Trigeminal ganglion innervates the auditory brainstem

A neural connection between the trigeminal ganglion and the auditory brainstem was investigated by using retrograde and anterograde tract tracing methods: iontophoretic injections of biocytin or biotinylated dextran-amine (BDA) were made into the guinea pig trigeminal ganglion, and anterograde labeling was examined in the cochlear nucleus and superior olivary complex. Terminal labeling after biocytin and BDA injections into the ganglion was found to be most dense in the marginal cell area and secondarily in the magnocellular area of the ventral cochlear nucleus (VCN). Anterograde and retrograde labeling was also seen in the shell regions of the lateral superior olivary complex and in periolivary regions. The labeling was seen in the neuropil, on neuronal somata, and in regions surrounding blood vessels. Retrograde labeling was investigated using either wheatgerm agglutinin-horseradish peroxidase (WGA-HRP), BDA, or a fluorescent tracer, iontophoretically injected into the VCN. Cells filled by retrograde labeling were found in the ophthalmic and mandibular divisions of the trigeminal ganglion. We have previously shown that these divisions project to the cochlea and middle ear, respectively. This study provides the first evidence that the trigeminal ganglion innervates the cochlear nucleus and superior olivary complex. This projection from a predominantly somatosensory ganglion may be related to integration mechanisms involving the auditory end organ and its central targets.     

Convergence of spinal trigeminal and cochlear nucleus projections in the inferior colliculus of the guinea pig

In addition to ascending auditory inputs, the external cortex of the inferior colliculus (ICX) receives prominent somatosensory inputs. To elucidate the extent of interaction between auditory and somatosensory representations at the level of IC, we explored the dual projections from the cochlear nucleus (CN) and the spinal trigeminal nucleus (Sp5) to the inferior colliculus (IC) in the guinea pig, using both retrograde and anterograde tracing techniques. Injections of retrograde tracers into ICX resulted in cell-labeling primarily in the contralateral DCN and pars interpolaris and caudalis of Sp5. Labeled cells in DCN were either fusiform or multipolar cells, whereas those in Sp5 varied in size and shape. Injections of anterograde tracers into either CN or Sp5 resulted in terminal labeling in ICX primarily on the contralateral side. Most projection fibers from Sp5 terminated in a laminar pattern from ventromedial to dorsolateral within the ventrolateral ICX, the ventral border of IC, and the ventromedial edge of IC (collectively termed "the ventrolateral border region of IC," ICXV). Less dense anterograde labeling was observed in lateral and rostral ICX. Injecting different tracers into both Sp5 and CN confirmed the overlapping areas of convergent projections from Sp5 and CN in IC: The most intense dual labeling was seen in the ICXV, and less intense dual labeling was also observed in the rostral part of ICX. This convergence of projection fibers from CN and Sp5 provides an anatomical substrate for multimodal integration in the IC.     

Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus

Projections of glutamatergic somatosensory and auditory fibers to the cochlear nucleus (CN) are mostly nonoverlapping: projections from the spinal trigeminal nucleus (Sp5) terminate primarily in the granule cell domains (GCD) of CN, whereas type I auditory nerve fibers (ANFs) project to the magnocellular areas of the VCN (VCNm) and deep layers of Dorsal CN (DCN). Vesicular glutamate transporters (VGLUTs), which selectively package glutamate into synaptic vesicles, have different isoforms associated with distinct subtypes of excitatory glutamatergic neurons. Here we examined the distributions of VGLUT1 and VGLU2 expression in the CN and their colocalization with Sp5 and ANF terminals following injections of anterograde tracers into Sp5 and the cochlea in the guinea pig. The CN regions that showed the most intense expression of VGLUT1 and VGLUT2 were largely nonoverlapping and were consistent with ANF and Sp5 projections, respectively: VGLUT1 was highly expressed in VCNm and the molecular layer of the DCN, whereas VGLUT2 was expressed predominantly in the GCD. Half (47% +/- 3%) of the Sp5 mossy fiber endings colabeled with VGLUT2, but few (2.5% +/- 1%) colabeled with VGLUT1. In contrast, ANFs colabeled predominantly with VGLUT1. The pathway-specific expression of VGLUT isoforms in the CN may be associated with the intrinsic synaptic properties that are unique to each sensory pathway.     

GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil

The anatomical localization of glutamic acid decarboxylase (GAD), the synthesizing enzyme for GABA, was analyzed in the brainstem auditory nuclei of the adult gerbil. GAD-positive terminals and somata were present in the cochlear nucleus, superior olivary complex, lateral lemniscus, and inferior colliculus in varying concentrations and patterns. One of the highest densities of GAD-positive terminals is found in the superficial layers of the dorsal cochlear nucleus (DCN), whereas the ventral cochlear nucleus (VCN) has somewhat fewer terminals that are arranged in pericellular plexuses. GAD-positive neurons occur mainly in the superficial and fusiform layers of the DCN and are scattered throughout the VCN. Within the superior olivary complex, the highest concentration of immunoreactive terminals and neurons occurs in the ventral and lateral nuclei of the trapezoid body. In contrast, the medial nucleus of the trapezoid body and the medial superior olive contain fewer GAD-positive puncta and probably no immunoreactive somata. The lateral superior olive and superior periolivary nucleus contain a few immunoreactive puncta but a large number of immunoreactive somata. In the midbrain, the nuclei of the lateral lemniscus contain a moderate number of GAD-positive puncta and a large number of different types of GAD-positive neurons. The inferior colliculus also contains a heterogeneous population of labeled somata, most of which are multipolar neurons. In addition, a high concentration of immunoreactive puncta occurs in this region. These data demonstrate a diverse distribution of GAD-positive neurons and puncta throughout the brainstem auditory nuclei and suggest that GABA might be an important neurotransmitter in the processing of auditory information.     

Tuberculoventral neurons project to the multipolar cell area but not to the octopus cell area of the posteroventral cochlear nucleus.

Tuberculoventral neurons in the deep layer of the dorsal cochlear nucleus (DCN) provide frequency-specific inhibition to neurons in the anteroventral cochlear nucleus (AVCN) of the mouse (Wickesberg and Oertel, '88, '90). The present experiments examine the projection from the deep DCN to the posteroventral cochlear nucleus (PVCN). Horseradish peroxidase (HRP) injections into the PVCN reveal that the multipolar cell area, but not the octopus cell area, is innervated by neurons in the deep layer of the DCN. Injections into the multipolar cell area, in the rostral and ventral PVCN, labeled neurons across the entire rostrocaudal extent of the deep DCN. The labeled tuberculoventral neurons generally lay within the band of labeled auditory nerve terminals in the DCN. Injections of HRP into the octopus cell area, in the dorsal caudal PVCN, labeled almost no cells within the band of auditory nerve fiber terminals that were labeled by the same injection. The inhibition from tuberculoventral neurons onto ventral cochlear nucleus (VCN) neurons is likely to be mediated by glycine (Wickesberg and Oertel, '90). Slices of the cochlear nuclear complex were immunolabeled by an antibody against glycine conjugated with glutaraldehyde to bovine serum albumin (Wenthold et al., '87). Glycine-like immunoreactivity was found throughout the DCN, the AVCN and the multipolar cell area, but there was little labeling in the octopus cell area. This finding provides independent evidence that tuberculoventral neurons do not innervate the octopus cell area and indicates that the octopus cell area is anatomically and functionally distinct.     

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 of the pontine nuclei to the cochlear nucleus in rats.

In the cochlear nucleus, there is a magnocellular core of neurons whose axons form the ascending auditory pathways. Surrounding this core is a thin shell of microneurons called the granule cell domain (GCD). The GCD receives auditory and nonauditory inputs and projects in turn to the dorsal cochlear nucleus, thus appearing to serve as a central locus for integrating polysensory information and descending feedback. Nevertheless, the source of many of these inputs and the nature of the synaptic connections are relatively unknown. We used the retrograde tracer Fast Blue to demonstrate that a major projection arises from the contralateral pontine nuclei (PN) to the GCD. The projecting cells are more densely located in the ventral and rostral parts of the PN. They also are clustered into a lateral and a medial group. Injections of anterograde tracers into the PN labeled mossy fibers in the contralateral GCD. The terminals are confined to those parts of the GCD immediately surrounding the ventral cochlear nucleus. There is no PN projection to the dorsal cochlear nucleus. These endings have the form of bouton and mossy fiber endings as revealed by light and electron microscopy. The PN represent a key station between the cerebral and cerebellar cortices, so the pontocochlear nucleus projection emerges as a significant source of highly processed information that is introduced into the early stages of the auditory pathway. The cerebropontocerebellar pathway may impart coordination and timing cues to the motor system. In an analogous way, perhaps the cerebropontocochlear nucleus projection endows the auditory system with a timing mechanism for extracting temporal information.     

