucleus magnocellularis of the pigeon appears to correspond to the anterior ventral cochlear of higher mammals and the medial parts of nucleus angularis to the posterior ventral cochlear nucleus.     

Ascending brain stem projections of the anteroventral cochlear nucleus in the rhesus monkey

In a series of seventeen rhesus monkeys attempts were made to produce discrete stereotaxic lesions in the anteroventral cochlear nucleus (Av). Anterograde degeneration was described in detail in four cases with lesions confined within the cochlear complex to Av. Fibers decussating at pontine levels coursed exclusively in the trapezoid body. Degenerated fibers projected: ipsi-laterally to the lateral superior olivary nucleus; bilaterally to the preolivary nuclei; to the lateral side of the ipsilateral medial superior olive and the medial side of the contralateral medial superior olive; and to the contralateral medial trapezoid nucleus. A topographic projection upon the medial superior olive was demonstrated. Projections were bilateral but mainly crossed to the nuclei of the lateral lemniscus and central nucleus of the inferior colliculus; the posterior end of the ipsilateral ventral nucleus of the lateral lemniscus contained an island of profuse degeneration. A few fibers crossed in the commissure of the inferior colliculus. Few if any fibers from Av projected to the contralateral magnocellular medial geniculate.     

Connections of the dorsal nucleus of the lateral lemniscus: An inhibitory parallel pathway in the ascending auditory system?

This study examines the dorsal nucleus of the lateral lemniscus (DNLL) and its afferent and efferent connections. In Nissl-stained material, DNLL has three parts: dorsal, ventral, and lateral. Although each part contains neurons with similar Nissl patterns, the subdivisions may be distinguished by the size, shape, and orientation of the cells. The lateral DNLL contains a mixture of DNLL neurons and cells from the sagulum. Afferent connections to DNLL were investigated with anterograde axonal transport techniques. Bilateral inputs to DNLL arise from the anteroventral cochlear nucleus and lateral superior olive, while unilateral inputs are provided by the ipsilateral medial superior olive and the contralateral DNLL. The inputs appear to have a tonotopic organization. Afferent fibers to DNLL form horizontal bands that are continuous both mediolaterally and rostrocaudally. All parts of DNLL do not share the same inputs, and a medial-to-lateral gradient in the labeling of some pathways is evident. To study the efferent connections of DNLL, both retrograde and anterograde axonal transport techniques were used. The DNLL projects to the inferior colliculus and the contralateral DNLL. The topography of these projections suggests that areas of similar tonotopic organization are connected. In the inferior colliculus, the projection is heaviest to the central nucleus and extends to the adjacent dorsal and caudal cortex, the rostral pole nucleus, and the ventrolateral nucleus. Axons from DNLL terminate along the fibrodendritic laminae of the central nucleus as bands that are prominent on the contralateral side, whereas those on the ipsilateral colliculus are more diffuse. The afferent and efferent connections of DNLL constitute a multisynaptic pathway, parallel to the other ascending pathways to the inferior colliculus. The other ascending pathways include the direct pathways from the cochlear nucleus to the inferior colliculus and the indirect pathways via the superior olivary complex. Ascending pathways are discussed as to their relationship to the subdivisions of the inferior colliculus, the laterality of their projections, and their banding patterns in the central nucleus. In contrast to the excitatory pathways to the inferior colliculus, the neurons in DNLL may use GABA as a neurotransmitter. Axons from the DNLL terminate in the inferior colliculus as bands that could have a unique inhibitory function. Thus, the multisynaptic, DNLL pathway may provide feed-forward inhibitory inputs to the inferior colliculus, bilaterally, and to the contralateral DNLL.     

HRP study of the organization of auditory afferents ascending to central nucleus of inferior colliculus in cat

The ascending auditory projections to central nucleus of inferior colliculus its ventrolateral and dorsomedial subdivisions (IC_VI, and IC_DM) have been studied in cat using both pressure and electrophoretic injections of horseradish peroxidase (HRP). The results indicate that the predominant ascending projections to inferior colliculus orginate in (1) contralateral cochlear nucleus, (2) contralateral and ipsilateral lateral superior olive, (3) ipsilateral medial superior olive, (4) ipsilateral ventral nucleus of the lateral lemniscus, (5) ipsilateral and contralateral dorsal nucleus of the lateral lemniscus, and (6) contralateral inferior colliculus. In addition, ipsilateral cochlear nucleus, ipsilateral and contralateral intermediate nucleus of the lateral lemniscus, ipsilateral, and to a lesser extent contralateral, periolivary nuclei project to inferior colliculus. Of these nuclei, the lateral superior olive projects exclusively to IC_VL and ipsilateral cochlear nucleus and contralateral inferior colliculus project mostly, if not exclusively, to IC_DM. Many of these projections demonstrate a cochleotopic organization and frequently a nucleotopic organization as well. A cochleotopic organization of the projections is apparent for cochlear nucleus and superior olivary complex. A nucleotopic organization suggests that the heaviest terminations of contralateral inferior colliculus are medial and dorsal in inferior colliculus, of medial superior olive are dorsal and lateral, of superior olivary complex are rostral, of cochlear nucleus are caudal, and of ventral nucleus of the lateral leminiscus are caudal.     

