Projections from the spinal trigeminal nucleus to the cochlear nucleus in the rat

The integration of information across sensory modalities enables sound to be processed in the context of position, movement, and object identity. Inputs to the granule cell domain (GCD) of the cochlear nucleus have been shown to arise from somatosensory brain stem structures, but the nature of the projection from the spinal trigeminal nucleus is unknown. In the present study, we labeled spinal trigeminal neurons projecting to the cochlear nucleus using the retrograde tracer, Fast Blue, and mapped their distribution. In a second set of experiments, we injected the anterograde tracer biotinylated dextran amine into the spinal trigeminal nucleus and studied the resulting anterograde projections with light and electron microscopy. Spinal trigeminal neurons were distributed primarily in pars caudalis and interpolaris and provided inputs to the cochlear nucleus. Their axons gave rise to small (1-3 microm in diameter) en passant swellings and terminal boutons in the GCD and deep layers of the dorsal cochlear nucleus. Less frequently, larger (3-15 microm in diameter) lobulated endings known as mossy fibers were distributed within the GCD. Ventrally placed injections had an additional projection into the anteroventral cochlear nucleus, whereas dorsally placed injections had an additional projection into the posteroventral cochlear nucleus. All endings were filled with round synaptic vesicles and formed asymmetric specializations with postsynaptic targets, implying that they are excitatory in nature. The postsynaptic targets of these terminals included dendrites of granule cells. These projections provide a structural substrate for somatosensory information to influence auditory processing at the earliest level of the central auditory pathways.     

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.     

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.     

Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat

A reciprocal connection is known to exist between the cuneate nucleus, which is a first-order somatosensory nucleus, and the cochlear nucleus, which is a first-order auditory nucleus. We continued this line of study by investigating the fiber endings of this projection in the cochlear nucleus of rats using the neuronal tracer Phaseolus vulgaris leucoagglutinin in combination with ultrastructural and immunocytochemical analyses. In the cochlear nucleus, mossy fiber terminals had been described and named for their morphologic similarity to those in the cerebellum, but their origins had not been discovered. In the present study, we determined that the axonal projections from the cuneate region gave rise to mossy fiber terminals in the granule cell regions of the ipsilateral cochlear nucleus. The cuneate mossy fibers appear to be excitatory in nature, because they are filled with round synaptic vesicles, they make asymmetric synapses with postsynaptic targets, and they are labeled with an antibody to glutamate. The postsynaptic targets of the mossy fibers include dendrites of granule cells. This projection onto the granule cell interneuron circuit of the cochlear nucleus indicates that somatosensory cues are intimately involved with information processing at this early stage of the auditory system. © 1996 Wiley-Liss, Inc.     

Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat

The afferent projections to the lateral superior olive (LSO) were examined with horseradish peroxidase, horseradish peroxidase-wheat germ agglutinin conjugate, 125I-wheat germ agglutinin and tritiated leucine autoradiograhy, anterograde axonal degeneration, and 14C-2-deoxyglucose methods. The pathway to the ipsilateral LSO orginates in the spherical cells in anteroventral cochlear nucleus. Although some of the fibers pass above the lateral nucleus of the trapezoid body, most pass below it and turn at right angles to enter the LSO either directly through its ventral, lateral, or dorsal borders, or through its ventral or dorsal hilus. They end in unpolarized terminal fields throughout the LSO. Most if not all of these fibers are true collaterals of axons continuing across the midline in the trapezoid body. Verifying Held's (1893) finding of a major direct projection from the cochlear nucleus to the contralateral medial nucleus of the trapezoid body (MTB) and Rasmussen's ('46) finding of a major projection from the MTB to the LSO, the present results illustrate that this two-neuron pathway probably supplies all but a very small component of the relatively direct input to the LSO from the contralateral ear. This pathway originates in the globular cells of the ventral cochlear nucleus and relays mostly though not exclusively through the "principal cells" in the more rostral parts of the MTB. It terminates mostly in perisomal endings in unpolarized fields throughout the LSO, though most heavily within the (high frequency) medial and middle limbs and less heavily in the LSO's (low frequency) lateral limb. In addition to this indirect pathway, there is a small direct pathway to the contralateral LSO as suggested by Goldberg and Brown ('69) and Warr ('72, '82). This direct pathway to the contralateral LSO, like the direct ipsilateral pathway, probably originates in the spherical cell region of the ventral cochlear nucleus, crosses the midline in the trapezoid body, and terminates in a small circumscribed area within the LSO's ventromedial (high frequency) area. The 2-deoxyglucose method applied to cats in which the ipsilateral and contralateral pathways have been surgically isolated shows that each of the pathways converging on the LSO is topographically and tonotopically organized with the ipsilateral and the combined contralateral terminations in strict tonotopic register.     