Axonal pathways to the lateral superior olive labeled with biotinylated dextran amine injections in the dorsal cochlear nucleus of rats

The lateral superior olive (LSO) contains cells that are sensitive to intensity differences between the two ears, a feature used by the brain to localize sounds in space. This report describes a source of input to the LSO that complements bushy cell projections from the ventral cochlear nucleus (VCN). Injections of biotinylated dextran amine (BDA) into the dorsal cochlear nucleus (DCN) of the rat label axons and swellings in several brainstem structures, including the ipsilateral LSO. Labeling in the ipsilateral LSO was confined to a thin band that extended throughout the length of the structure such that it resembled an LSO isofrequency lamina. The source of this labeled pathway was not obvious, because DCN neurons do not project to the LSO, and VCN bushy cells were not filled by these injections. Filled neurons in several brainstem structures emerged as possible sources. Three observations suggest that most of the axonal labeling in the LSO derives from a single source. First, the number of labeled VCN planar multipolar cells and the amount of labeling in the LSO were consistent and robust across animals. In contrast, the number of labeled cells in most other structures was small and highly variable. Second, the locations of planar cells and filled axons in the LSO were related topographically to the position of the DCN injection site. Third, labeled terminal arborizations in the LSO arose from collaterals of axons in the trapezoid body (output tract of planar cells). We infer that planar multipolar cells, in addition to bushy cells, are a source of ascending input from the cochlear nucleus to the LSO.     

Trigeminocerebellar, trigeminotectal, and trigeminothalamic projections: a double retrograde axonal tracing study in the mouse

Double retrograde axonal tracing experiments were carried out in order to reveal potential patterns of divergence in axonal projections from the two major sensory nuclei of the mouse brainstem trigeminal complex: the principal sensory and spinal trigeminal nuclei (oralis, interpolaris, and caudalis divisions). The tracers wheat germ agglutinin, N-[acetyl-3H] and horseradish peroxidase were used in paired injection strategies within portions of the cerebellum, superior colliculus, and thalamic ventrobasal complex and/or posterior group of adult ICR white mice. Trigeminal neurons with projections to tactile areas of the cerebellar cortex or underlying deep cerebellar nuclei were found scattered throughout the principal sensory nucleus and interpolaris division, and mainly in dorsal regions of the oralis division of the spinal trigeminal nucleus. Injections of either tracer which involved lateral portions of the rostral half of the superior colliculus labeled trigeminotectal neurons mainly in the contralateral interpolaris division, ventral half of the oralis division, and a ventral region of the principal sensory nucleus near the oralis border. Fewer trigeminotectal neurons were found scattered throughout the principal sensory nucleus and the magnocellular layer of the caudalis divisions, although an occasional labeled neuron wa also found in the marginal layer. Contralaterally projecting trigeminothalamic neurons were observed throughout the principal sensory nucleus, interpolaris division, and within the marginal and magnocellular layers of caudalis. Double-labeled neurons were observed only after paired injections of the tracers in the thalamus and ipsilateral superior colliculus, and they were found within the caudoventral portion of the principal sensory nucleus near the oralis border, throughout the interpolaris division, within the magnocellular layer of caudalis, and only a few double-labeled neurons were also found within the marginal layer. After such injections, 50% of the labeled tectum-projecting neurons in the principal sensory nucleus, 64% in the interpolaris division, and 57% in the caudalis division are branched neurons which have collateralized projections to both the superior colliculus and thalamus. These projections, which have not been described before, appear to arise from more than one class of projection neuron which is differentially distributed within different regions of the trigeminus.     

In vitro modulation of somatic glycine-like immunoreactivity in presumed glycinergic neurons