EM autoradiographic study of the projections from the dorsal nucleus of the lateral lemniscus: a possible source of inhibitory inputs to the inferior colliculus

The fine structure of the projection from the dorsal nucleus of the lateral lemniscus (DNLL) to the inferior colliculus is examined in the cat. Anterograde axonal transport of 3H-leucine and EM autoradiographic techniques are used to label axonal endings from DNLL. The primary finding is that axonal endings from DNLL contain pleomorphic synaptic vesicles and make symmetrical synaptic contacts. This morphology is associated with inhibitory synapses. The projection from DNLL is the source of approximately one-third of the axonal endings with pleomorphic vesicles in the central nucleus of the inferior colliculus. In the contralateral central nucleus, only labeled endings with pleomorphic vesicles are found. By comparison, on the ipsilateral side, both endings with pleomorphic vesicles and, to a lesser degree, endings with round vesicles are labeled. Endings from DNLL are more numerous per unit area on the contralateral side. About half of the labeled axonal endings from DNLL terminate upon small dendrites, and another third terminate upon more proximal dendrites and several types of cell bodies. Many axonal endings form multiple synaptic contacts, sometimes on more than one postsynaptic structure. Sites of termination for axonal endings include dendritic spines and branch points of dendrites. These data support the hypothesis that the DNLL pathway to the inferior colliculus may have an inhibitory function. Previous studies show that DNLL neurons exhibit immunoreactivity to GAD and GABA antibodies. The crossed projection of DNLL to the inferior colliculus forms tonotopically organized bands that terminate as endings with pleomorphic vesicles. These endings may supply GABAergic inputs to the inferior colliculus. Thus, bands from DNLL could provide inhibitory inputs and overlap with bands from other sources that provide excitatory inputs. Overlapping bands may form unique synaptic domains in the inferior colliculus. The uncrossed projections from DNLL may provide the inferior colliculus with a more diffusely organized projection that could include excitatory and inhibitory inputs. Since the DNLL on one side may inhibit the opposite DNLL and the inferior colliculus, the DNLL pathway may regulate ascending inhibition to the midbrain. Presumed inhibitory inputs from DNLL to the inferior colliculus could be involved in binaural information processing and contralateral dominance.     

Neurotransmitter-specific uptake and retrograde transport of [3H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus.

Neurotransmitter-specific uptake and retrograde axonal transport of [3H]glycine were used to identify glycinergic projections to the inferior colliculus in chinchillas and guinea pigs. Six h after injection of [3H]glycine in the inferior colliculus, autoradiographically labeled cells were found ipsilaterally in the ventral nucleus of the lateral lemniscus, the lateral superior olive and the dorsomedial periolivary nucleus. These 3 regions accounted for 95% of the labeled projection neurons, with the remainder scattered elsewhere in the ipsilateral superior olivary complex. No labeled cells were found contralaterally even after survival times as long as 24 h. Retrograde transport of HRP from the inferior colliculus in these same cases confirmed the presence of additional projections that did not accumulate [3H]glycine. These included ipsilateral projections from the medial superior olive and cochlear nucleus and contralateral projections from the inferior colliculus, dorsal nucleus of the lateral lemniscus, lateral superior olive, periolivary nuclei and cochlear nucleus. The results implicate uncrossed projections from the ventral nucleus of the lateral lemniscus, lateral superior olive, and dorsomedial periolivary nucleus as the principal sources of inhibitory glycinergic inputs to the inferior colliculus.     

Second order auditory pathways in the chimpanzee

Substantial portions of the dorsal, and almost the entire posteroventral and anteroventral (Av) cochlear nuclei were aspirated unilaterally in a chimpanzee. Axonal degeneration was studied by the Fink-Heimer method. The greatest amount of degeneration was followed medially from the region of Av into the lateral part of the trapezoid body. Degeneration also coursed around the superior surface of the restiform body and was traced into the dorsal and intermediate acoustic striae. Within the superior olivary complex, degeneration was distributed to: the ipsilateral lateral superior olive; laterally and medially oriented dendrites of the ipsilateral and contralateral medial superior olivary nuclei respectively (some periosomatic degeneration also was present bilaterally); the contralateral medial trapezoid nucleus; retro-olivary and preolivary cell groups bilaterally. Abundunt degeneration passed into the contralateral lateral lemniscus and was distributed largely to its ventral nucleus. The contralateral central nucleus of the inferior colliculus was a major site of termination of ascending second order auditory fibers. The caudal tip of the ipsilateral ventral nucleus of the lateral lemniscus received abundant degeneration, but this diminished rostrally. The ipsilateral inferior colliculus contained a moderate amount of degeneration. A fair number of degenerated second order auditory fibers ascended in the contralateral brachium of the inferior colliculus and were distributed both to the principal and magnocellular divisions of the medial geniculate body. This pathway appears to represent a phylogenetic advance in the brain of the great ape.     

