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.

Glycine immunoreactivity of multipolar neurons in the ventral cochlear nucleus which project to the dorsal cochlear nucleus.

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.

Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats.

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.

Neural contributions to the perstimulus compound action potential: implications for measuring the growth of the auditory nerve spike count as a function of stimulus intensity.

The perstimulus compound action potential (PCAP), unlike the more familiar compound action potential (CAP), can be recorded in response to asynchronous as well as synchronous auditory nerve activity. When all neurons contribute equally to the PCAP, the area under the PCAP (the PCAP area) is proportional to the number of action potentials fired by auditory nerve neurons (the auditory nerve spike count). The auditory nerve spike count is one proposed code for stimulus intensity, and our goal is to use the PCAP to test this hypothesis. In this study, two independent tests were developed to measure the contributions of neurons to the PCAP as a function of their characteristic frequency (CF). The test results were verified using a model of the auditory periphery designed to calculate the auditory nerve spike count as a function of pure tone intensity and frequency. In nearly all experiments, neurons having CFs that span contiguous three or four octave bands contribute equally to the PCAP. For pure tones that stimulate only those neurons contributing equally to the PCAP, the PCAP area grows over intensity ranges frequently exceeding 80 dB, and in one case equaling 108 dB. These results demonstrate that the auditory nerve spike count, at least for pure tones, is capable of encoding changes in stimulus intensity over the entire dynamic range of the auditory system.

Is loudness simply proportional to the auditory nerve spike count?

It is often asserted that the physiological correlate of loudness is the simple sum of the spike activity produced by all neurons in the auditory nerve (the auditory nerve spike count). We will refer to this hypothesis as the spike count hypothesis. The spike count hypothesis has been tested in the past using models of the auditory periphery and in almost all cases, the hypothesis has been supported. Our new technique for recording a compound potential from the chinchilla auditory nerve, the perstimulus compound action potential (PCAP), makes possible the measurement of the growth of the auditory nerve spike count, thus providing data that can be used to test the spike count hypothesis empirically. It was observed that the growth of the auditory nerve spike count in response to a 1-kHz pure tone (in dB/dB) is 33% shallower than the growth of loudness for a 1-kHz tone, and this discrepancy increases to 66% for an 8-kHz tone. In addition, "equal-count" contours were constructed in a manner analogous to equal-loudness contours. It was found that as reference intensity increases, equal-count contours become sharply curved upward at high frequencies whereas equal-loudness contours become increasingly flat. These differences are unlikely to be the result of the cross-species comparison, since the discrepancies are mostly attributable to the skewed pattern of spread of excitation along the basilar membrane, a property shared by humans and chinchillas. Therefore, we conclude that the simple sum of the spike activity in the auditory nerve cannot be the physiological correlate of loudness.

Recovery of the compound action potential following prior stimulation: evidence for a slow component that reflects recovery of low spontaneous-rate auditory neurons.

Relkin and Doucet (1991) have shown that recovery of single auditory-nerve neurons from the effects of prior stimulation by a 100 ms pure tone varies with the spontaneous activity of the neuron. Recovery of thresholds for low spontaneous-rate (SR) neurons takes up to 2.0 s, a factor of 10 times greater than the 200 ms required for recovery of high SR neurons. The purpose of this study was to see if the different recovery rates for the two classes of neurons is reflected in recovery of the amplitude of the compound and potential (CAP) recorded in response to a brief probe tone with similar prior stimulation. We present evidence for two components in the recovery of the CAP amplitude, a slow and fast component, that have time courses similar to those for the recovery of responses for single low and high SR neurons, respectively. Thus, we conclude that the recovery of the CAP amplitude does indeed reflect the underlying recovery processes of single auditory-nerve neurons.

Recovery from prior stimulation. I: Relationship to spontaneous firing rates of primary auditory neurons.

Recovery of neural thresholds following a forward masker was measured for auditory neurons in anesthetized chinchillas. We find that recovery of forward-masked thresholds is slower for low spontaneous-rate neurons compared to high spontaneous-rate neurons. In addition, we studied the dependence of the shape of PST histograms on the time between repetitions of a tone-burst. We find that for low spontaneous-rate neurons, peak onset responses increase in magnitude over a longer range of interstimulus intervals compared to high spontaneous-rate neurons. Both results are consistent with the conclusion that low spontaneous-rate neurons take longer to recover from prior stimulation compared to high spontaneous-rate neurons. We suggest applications of this finding in psychophysical experiments to investigate the role of low spontaneous-rate neurons in intensity coding.