Previous studies indicate that tuberculoventral and cartwheel cells in the dorsal cochlear nucleus as well as a group of stellate cells in the ventral cochlear nucleus are likely to be glycinergic. To test whether these neurons contain higher levels of free glycine than cells that are probably not glycinergic, immunocytochemical studies with antibodies against glycine conjugates were undertaken on slices of the murine cochlear nuclear complex. Present results show that the cell bodies of all three groups of neurons are immunolabeled. However, the somatic labeling of the tuberculoventral and cartwheel cells can be modulated by experimental conditions. In slices fixed immediately after cutting, many cell bodies in the deep layer of the dorsal cochlear nucleus (DCN), presumably tuberculoventral neurons, are labeled. As a slice is incubated in vitro, cell bodies in the deep layer of the DCN lose their glycine-like immunoreactivity. After 7 hours in vitro, labeled cells are absent in the deep DCN, but the immunoreactivity can be regained by electrically stimulating the auditory nerve for 20 minutes. The loss of immunoreactivity is prevented by electrical stimulation, by axotomy, and by inclusion of 0.8 μM tetrodotoxin, or 1 μM strychnine, or 50 μM colchicine or 50 μM μ-lumicolchicine in the bathing saline. Cartwheel cells retain their immunoreactivity during incubation in vitro without electrical stimulation, but lose it under two conditions. One is following a cut across the ventral cochlear nucleus (VCN) that severs most of their granule cell input, and the other is the inclusion of tetrodotoxin in the bathing saline. The labeling of cell bodies in the ventral cochlear nucleus and of puncta and processes is not changed by any of these experimental manipulations. © 1994 Wiley-Liss, Inc.     

Collaterals from lateral and medial olivocochlear efferent neurons innervate different regions of the cochlear nucleus and adjacent brainstem.

Two populations of superior olivary neurons which project to different sensory cell regions in the cochlea also give off collateral projections to the ventral cochlear nucleus (VCN) and adjacent brainstem. To determine whether these VCN projections also have different targets they were characterized by selective retrograde amino acid transport. Retrograde transport of 3H-d-aspartate (D-ASP) selectively labeled the unmyelinated fibers and neurons of the lateral olivocochlear (OC) system including a dense collateral projection to the central VCN. Retrograde transport of 3H-nipecotic acid (NIP) labeled the myelinated fibers and neurons of the medial OC system, including collateral projections to the peripheral VCN, subpeduncular granule cells, and nucleus Y. Medial and lateral OC efferent collaterals thus innervate different regions of the CN. Lateral system collaterals overlap extensively with Type I spiral ganglion cell afferent input. They are well positioned to play a role in modulating afferent input to the central auditory system, as is the primary projection of these efferents to the cochlea. The medial system collaterals project near the recently described afferent projections of Type II spiral ganglion cells. The medial system collaterals may therefore be related to the function of outer hair cells, as the medial system primary axons appear to be in the cochlea.     

Somatosensory projection to the mesencephalon: an anatomical study in the monkey

The terminal areas and cells of origin of the somatosensory projection to the mesencephalon in the monkey were investigated by the intraaxonal transport method. Following injection of wheat germ agglutinin-horseradish peroxidase conjugate (WGA-HRP) into the spinal enlargements, the lateral cervical nucleus (LCN), the dorsal column nuclei (DCN), or the spinal trigeminal nucleus, anterograde labeling was observed in several regions of the mid-brain. (1) Injection of tracer into the spinal enlargements resulted in dense terminal labeling in the parabrachial nucleus (PBN) and the periaqueductal gray matter (PAG); moderate termination was observed in the intercollicular nucleus (Inc), the intermediate and deep gray layers of the superior colliculus (SGI, SGP), the posterior pretectal nucleus (PTP), and the nucleus of Darkschewitsch (D); and scattered terminal fibers were seen in the cuneiform nucleus (CNF) and the pars compacta of the anterior pretectal nucleus (PTAc). The projections from the cervical enlargement to PAG, Inc, and the superior colliculus terminated more rostrally than those from the lumbar segments, indicating a somatotopic organization. (2) Terminal labeling after injection of tracer into LCN was found mainly in Inc, SGI, and SGP, but sparse labeling was also observed in the nucleus of the brachium of the inferior colliculus (BIN), PAG, PBN, PTP, and D. (3) The projection from DCN terminated densely in the external and pericentral nuclei of the inferior colliculus (ICX, ICP), Inc, SGI, SGP, PTP, PTAc, the nucleus ruber, and D, and weak terminal labeling was seen in BIN, PAG, and PBN. Comparisons of the anterograde labeling following injections involving both the gracile nucleus and the cuneate nucleus with that after injection restricted to the gracile nucleus alone suggested a somatotopic termination pattern in Inc, the superior colliculus, and the pretectal nuclei. (4) The patterns of projection from the laminar and alaminar parts of the spinal trigeminal nucleus differed: injection of tracer into the caudal part of the alaminar spinal trigeminal nucleus (nucleus interpolaris) resulted in dense anterograde labeling in SGI and SGP, moderate termination in Inc, and minor projections to PBN, PAG, and PTP, whereas after tracer injection into the laminar trigeminal nucleus (nucleus caudalis) terminal labeling was present only in PBN and PAG. Following injection of tracer into the midbrain terminal areas retrogradely labeled neurons were found in the spinal cord, LCN, DCN, and the spinal trigeminal nucleus, with the majority of labeled cells situated on the side contralateral to the injection site.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

