Kevin A. Davis

Circuitry and Function of the Dorsal Cochlear Nucleus

In Chapter 2 of this volume, Smith and Spirou describe the wonderful complexity of the brainstem auditory system. This system forms a collection of parallel pathways that diverge at the first auditory synapse in the brainstem, in the cochlear nucleus (CN), and then converge again, at least in a gross anatomical sense, in the inferior colliculus (for abbreviations, see Table 5.1). The CN is a well-studied collection of neural circuits that are diverse both in anatomical and physiological terms (reviewed by Cant 1992; Rhode and Greenberg 1992; Young 1998). These vary from the simplest system, the bushy cells of the ventral cochlear nucleus (VCN; see Yin, Chapter 4), to the most complex, in the dorsal cochlear nucleus (DCN). The DCN differs from other parts of the CN by having an extensive internal neuropil formed by groups of interneurons (Lorente de No 1981; Osen et al. 1990). As a result, the DCN makes significant changes in the auditory representation from its inputs to its outputs. In this chapter, the neural organization of the DCN is reviewed, paying most attention to data from the cat. The response properties of DCN neurons are discussed in the context of its neural organization and related to data on the functional role of the DCN in hearing.

Auditory Processing of Spectral Cues for Sound Localization in the Inferior Colliculus

The head-related transfer function (HRTF) of the cat adds directionally dependent energy minima to the amplitude spectrum of complex sounds. These spectral notches are a principal cue for the localization of sound source elevation. Physiological evidence suggests that the dorsal cochlear nucleus (DCN) plays a critical role in the brainstem processing of this directional feature. Type O units in the central nucleus of the inferior colliculus (ICC) are a primary target of ascending DCN projections and, therefore, may represent midbrain specializations for the auditory processing of spectral cues for sound localization. Behavioral studies confirm a loss of sound orientation accuracy when DCN projections to the inferior colliculus are surgically lesioned. This study used simple analogs of HRTF notches to characterize single-unit response patterns in the ICC of decerebrate cats that may contribute to the directional sensitivity of the brains spectral processing pathways. Manipulations of notch frequency and bandwidth demonstrated frequency-specific excitatory responses that have the capacity to encode HRTF-based cues for sound source location. These response patterns were limited to type O units in the ICC and have not been observed for the projection neurons of the DCN. The unique spectral integration properties of type O units suggest that DCN influences are transformed into a more selective representation of sound source location by a local convergence of wideband excitatory and frequency-tuned inhibitory inputs.

Somatosensory context alters auditory responses in the cochlear nucleus

The cochlear nucleus, the first central auditory structure, performs initial stimulus processing and segregation of information into parallel ascending pathways. It also receives nonauditory inputs. Here we show in vivo that responses of dorsal cochlear nucleus (DCN) principal neurons to sounds can change significantly depending on the presence or absence of inputs from the somatosensory dorsal column nucleus occurring before the onset of auditory stimuli. The effects range from short-term suppression of spikes lasting a few milliseconds at the onset of the stimulus to long-term increases or decreases in spike rate that last throughout the duration of an acoustic stimulus (up to several hundred milliseconds). The long-term effect requires only a single electrical stimulus pulse to initiate and seems to be similar to persistent activity reported in other parts of the brain. Among the DCN inhibitory interneurons, only the cartwheel cells show a long-term rate decrease that could account for the rate increases (but not the decreases) of DCN principal cells. Thus even at the earliest stages of auditory processing, the represented information is dependent on nonauditory context, in this case somatosensory events.

Contralateral effects and binaural interactions in dorsal cochlear nucleus.

The dorsal cochlear nucleus (DCN) receives afferent input from the auditory nerve and is thus usually thought of as a monaural nucleus, but it also receives inputs from the contralateral cochlear nucleus as well as descending projections from binaural nuclei. Evidence suggests that some of these commissural and efferent projections are excitatory, whereas others are inhibitory. The goals of this study were to investigate the nature and effects of these inputs in the DCN by measuring DCN principal cell (type IV unit) responses to a variety of contralateral monaural and binaural stimuli. As expected, the results of contralateral stimulation demonstrate a mixture of excitatory and inhibitory influences, although inhibitory effects predominate. Most type IV units are weakly, if at all, inhibited by tones but are strongly inhibited by broadband noise (BBN). The inhibition evoked by BBN is also low threshold and short latency. This inhibition is abolished and excitation is revealed when strychnine, a glycine-receptor antagonist, is applied to the DCN; application of bicuculline, a GABAA-receptor antagonist, has similar effects but does not block the onset of inhibition. Manipulations of discrete fiber bundles suggest that the inhibitory, but not excitatory, inputs to DCN principal cells enter the DCN via its output pathway, and that the short latency inhibition is carried by commissural axons. Consistent with their respective monaural effects, responses to binaural tones as a function of interaural level difference are essentially the same as responses to ipsilateral tones, whereas binaural BBN responses decrease with increasing contralateral level. In comparison to monaural responses, binaural responses to virtual space stimuli show enhanced sensitivity to the elevation of a sound source in ipsilateral space but reduced sensitivity in contralateral space. These results show that the contralateral inputs to the DCN are functionally relevant in natural listening conditions, and that one role of these inputs is to enhance DCN processing of spectral sound localization cues produced by the pinna.