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.     

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.     

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.     

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.     

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.     

Chemical anatomy of excitatory endings in the dorsal cochlear nucleus of the rat: Differential synaptic distribution of aspartate aminotransferase,glutamate, and vesicular zinc

In order to identify cytochemical traits relevant to understanding excitatory neurotransmission in brainstem auditory nuclei, we have analyzed in the dorsal cochlear nucleus the synaptic distribution of aspartate aminotransferase, glutamate, and vesicular zinc, three molecules probably involved in different steps of excitatory glutamatergic signaling. High levels of glutamate immunolabeling were found in three classes of synaptic endings in the dorsal cochlear nucleus, as determined by quantitation of immunogold labeling. The first type included auditory nerve endings, the second were granule cell endings in the molecular layer, and the third very large endings, better described as “mossy.” This finding points to a neurotransmitter role for glutamate in at least three synaptic populations in the dorsal cochlear nucleus. The same three types of endings enriched in glutamate immunoreactivity also contained histochemically detectable levels of aspartate aminotransferase activity, suggesting that this enzyme may be involved in the synaptic handling of glutamate in excitatory endings in the dorsal cochlear nucleus. There was also extrasynaptic localization of the enzyme. Zinc ions were localized exclusively in granule cell endings, as determined by a Danscher-selenite method, suggesting that this ion is involved in the operation of granule cell synapses in the dorsal cochlear nucleus. J. Comp. Neurol. 399:341–358, 1998. © 1998 Wiley-Liss, Inc.     

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.     

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.     

Projections of the trapezoid body and the superior olivary complex of the Kangaroo rat (Dipodomys merriami).

Glass micropipettes filled with 2 M sodium cyanide were used to physiologically locate and iontophoretically damage the nucleus of the trapezoid body (NTB), the medial superior olive (MSO), and the lateral superior olive (LSO). Mechanical lesions were made in the trapezoid body as it leaves the cochlear nuclei. After a 3- to 10-day survival time the projections and terminal degeneration were traced with the Fink-Heimer and Nauta-Gygax stains. The ventral cochlear nucleus (VCN) projects via the trapezoid body to ipsilateral LSO, ipsilateral preolivary nuclei, ipsilateral lateral and a contralateral medial dendritic fields of MSO, and contralateral NTB; there is also a small ipsilateral projection to the ventral nucleus of the lateral lemniscus (VNLL) and the central nucleus of the inferior colliculus (CNIC). Some trapezoid body fibers ascend via the contralateral lateral lemniscus to VNLL, DNLL (dorsal nucleus of the lateral lemniscus), and CNIC. There is no projection from the ventral cochlear nucleus to the ipsilateral NTB and contralateral preolivary nuclei. All portions of NTB project ipsilaterally to LSO (ventral NTB to dorsomedial LSO, dorsal NTB to ventral LSO) and to the retro-olivary nucleus. In two animals with NTB lesions there is also degeneration in the ventromedial portion of the ipsilateral facial nucleus. NTB projects contralaterally by way of the stria of Monakow to the pyramidal and molecular cell layers of the dorsal cochlear nucleus (DCN). The NTB does not project ipsilaterally to MSO, preolivary nuclei, VNLL, DNLL and CNIC. Contralaterally there are no projections to any of the nuclei of the auditory pathway except the DCN. Most MSO projections are ipsilateral. The densest goes by way of the lateral lemniscus to the lateral aspect of the ipsilateral CNIC, terminating throughout its dorsoventral axis. MSO also projects bilaterally to the pyramidal and molecular cell layers of dorsal cochlear nucleus (DCN), and ipsilaterally to the ventral portion of the motor nucleus of V and to the facial nucleus. MSO does not project ipsilaterally to the LSO, NTB, preolivary, VCN and retro-olivary nuclei. On the contralateral side, all structures except the DCN are free of projection patterns from axons originating in the MSO. LSO projects bilaterally to the central and ventral portions of CNIC and to the nuclei of the lateral lemnisci, and ipsilaterally to the large and small spherical cell areas of anterior ventral cochlear nucleus (AVCN) and to all portions of DCN. The LSO does not project ipsilaterally to the NTB, MSO, preolivary and retro-olivary nuclei. On the side opposite, this nucleus does not project to NTB, MSO, retro-olive, VCN, preolivary and LSO. For all lesions regardless of the site, there is no degeneration found rostral to the CNIC. The medial geniculate body or other structures in the diencephalon or cortex are free of any fields of terminal degeneration.     