Central distribution of primary afferent fibers in the Arnold's nerve (the auricular branch of the vagus nerve): A transganglionic HRP study in the cat

Central projections of the Arnold's nerve (the auricular branch of the vagus nerve; ABV) of the cat were examined by the transganglionic HRP method. After applying HRP to the central cut end of the ABV, HRP-labeled neuronal somata were seen in the superior ganglion of the vagus nerve. Main terminal labeling was seen ipsilaterally in the solitary nucleus, in the lateral portions of the ventral division of the principal sensory trigeminal nucleus, in the marginal regions of the interpolar subnucleus of the spinal trigeminal nucleus, in the marginal and magnocellular zones of the caudal subnucleus of the spinal trigeminal nucleus, in the ventrolateral portions of the cuneate nucleus, and in the dorsal horn of the C1–C3 cord segments. In the solitary nucleus, labeled terminals were seen in the interstitial, dorsal, dorsolateral and commissural subnuclei; some of these terminals may be connected monosynaptically with solitary nucleus neurons which send their axons to the somatomotor and/or visceromotor centers in the brainstem and spinal cord.     

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.     

Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat

The olivocochlear projection constitutes the last stage of the descending auditory system in the mammalian brain. Its neurons reside in the superior olivary complex (SOC) and project to the inner and outer hair cell receptors in the cochlea. Olivocochlear neurons were also reported to send axon collaterals into the cochlear nucleus, but controversies about their number and about species differences persist. By injecting the fluorescent retrograde axonal tracers diamidino yellow and fast blue into the cochlea and the ventral cochlear nucleus (VCN), we studied the distribution and number of olivocochlear neurons with and without axon collaterals into the VCN of the rat. We found that olivocochlear neurons residing in the lateral superior olive (LSO), the intrinsic lateral olivocochlear cells (intrinsic LOCs), do not send axon collaterals into the VCN. By contrast, a majority, and possibly all, olivocochlear neurons residing in the ventral nucleus of the trapezoid body (VNTB), the medial olivocochlear cells (MOCs), do have such axon collaterals. These cells may thus affect processing in the ascending auditory pathway at the level of the receptors and concurrently at the level of the secondary sensory neurons in the cochlear nucleus. Belonging to the lateral olivocochlear system, shell neurons reside around the LSO and form a third group of olivocochlear cells (shell LOCs). Like intrinsic LOCs, they innervate the inner hair cells, but like MOCs they do, by means of axon collaterals, project into the VCN. These findings have implications for understanding both auditory signal processing and the plasticity responses that occur following loss of cochlear function.     

Trigeminal projections to hypoglossal and facial motor nuclei in the rat

This study was undertaken to identify the trigeminal nuclear regions connected to the hypoglossal (XII) and facial (VII) motor nuclei in rats. Anterogradely transported tracers (biotinylated dextran amine, biocytin) were injected into the various subdivisions of the sensory trigeminal complex, and labeled fibers and terminals were searched for in the XII and VII. In a second series of experiments, injections of retrogradely transported tracers (biotinylated dextran amine, gold-horseradish peroxidase complex, fluoro-red, fluoro-green) were made into the XII and the VII, and labeled cells were searched for in the principal sensory trigeminal nucleus, and in the pars oralis, interpolaris, and caudalis of the spinal trigeminal nucleus. Trigeminohypoglossal projections were distributed throughout the ventral and dorsal region of the XII. Neurons projecting to the XII were found in all subdivisions of the sensory trigeminal complex with the greatest concentration in the dorsal part of each spinal subnucleus and exclusively in the dorsal part of the principal nucleus. Trigeminofacial projections reached all subdivisions of the VII, with a gradual decreasing density from lateral to medial cell groups. They mainly originated from the ventral part of the principal nucleus. In the spinal nucleus, most of the neurons projecting to the VII were in the dorsal part of the nucleus, but some were also found in its central and ventral parts. By using retrograde double labeling after injections of different tracers in the XII and VII on the same side, we examined whether neurons in the trigeminal complex project to both motor nuclei. These experiments demonstrate that in the spinal trigeminal nucleus, neurons located in the pars caudalis and pars interpolaris project by axon collaterals to XII and VII. J. Comp. Neurol. 415:91–104, 1999. © 1999 Wiley-Liss, Inc.     