Rate representation of tones in noise in the inferior colliculus of decerebrate cats

Neurons in the central nucleus of the inferior colliculus (ICC) of decerebrate cats show three major response patterns when tones of different frequencies and sound-pressure levels (SPLs) are presented to the contralateral ear. The frequency response maps of type I units are uniquely defined by a narrow excitatory area at best frequency (BF: a units most sensitive frequency) and surrounding inhibition at higher and lower frequencies. As a result of this receptive field organization, type I units exhibit strong excitatory responses to BF tones but respond only weakly to broadband noise (BBN). These response characteristics predict that type I units are well suited to encode narrowband signals in the presence of background noise. To test this hypothesis, the dynamic range properties of ICC unit types were measured under quiet conditions and in multiple levels of continuous noise. As observed in previous studies of the auditory nerve and cochlear nucleus, type I units showed upward threshold shifts and discharge rate compression in background noise that partially degraded the dynamic range properties of neural representations at high noise levels. Although the other two unit types in the ICC showed similar trends in threshold shift and noise compression, their ability to encode auditory signals was compromised more severely in increasing noise levels. When binaural masking effects were simulated, only type I units showed an enhanced representation of spatially separated signals and maskers that was consistent with human perceptual performance in independent psychoacoustic observations. These results support the interpretation that type I units play an important role in the auditory processing of narrowband signals in background noise and suggest a physiological basis for spatial factors that govern signal detection under free-field listening conditions.

Modeling inhibition of type II units in the dorsal cochlear nucleus.

Abstract. Type II units in the dorsal cochlear nucleus (DCN) are characterized by vigorous but nonmonotonic responses to best frequency tones as a function of sound pressure level, and relatively weak responses to noise. A model of DCN neural circuitry was used to explore two hypothetical mechanisms by which neurons may be endowed with type II unit response properties. Both mechanisms assume that type II units receive excitatory input from auditory nerve (AN) fibers and inhibitory input from an unspecified class of cochlear nucleus interneurons that also receive excitatory AN input. The first mechanism, a lateral inhibition (LI) model, supposes that type II units receive inhibitory input from a number of narrowly tuned interneurons whose best frequencies (BFs) flank the BF of the type II unit. Tonal stimuli near BF result in only weak inhibitory input, but broadband stimuli recruit enough lateral inhibitors to greatly weaken the type II unit response. The second mechanism, a wideband inhibition (WBI) model, supposes that type II units receive inhibitory input from interneurons that are broadly tuned so that they respond more vigorously to broadband stimuli than to tones. Physiological and anatomical evidence points to the possible existence of such a class of neurons in the cochlear nucleus. The model extends an earlier computer model of an iso-frequency DCN patch to multiple frequency slices and adds a population of interneurons to provide the inhibition to model type II units (called I2-cells). The results show that both mechanisms accurately simulate responses of type II units to tones and noise. An experimental paradigm for distinguishing the two mechanisms is proposed.

Spectral processing in the inferior colliculus.

Publisher Summary This chapter reviews the anatomy of a mammalian. The frequency response areas of inferior colliculus (ICC) units are described, followed by the roles of the various excitatory and inhibitory inputs to the ICC in shaping these response areas. The functional roles of the ICC in the processing of spectral information are discussed. The central nucleus of the inferior colliculus (ICC) occupies a pivotal position in the central auditory system; it receives converging projections from most, if not all, of the auditory nuclei in the brainstem and, in turn, provides nearly all of the input to the auditory forebrain. Some of the ascending projections to the ICC are excitatory (e.g., cochlear nucleus, superior olive), whereas others are inhibitory. Moreover, the inhibitory projections are both GABAergic and glycinergic. The manner in which these inputs combine creates functionally distinct synaptic domains within the ICC and presumably basic differences in ICC frequency response areas.