The projection of the acoustic nerve to the ventral cochlear nucleus of the rat. A Golgi study

Acoustic nerve fibers, stained by the rapid Golgi method, were observed to bifurcate, after entering the ventral cochlear nucleus, into an ascending and a descending branch. Each branch was composed of fibers running parallel to each other with very little overlap. Prior to bifurcating, the acoustic nerve fibers gave rise to collaterals which ramified in the region of the bifurcations. Ascending branch fibers terminated in bulbs of Held and bore from zero to five additional collateral endings, including bulbs of Held. Descending, branch fibers gave rise within the posterior ventral cochlear nucleus to from zero to five collateral endings. These included large endings identified as bulbs of Held. Ascending and descending branch collaterals did not extend beyond 40–50 μ from their paret axons. Descending branch fibers projected into the dorsal cochlear nucleus. The area of the ventral cochlear nucleus dorsal to the region of bifurcations was innervated in a unique manner. This innervation occurred via long dorsally running collaterals arising from the most dorsal fibers of the ascending and descending branch projections. The data suggest morphological correlates of certain neurophysiological and behavioral findings in the areas of auditory localization and discrimination.     

Development of ventral cochlear nucleus projections to the superior olivary complex in gerbil

The postnatal development of the projection from the ventral cochlear nucleus to the principal nuclei in the superior olivary complex in gerbil (Meriones unguiculatus) was studied in an age-graded series of pups ranging from 0 to 18 days old. Small crystals of 1, 1′-dioctadecyl3, 3, 3′, 3′-tetramethylindocarbocyanine perchlorate (DiI) were inserted into the ventral cochlear nucleus of aldehyde-fixed brains, and the labeled projections were examined with epifluorescence microscopy. Selected sections were photooxidized in a solution of diaminobenzidine and subsequently processed for electron microscopy to examine the development of labeled synapses in the target nuclei. Horseradish peroxidase was injected into the ventral cochlear nucleus of adult gerbils to assess the form and persistence of projections observed in the neonatal animals. In addition, electrophysiological responses to acoustic stimuli of single units in the adult auditory brainstem were analyzed to confirm the functionality of the novel projection from the ventral cochlear nucleus to the contralateral lateral superior olive. By the day of birth (PO), developing axons from the ventral cochlear nucleus have already established highly ordered pathways to the three primary nuclei of the superior olivary complex: the ipsilateral lateral superior olive, the contralateral medial nucleus of the trapezoid body, and at the lateral and medial dendrites of the ipsilateral and contralateral medial superior olive, respectively. Developing axons from the ventral cochlear nucleus that innervated the contralateral medial nucleus of the trapezoid body lacked the terminal morphology characteristic of the calyx of Held, but began to adopt a more characteristic form on P5. The mature calyx appeared around P14–16. Exuberant developmental projections to topographically inappropriate areas of the superior olivary complex were not observed at the postnatal ages studied. In addition to the projections of the ventral cochlear nucleus to the superior olivary complex described in other species, we observed the development and maintenance of a major direct projection from the ventral cochlear nucleus to the contralateral lateral superior olive. On PO, ventral cochlear nucleus axons decussate in the dorsal trapezoid body, form a plexus at the dorsal edge of the contralateral medial superior olive, and enter the ventrolateral limb of the contralateral lateral superior olive. Over the next 2 weeks, fascicles of fibers form on the hilar and ventral aspects of the ventrolateral limb. Fibers arising from these fascicles form converging, but nonoverlapping, arborizations within the ventrolateral limb at right angles to the curvature of the nucleus. The medial region was devoid of labeled axons. The direct innervation of the contralateral lateral superior olive was confirmed in the adult gerbil with anterograde horseradish peroxidase histochemistry and by the recording of excitatory responses in the innervated region to acoustic stimulation of the contralateral ear. © 1995 Wiley-Liss, Inc.     