Delayed, frequency-specific inhibition in the cochlear nuclei of mice: a mechanism for monaural echo suppression

To understand how auditory information is processed in the cochlear nuclei, it is crucial to know what circuitry exists and how it functions. Previous anatomical experiments have shown that neurons in the deep layer of the dorsal cochlear nucleus (DCN) project topographically to the anteroventral cochlear nucleus (AVCN) (Wickesberg and Oertel, 1988). Because interneurons in the DCN and their targets in AVCN are excited by the same group of auditory nerve fibers, the projection is frequency-specific. Here we report that microinjections of glutamate in the DCN evoke trains of IPSPs in individual, impaled AVCN neurons in brain slices of the cochlear nuclear complex. Only injections along a rostrocaudal band in the DCN, matching the anatomical projection of tuberculoventral neurons, evoke IPSPs; elsewhere, there were no responses to the glutamate. The inhibition is blocked by 0.5 microM strychnine. Both bushy and stellate cells are targets of the inhibitory projection. Inhibition in the AVCN is delayed by an additional synaptic delay with respect to the excitation. Delayed, frequency-specific inhibition allows the first wavefront to be transmitted to higher auditory centers by bushy and stellate cells, while following inputs encoding signals of similar frequencies are attenuated at least for the duration of an IPSP. These findings are consistent with results from psychoacoustic experiments and suggest that this circuit provides a source of monaural echo suppression.     

Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice

To understand how auditory information is processed in the cochlear nuclei, it is crucial to know what circuitry exists and how it functions. In slice preparations, horseradish peroxidase (HRP) injections into the anteroventral cochlear nucleus (AVCN) reveal two circuits: a connection between the dorsal cochlear nucleus (DCN) and AVCN and a local circuit confined to the AVCN. Extracellular injection in the AVCN labels a band of cells in the DCN. The labeled cells in the DCN lie within a band of auditory nerve fiber terminals that are labeled by the same injection, showing that the connection from the DCN to the AVCN is frequency specific. The injections into the AVCN also labeled a cluster of neurons in the AVCN dorsal to the injection site. These cells may be interneurons that relay information from areas encoding higher frequencies to areas encoding lower frequencies within the AVCN. In the parasagittal plane, the AVCN is organized along two orthogonal axes that are indicated with HRP labeling of fibers and cell bodies. The tonotopic axis runs approximately dorsoventrally; the isofrequency axis runs approximately rostrocaudally. The axons of labeled DCN neurons and the cluster lie along the tonotopic axis, whereas the labeled auditory nerve fibers define the isofrequency axis. Where they cross is where HRP is taken up by the fibers. The area of uptake is small and lies in the middle of the darkly stained injection site.     

Topographic organization of the central projections of the spiral ganglion in cats

The morphological organization of inputs from restricted sectors of the cat cochlear spiral ganglion into the cochlear nucleus was studied by making focal extracellular injections of horseradish peroxidase (HRP) into the spiral ganglion. Injections resulted in Golgi-like labeling of a small cluster of spiral ganglion cells and their peripheral and central axons. Large injections involved most of the cells within Rosenthal's canal in sectors of the spiral ganglion innervating greater than or equal to 1 mm of the basilar membrane and resulted in narrow, complete laminae of labeled axons and preterminal fields within each cochlear nucleus subdivision. The positions of these bands were consistent with the "isofrequency laminae" appropriate for the frequencies represented at the injection sites, with high frequency laminae situated more dorsally, and lower frequencies progressively more ventral. A discrete projection to the small cell cap area was observed that was discontinuous with the main projection laminae in the ventral cochlear nuclei (VCN). In the dorsal cochlear nucleus, projecting fibers and terminals were excluded from the molecular cell layer. No labeled fibers entered the granule cell areas. In contrast to larger injections, very small HRP deposits labeled only part of an isofrequency lamina. Specifically, injections restricted to the scala tympani aspect of the spiral ganglion labeled only the lateral part of VCN isofrequency laminae, whereas injections limited to the scala vestibuli aspect of the ganglion labeled the medial aspect of the isofrequency planes. Thus these data indicate a previously unrecognized topographic representation of the vertical dimension of the spiral ganglion across VCN isofrequency laminae. Some possible functional implications of this projection organization are discussed.