A statistically based method to generate response maps objectively

One scheme to classify the physiological response properties of single units in the cochlear nucleus is based on the average discharge rate of the unit and is reflected in the distribution of excitatory and inhibitory regions in a frequency-level map (response map) that spans the units receptive area (e.g., Evans and Nelson, 1973; Young and Brownell, 1976; Young and Voigt, 1982; Shofner and Young, 1985, Spirou and Young, 1991). Typically, discharge rate versus level curves are acquired at many frequencies and the investigator determines that a unit is excited or inhibited at a given level if the driven rate is above or below a spontaneous rate estimate by a specified criterion (for example, 20%). The investigator then encloses regions of excitation and inhibition where responses over adjacent frequencies and levels are consistent. In the present report, we describe an objective 3-step computer-based method to generate response maps: raw driven and spontaneous rate estimates are smoothed with a low-pass spatial filter; a unit is said to be excited or inhibited at a given level if the filtered driven rate is above or below the mean filtered spontaneous rate for that frequency by a specified criterion (percentage or statistical); and resultant response maps are median spatial filtered to eliminate spurious regions. The results shown here demonstrate that use of a statistical criterion provides a more reliable detection of excitation and inhibition than a 20% criterion, particularly when the variance of the rate estimates is high. Further, the statistically based method permits unit classification based on response map data that are more rapidly acquired with shorter duration stimuli (32 vs. 200 ms). Although this method is applied to units recorded in the dorsal cochlear nucleus, the technique may be applicable to studies of receptive fields and their plasticity in other systems.

Respiratory impedance spectral estimation for digitally created random noise.

Measurement of respiratory input mechanical impedance (Zrs) is noninvasive, requires minimal subject cooperation, and contains information related to mechanical lung function. A common approach to measure Zrs is to apply random noise pressure signals at the airway opening, measure the resulting flow variations, and then estimate Zrs using Fast-Fourier Transform (FFT) techniques. The goal of this study was to quantify how several signal processing issues affect the quality of a Zrs spectral estimate when the input pressure sequence is created digitally. Random noise driven pressure and flow time domain data were simulated for three models, which permitted predictions of Zrs characteristics previously reported from 0–4, 4–32, and 4–200 Hz. Then, the quality of the Zrs estimate was evaluated as a function of the number of runs ensemble averaged, windowing, flow signal-to-noise ratio (SNR), and pressure spectral magnitude shape |P(jω)|. For a |P(jω)| with uniform power distribution and a SNR<100, the 0–4 Hz and 4–200 Hz Zrs estimates for 10 runs were poor (minimum coherence γ2<0.75) particularly where Zrs is high. When the SNR>200 and 10 runs were averaged, the minimum γ2 >0.95. However, when |P(jω)| was matched to |Zrs|, γ2 > 0.91 even for 5 runs and a SNR of 20. For data created digitally with equally spaced spectral content, the rectangular window was superior to the Hanning. Finally, coherence alone may not be a reliable measure of Zrs quality because coherence is only an estimate itself. We conclude that an accurate estimate of Zrs is best obtained by matching |P(jω)| to |Zin| (subject and speaker) and using rectangular windowing.

Neural modeling of the dorsal cochlear nucleus: cross-correlation analysis of short-duration tone-burst responses

A conceptual model of a portion of dorsal cochlear nucleus (DCN) neural circuitry has emerged over the past two decades. This model suggests that the response properties of the DCNs major projection neurons, called type IV units, are due, in part, to the behavior of local circuit inhibitory interneurons called type II units (Young and Brownell 1976). Cross-correlation studies of simultaneously recorded pairs of DCN units in decerebrate cat derived from 50-s best frequency (BF) stimuli are consistent with and have extended this conceptual model (Voigt and Young 1980, 1985, 1988, 1990). Interestingly, Gochin et al. (1989) found no signs of inhibition in the anesthetized rat DCN in cross-correlograms derived from 55-ms short-duration BF tone bursts. This seemingly contradictory result has motivated this study. Computer simulations were run using our network model of the intrinsic DCN neural circuitry. This model has previously been shown to reproduce the major features of both type II and type IV rate-level curves and the inhibitory trough (IT) observed in cross-correlograms derived from long-duration stimuli (Voigt and Davis 1994). The goal was to study the stimulusduration-dependent strength of ITs in the cross-correlograms derived from short-duration BF tone-burst stimuli. The results suggest that ITs may not be detectable when the stimulus duration is 50 ms but may be detectable when the stimulus duration is 200 ms or greater. Furthermore, when the ITs are detected in cross-correlograms derived from 200-ms data sets, the strength of the IT, as measured by effectiveness, is comparable to the strength of ITs measured when the stimulus duration is 50 s.