Convergence and divergence of ascending binaural and monaural pathways from the superior olives of the mustached bat

The lateral superior olive and medial superior olive give rise to pathways that terminate in the dorsal nucleus of the lateral lemniscus and central nucleus of the inferior colliculus. In most mammals, neurons in both the medial and lateral superior olives are binaural, but in the mustached bat most neurons in the medial superior olive are monaural. The aims of this study were to determine how the inputs to the medial superior olive contribute to its monaurality and to determine whether the ascending projections from the lateral and medial superior olives overlap or rema in segregated at their targets. Injections of two different tracers were placed in tonotopically matched areas of the lateral and medial superior olives in the same animal. Retrograde transport from injections in the medial superior olive labeled spherical cells in the contralateral anteroventral cochlear nucleus and principal cells in the ipsilateral medial nucleus of the trapezoid body. Few cells were labeled in ipsilateral cochlear nucleus. Anterograde transport resulted in tonotopically specific distributions of label with the same laterality as in nonecholocating mammals. In the dorsal nucleus of the lateral lemniscus, label from the lateral and medial superior olives largely overlapped. In the inferior colliculus, label from the two sources overlapped in the high and low frequency ranges, but in the frequency range around 60 kHz, label from the medial superior olive extended more dorsally than that from the lateral superior olive. These results indicate that projections of the lateral and medial superior olives overlap extensively at their targets. © 1995 Willy-Liss, Inc.     

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)     

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 from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei

The projections from the cochlear nucleus to the lateral and medial superior olivary nuclei were studied in the cat by use of retrograde transport of horseradish peroxidase to demonstrate the connections. The medial superior olivary nucleus receives input only from the anterior and posterodorsal subdivisions of the anterior division of the anteroventral cochlear nucleus (AA and APD, respectively; Brawer, Morest, and Kane: J. Comp. Neurol. 155: 251-300, 1974). These two subdivisions are populated almost exclusively by spherical bushy cells. Like the medial superior olivary nucleus, the lateral superior olivary nucleus receives inputs from AA and APD. In addition, the lateral superior olivary nucleus receives projections from the posterior subdivision (AP) of the anterior division and also from the posterior division of the anteroventral cochlear nucleus. The projections to the medial superior olivary nucleus are bilateral, whereas the projections to the lateral superior olivary nucleus are almost entirely ipsilateral. One implication of the results is that the medial superior olivary nucleus receives inputs from only one cell type--the spherical bushy cell--but that, at the least, two cell types project to the lateral superior olivary nucleus. Both the olivary nuclei receive input from most, if not all, of the dorsoventral extent of the anteroventral cochlear nucleus, implying that both receive input from neurons arrayed across the entire frequency representation of the anteroventral cochlear nucleus. All of the projections appear to be organized topographically such that frequency representation is preserved.     

Neurotransmitter-specific uptake and retrograde transport of [H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus

Neurotransmitter-specific uptake and retrograde axonal transport of [³H]glycine were used to identify glycinergic projections to the inferior colliculus in chinchillas and guinea pigs. Six h after injections of [³H]glycine in the inferior colliculus, autoradiographically labeled cells were found ipsilaterally in the ventral nucleus of the lateral lemniscus, the lateral superior olive and the dorsomedial periolivary nucleus. These 3 regions accounted for 95% of the labeled projection neurons, with the remainder scattered elsewhere in the ipsilateral superior olivary complex. No labeled cells were found contralaterally even after survival times as long as 24 h. Retrograde transport of HRP from the inferior colliculus in these same cases confirmed the presence of additional projections that did not accumulate [³H]glycine. These include ipsilateral projections from the medial superior olive and cochlear nucleus and contralateral projections from the inferior colliculus, dorsal nucleus of the lateral lemniscus, lateral superior olive, periolivary nuclei and cochlear nucleus. The results implicate uncrossed projections from the ventral nucleus of the lateral lemniscus, lateral superior olive, and dorsomedial periolivary nucleus as the principal sources of inhibitory glycinergic inputs to the inferior colliculus.     

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.     

Descending auditory pathways: projections from the inferior colliculus contact superior olivary cells that project bilaterally to the cochlear nuclei.

