No abstract

The present study examined the morphological cell types of neurons labeled with intracellular horseradish peroxidase injections, many of them following electrophysiological recordings in the cochlear nucleus of gerbils and chinchillas. Most of the subdivisions and neuronal types previously described in the cat were identified in the present material, including spherical and globular bushy cells, stellate, bushy multipolar, elongate, octopus, and giant cells in the ventral cochlear nucleus, and a cartwheel cell in the dorsal cochlear nucleus. In many cases these structurally distinct neurons were correlated with their characteristic responses to stimulation by sound or intracellular injection of depolarizing current. The dendritic terminals of the elongate, antenniform, and clavate cells of the posteroventral cochlear nucleus link each of these cell types with neighboring structures in distinct patterns, which may provide a basis for differences in synaptic organization. These cell types differ from each other and from the stellate cells of the anteroventral cochlear nucleus. Despite their heterogeneous morphology, most of these neurons had a regular discharge in response to stimulation (choppers). Irregularly firing neurons (primary-like) had very different structures, e.g., the spherical and globular bushy cells and the bushy multipolar neuron. They, too, represent a heterogeneous population. An onset neuron was identified as an octopus cell. This paper compares the morphological observations with the electrophysiological properties of different cell types reported in a companion paper (Feng et al. [1994] J. Comp. Neurol.). Together, these findings imply that response properties may be partially independent of neuronal structure. Morphologically distinct neurons can generate similar temporal patterns in response to simple acoustic stimuli. Nevertheless, the synaptic organization of these different neuron types, including their connections, would be expected to affect or alter the cells' responses to appropriate stimuli. The possibility is raised that membrane properties and synaptic organization complement and interact with each other.

Retrograde transport of horseradish peroxidase was combined with immunocytochemistry to identify the origins of potential gamma-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.

Neurons in the cochlear nucleus differ in their discharge patterns when stimulated by tones. They also differ in their responses to depolarizing current injection in vitro. We made intracellular recordings from neurons in the cochlear nucleus of gerbils and chinchillas. The responses to tones and to depolarizing current were compared for the same neurons. Three categories of response patterns to tones were observed: chopper, primary-like, and onset. Chopper neurons responded with regularly spaced action potentials to stimulation with tones and to injections of depolarizing current. Their response rate rose with increasing levels of current to a maximum, which was comparable to that evoked by suprathreshold tones. These observations suggest that the regularity and maximal firing rate of these neurons are determined by voltage-dependent membrane properties. Primary-like neurons responded with irregularly spaced action potentials to tones. Injection of depolarizing current into these neurons produced a single action potential at current onset, which could be followed by a few irregularly spaced action potentials. The response rate showed little relation to current level. These data suggest that the membrane characteristics of primary-like neurons are different from those of chopper neurons. Onset neurons produced action potentials only at the beginning of the stimulus for both tones and depolarizing current, even though there was a sustained depolarization throughout the duration of the tone. The findings suggest that cochlear nucleus neurons have different membrane properties and that these properties may play a critical role in a neuron's temporal response pattern to acoustic stimulation.

The synaptic organization of globular bushy cells of the anteroventral cochlear nucleus was quantitatively analyzed in order to understand better their functional attributes. A method was devised to estimate the concentrations and relative proportions of synapses on the entire postsynaptic surface of Golgi-impregnated neurons, by sampling with limited series of sections for electron microscopy. This provided a characteristic synaptic profile which was homogeneous for the population measured. The total concentration of synaptic endings decreases with distance from the soma. The cochlear, presumably glutamatergic and excitatory, endings with large spherical vesicles (LS) account for most of this decrease. Of the noncochlear inputs, the putative glycinergic endings with flattened vesicles (FL) decrease slightly, and the presumed GABAergic terminals with pleomorphic vesicles (PL) maintain a relatively constant concentration, while endings with small spherical vesicles (SS) increase on the distal dendrites. LS endings have the largest proportion of synapses near the soma, while FL synapses maintain a constant proportion in all cell regions, and PL and SS proportions increase on higher-order dendrites. Excitatory and inhibitory synapses have significant inputs to the axon hillock and initial segment, as well as to the distal dendrites, where dual synapses may provide a way to sample the activity of surrounding neurons. These features must be considered in explanations of physiological properties, such as the synaptic security, level of spontaneous activity, and well-timed, rapid onset responses, as well as their potential for normalizing and synchronizing an important inhibitory pathway involved in binaural signal processing. Synaptic profile analysis should be useful for experimental studies and for developing realistic computational models.