Local circuit interactions between the dorsal and ventral divisions of the cochlear nucleus are known to influence the evoked responses of the resident neurons to sound. In the present study, we examined the projections of neurons in the ventral cochlear nucleus to the dorsal cochlear nucleus by using retrograde transport of biotinylated dextran amine injected into restricted but different regions of the dorsal cochlear nucleus. In all cases, we found retrogradely labeled granule, unipolar brush, and chestnut cells in the granule cell domain, and retrogradely labeled multipolar cells in the magnocellular core of the ventral cochlear nucleus. A small number of the labeled multipolar cells were found along the margins of the ventral cochlear nucleus, usually near the boundaries of the granule cell domain. Spherical bushy, globular bushy, and octopus cells were not labeled. Retrogradely-labeled auditory nerve fibers and the majority of labeled multipolar neurons formed a narrow sheet extending across the medial-to-lateral extent of the ventral cochlear nucleus whose dorsoventral position was topographically related to the injection site. Labeled multipolar cells within the core of the ventral cochlear nucleus could be divided into at least two distinct groups. Planar neurons were most numerous, their somata found within the associated band of labeled fibers, and their dendrites oriented within this band. This arrangement mimics the organization of isofrequency contours and implies that planar neurons respond best to a narrow range of frequencies. In contrast, radiate neurons were infrequent, found scattered throughout the ventral cochlear nucleus, and had long dendrites oriented perpendicular to the isofrequency contours. This dendritic orientation suggests that radiate neurons are sensitive to a broad range of frequencies. These structural differences between planar and radiate neurons suggest that they subserve separate functions in acoustic processing.
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.
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.
Cortical area Te1 in the rat commonly is associated with primary auditory cortex. It is the source of direct projections to the inferior colliculus (IC), superior olivary complex (SOC), and the cochlear nucleus (CN). A question that arises is whether these descending pathways derive from a common source or separate populations of cortical neurons. We addressed this question in seven rats by injecting either Diamidino yellow (DiY) or Fast blue (FB) into the IC and injecting the other tracer into the CN (n=4) or SOC (n=3). All injections were made on the left side of the brain. In a sample of sections through area Te1 in both hemispheres, we counted single- and double-labeled cells. We estimate that IC-projecting cells outnumber those projecting to the CN or SOC by at least a factor of ten. The source of corticofugal pathways to the left IC was heavily biased towards the same side of the brain (ipsi/contra ratio 8 +/- 2.5), whereas it was more equally distributed between the two hemispheres for the left CN and SOC (ipsi/contra ratios ranged from 0.7-2.3). Finally, we observed that only 10-20% of those cells filled with a tracer injection in the CN or SOC also contained the tracer injected into the IC. In a previous study, we observed a similarly small percentage of double labeled cells when FB and DiY were injected into the CN and SOC, respectively. Combined with the distinct laminar distribution of IC-, SOC-, and CN-projecting neurons within layer V, the results suggest that these three pathways largely derive from different populations of cortical neurons.
There is growing evidence that hearing involves the integration of many brain functions, including vision, balance, somatic sensation, learning and memory, and emotional state. Some of these integrative processes begin at the earliest stages of the central auditory system. In this review, we will discuss evidence that reveals multimodal projections into the granule cell domain of the cochlear nucleus.
Multipolar cells in the ventral cochlear nucleus (VCN) are a structurally and functionally diverse group of projection neurons. Understanding their role in the ascending pathway involves partitioning multipolar cells into distinct populations and determining where in the brain each sends its coded messages. In this study, we used retrograde labeling techniques in rats to identify multipolar neurons that project their axons to the ipsilateral dorsal cochlear nucleus (DCN), the contralateral CN, or both structures. Three rats received injections of biotinylated dextran amine in the ipsilateral DCN and diamidino yellow in the contralateral CN. Several radiate multipolar neurons (defined by their axonal projections to the ipsilateral DCN and their dendrites that traverse VCN isofrequency sheets) were double-labeled but over 70% were not. This result suggests two distinct populations: (1) radiate-commissural (RC) multipolar cells that project to the ipsilateral DCN and the contralateral CN, and (2) radiate multipolar cells that project exclusively (in this context) to the ipsilateral DCN. In a different group of animals, we retrogradely labeled multipolar neurons that project their axons to the contralateral CN and measured the size of their cell bodies. The mean size of this population (266 Ϯ 156 m 2 ) was significantly smaller than those of RC-multipolar cells (418 Ϯ 140 m 2 ). We conclude that the CN commissural pathway is composed of at least two components: (1) RC multipolar cells and (2) commissural multipolar cells that are small-and medium-sized neurons that project exclusively (in this context) to the contralateral CN. These results identify separate structural groups of multipolar cells that may correspond to physiological unit types described in the literature. They also provide protocols for isolating and studying different populations of multipolar cells to determine the neural mechanisms that govern their responses to sound. Anat Rec Part 288A:331-344, 2006. Key words: hearing; ascending pathways; classifying neurons; naming neuronsInformation about sound is conveyed to the brain by patterns of action potentials in the auditory nerve. These patterns are analyzed first by neurons in the cochlear nucleus (CN) that are the source of all ascending pathways in the central auditory system. An important step toward understanding the neural circuits that underlie hearing is to define how CN neurons divide, select, and encode the enormous amount of acoustic information that they receive.Dendritic morphology can be used to partition ventral cochlear nucleus (VCN) projection neurons into three groups: bushy, multipolar, and octopus. Octopus cells are located in the caudal pole of the VCN and they are distinguished by several long dendrites that extend from one side of the cell body. Bushy cells usually have one or two primary dendrites. Shortly after arising from the soma, each primary dendrite ends in a spray of thinner and
Certain distinct populations of neurons in the dorsal cochlear nucleus are inhibited by a neural source that is responsive to a wide range of acoustic frequencies. In this study, we examined the glycine immunoreactivity of two types of ventral cochlear nucleus neurons (planar and radiate) in the rat which project to the dorsal cochlear nucleus (DCN) and thus, might be responsible for this inhibition. Previously, we proposed that planar neurons provided a tonotopic and narrowly tuned input to the DCN, whereas radiate neurons provided a broadly tuned input and thus, were strong candidates as the source of broadband inhibition (Doucet and Ryugo [1997] J. Comp. Neurol. 385:245-264). We tested this idea by combining retrograde labeling and glycine immunohistochemical protocols. Planar and radiate neurons were first retrogradely labeled by injecting biotinylated dextran amine into a restricted region of the dorsal cochlear nucleus. The labeled cells were visualized using streptavidin conjugated to indocarbocyanine (Cy3), a fluorescent marker. Sections that contained planar or radiate neurons were then processed for glycine immunocytochemistry using diaminobenzidine as the chromogen. Immunostaining of planar neurons was light, comparable to that of excitatory neurons (pyramidal neurons in the DCN), whereas immunostaining of radiate neurons was dark, comparable to that of glycinergic neurons (cartwheel cells in the dorsal cochlear nucleus and principal cells in the medial nucleus of the trapezoid body). These results are consistent with the hypothesis that radiate neurons in the ventral cochlear nucleus subserve the wideband inhibition observed in the dorsal cochlear nucleus.
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