Multiple retrograde and anterograde tracers were used to characterize a pathway that extends from the inferior colliculus to both the left and right cochlear nuclei via a synaptic relay in the superior olivary complex. Different fluorescent tracers were injected into the left and right cochlear nuclei to identify cells in the superior olivary complex that project bilaterally. Double-labeled cells were present in almost all periolivary nuclei; the majority were located in the ventral nucleus of the trapezoid body and the anteroventral periolivary nucleus. Because these two nuclei are targets of descending projections from the inferior colliculus, triple-labeling experiments were performed to determine whether collicular axons contact the periolivary cells that project to the cochlear nuclei. The results demonstrate that descending axons from the inferior colliculus contact periolivary cells that project to the cochlear nuclei, including periolivary cells that project bilaterally. This pathway could provide an opportunity for higher levels of the auditory system to influence activity bilaterally in the cochlear nuclei and thus to modulate the initial processing of acoustic information by the brain.     

Differential ascending projections to aural regions in the 60 kHz contour of the mustache bat's inferior colliculus

The inferior colliculus of the mustache bat is similar in many respects to the inferior colliculus of more commonly studied mammals. However, the isofrequency contour devoted to processing 60 kHz, the dorsoposterior division (DPD) is greatly expanded, encompassing an area approximately equal to one-third of the central nucleus. Of particular significance is that monaural and binaural neurons are segregated in the DPD into 4 spatially distinct aural regions. In this study we exploit the great enlargement of the 60 kHz region in the central nucleus of the inferior colliculus (ICc) of the mustache bat to determine the source of ascending projections to the 4 different aural regions of the DPD. Small iontophoretic deposits of HRP were made within each of the physiologically defined aural regions, and the locations and numbers of retrogradely labeled cells in the auditory brainstem nuclei were determined. Two major features of collicular organization were found. The first is that each aural region receives a unique set of projections from a subset of lower auditory nuclei and thus is distinguished both by its neural response properties and by the pattern of ascending projections it receives. The dorsomedial EE region receives inputs primarily from the ipsilateral intermediate nucleus of the lateral lemniscus (INLL) and ventral nucleus of the lateral lemniscus (VNLL), and the contralateral ICc. In contrast, the ventrolateral EE region receives projections from the ipsilateral medial superior olivary nucleus (MSO), VNLL, and INLL. The inputs to the EI region originate primarily from the dorsal nucleus of the lateral lemniscus (DNLL) and lateral superior olivary nucleus (LSO) bilaterally and from the ipsilateral INLL. The afferents to the EO region include the contralateral cochlear nucleus, the ipsilateral VNLL and INLL and MSO. The second major organizational feature is that the binaural nuclei of the brain-stem project upon the DPD in a more restricted manner than do some of the lower monaural nuclei, such as the VNLL and INLL, which project in a more widespread manner. The unique set of projections terminating in each aural region of the DPD suggests that the neurons should have substantially different properties, even when neurons in different regions are of the same general aural type. Moreover, the elucidation of the micro-organization of the DPD provides insights into the different ways that binaural properties of DPD neurons are created by the convergence of inputs from particular subsets of lower auditory nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cochlear and middle ear effects on metabolism in the central auditory pathway during silence: A 2-deoxyglucose study

The [¹⁴C]2-deoxy-d-glucose (2-DG) autoradiographic technique was used to investigate metabolic activity in the central auditory pathways during silence. Relative 2-DG uptake was assessed in silence for three groups of Mongolian gerbils: control animals; those with unilateral cochlear ablations, and those with unilateral conductive hearing losses. Control subjects showed no differences between the two sides of their central auditory pathways. Subjects with unilateral cochlear ablations showed markedly lower 2-DG uptake in the major afferent projection pathway from the ablated cochlea compared with 2-DG uptake in contralateral structures. That is, relative 2-DG uptake was significantly lower ipsilateral to the ablation in the anteroventral and dorsal cochlear nuclei, and contralateral to the ablation in the ventral nucleus of the lateral lemniscus, the dorsal nucleus of the lateral lemniscus, and the inferior colliculus. No effect of ablation was seen in the superior olivary complex, the medial geniculate nucleus or the auditory cortex. Subjects with a unilateral conductive hearing loss, unexpectedly, showed significantly higher 2-DG incorporation in the major afferent projection from the impaired side. That is, relative 2-DG uptake was higher in the anteroventral cochlear nucleus, the dorsal cochlear nucleus and the lateral superior olivary nucleus ipsilateral to the hearing loss, and in the dorsal nucleus of the lateral lemniscus contralateral to the hearing loss. These increases in 2-DG uptake following conductive hearing loss represent a mechanism which may account for clinical hearing disorders such as tinnitus. It is concluded that, even under conditions of silence, the intact cochlea and middle ear conductive apparatus significantly influence metabolic activity in the central auditory pathway up through the level of the inferior colliculus.