Neuronal organization of the cochlear nuclei in alligator lizards: a light and electron microscopic investigation.

The organization of neurons and fibers in the cochlear nuclei of the alligator lizard (Gerrhonotus multicarinatus) was examined with light and electron microscopy. In this species, much is known about the anatomy and physiology of the inner ear including the cochlear nerve, but little is known about the synaptic connections of cochlear fibers on second-order neurons. These data will help to develop general principles addressing the cellular organization of the vertebrate auditory system. Subdivisions of the cochlear nuclei were defined on the basis of their histologic appearance and neuronal composition. Neuron classes were proposed from their light microscopic and ultrastructural features. Nucleus magnocellularis medialis consists of a homogeneous population of neurons called "lesser ovoid" cells. Nucleus magnocellularis lateralis consists of "greater ovoid" and "small" cells. Nucleus angularis lateralis consists of "spindle" cells. Lastly, nucleus angularis medialis contains a population of large neurons called "duckhead" and "multipolar" cells, and a population of smaller neurons called "bulb" and "agranular" cells. These neuron populations are differentially innervated by tectorial and free-standing cochlear fibers that are associated with separate frequency ranges. All neuronal populations except agranular cells were observed to receive synaptic input from cochlear nerve fibers. In nucleus magnocellularis medialis and nucleus angularis medialis, primary afferents form both chemical and electrical synapses with resident neurons. These observations imply that acoustic information is synaptically processed in fundamentally distinct ways in the cochlear nuclei of alligator lizards and distributed along separate neural circuits. Thus, the characteristic structural and functional dichotomy of the alligator lizard inner ear is extended to central auditory pathways by way of cochlear nerve projections.

Central projections of cochlear nerve fibers in the alligator lizard.

The auditory (cochlear) ganglion cells of the alligator lizard (Gerrhonotus multicarinatus) give rise to two types of peripheral fibers: tectorial fibers, which contact hair cells covered by a tectorial membrane, and free-standing fibers, which contact hair cells without a tectorial membrane. To determine the central projections of these fibers, we applied intracellular and extracellular injections of horseradish peroxidase (HRP) to the peripheral component of the cochlear nerve. After histological processing with diaminobenzidine, individual cochlear nerve fibers could be traced through serial sections with the aid of a light microscope and drawing tube. The projection patterns formed two morphologically distinct groups. Neurons whose peripheral processes contacted tectorial hair cells in the cochlea projected to three divisions of the cochlear nucleus: nucleus magnocellularis lateralis (NML), nucleus magnocellularis medialis (NMM), and nucleus angularis lateralis (NAL). Neurons whose peripheral processes contacted free-standing hair cells projected primarily to the nucleus angularis medialis (NAM), although some also sent a single, thin branch to the NML; these neurons never projected to NAL or NMM. Morphometric comparisons of tectorial and free-standing fibers demonstrate that tectorial fibers have a larger axonal diameter, form a greater number of terminal swellings, and make proportionally more somatic contacts. By correlating the morphologically defined groups with previously reported physiologically defined groups, we conclude that different divisions of the cochlear nucleus are associated with separate frequency ranges and that stimuli in the different frequency ranges may be processed separately in the brain.