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.     

Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: Mossy fiber endings and their targets

The principal projection neurons of the cochlear nucleus receive the bulk of their input from the auditory nerve. These projection neurons reside in the core of the nucleus and are surrounded by an external shell, which is called the granule cell domain. Interneurons of the cochlear granule cell domain are the target for nonprimary auditory inputs, including projections from the superior olivary complex, inferior colliculus, and auditory cortex. The granule cell domain also receives projections from the cuneate and trigeminal nuclei, which are first-order nuclei of the somatosensory system. The cellular targets of the nonprimary projections are mostly unknown due to a lack of information regarding postsynaptic profiles in the granule cell areas. In the present paper, we examined the synaptic relationships between a heterogeneous class of large synaptic terminals called mossy fibers and their targets within subdivisions of the granule cell domain known as the lamina and superficial layer. By using light and electron microscopic methods in these subdivisions, we provide evidence for three different neuron classes that receive input from the mossy fibers: granule cells, unipolar brush cells, and a previously undescribed class called chestnut cells. The distinct synaptic relations between mossy fibers and members of each neuron class further imply fundamentally separate roles for processing acoustic signals. © 1996 Wiley-Liss, Inc.     

The subcortical auditory structures in the Mongolian gerbil: II. Frequency‐related topography of the connections with cortical field AI

We investigated the frequency‐related topography of connections of the primary auditory cortical field (AI) in the Mongolian gerbil with subcortical structures of the auditory system by means of the axonal transport of two bidirectional tracers, which were simultaneously injected into regions of AI with different best frequencies (BFs). We found topographic, most likely frequency‐matched (tonotopic) connections as well as non‐topographic (non‐tonotopic) connections. AI projects in a tonotopic way to the ipsilateral ventral (MGv) and dorsal divisions (MGd) of the medial geniculate body (MGB), the reticular thalamic nucleus and dorsal nucleus of the lateral lemniscus, and the ipsi‐ and contralateral dorsal cortex of the inferior colliculus (IC) and central nucleus of the IC. AI receives tonotopic inputs from MGv and MGd. Projections from different BF regions of AI terminate in a non‐tonotopic way in the ipsilateral medial division of the MGB (MGm), the suprageniculate thalamic nucleus (SG) and brachium of the IC (bic), and the ipsi‐ and contralateral external cortex and pericollicular areas of the IC. The anterograde labeling in the intermediate and ventral nucleus of the lateral lemniscus, parts of the superior olivary complex, and divisions of the cochlear nucleus was generally sparse; thus a clear topographic arrangement of the labeled axons could not be ruled out. AI receives non‐tonotopic inputs from the ipsilateral MGm, SG, and bic. In conclusion, the tonotopic and non‐tonotopic corticofugal connections of AI can potentially serve for both conservation and integration of frequency‐specific information in the respective target structures. J. Comp. Neurol. 521:2772–2797, 2013. © 2013 Wiley Periodicals, Inc.     

Organization of the auditory brainstem in a lizard, Gekko gecko. I. Auditory nerve, cochlear nuclei, and superior olivary nuclei

We used tract tracing to reveal the connections of the auditory brainstem in the Tokay gecko (Gekko gecko). The auditory nerve has two divisions, a rostroventrally directed projection of mid- to high best-frequency fibers to the nucleus angularis (NA) and a more dorsal and caudal projection of low to middle best-frequency fibers that bifurcate to project to both the NA and the nucleus magnocellularis (NM). The projection to NM formed large somatic terminals and bouton terminals. NM projected bilaterally to the second-order nucleus laminaris (NL), such that the ipsilateral projection innervated the dorsal NL neuropil, whereas the contralateral projection crossed the midline and innervated the ventral dendrites of NL neurons. Neurons in NL were generally bitufted, with dorsoventrally oriented dendrites. NL projected to the contralateral torus semicircularis and to the contralateral ventral superior olive (SOv). NA projected to ipsilateral dorsal superior olive (SOd), sent a major projection to the contralateral SOv, and projected to torus semicircularis. The SOd projected to the contralateral SOv, which projected back to the ipsilateral NM, NL, and NA. These results suggest homologous patterns of auditory connections in lizards and archosaurs but also different processing of low- and high-frequency information in the brainstem.