Azimuth and envelope coding in the inferior colliculus of the unanesthetized rabbit: effect of reverberation and distance

Recognition and localization of a sound are the major functions of the auditory system. In real situations, the listener and different degrees of reverberation transform the signal between the source and the ears. The present study was designed to provide these transformations and examine their influence on neural responses. Using the virtual auditory space (VAS) method to create anechoic and moderately and highly reverberant environments, we found the following: 1) In reverberation, azimuth tuning was somewhat degraded with distance whereas the direction of azimuth tuning remained unchanged. These features remained unchanged in the anechoic condition. 2) In reverberation, azimuth tuning and envelope synchrony were degraded most for neurons with low best frequencies and least for neurons with high best frequencies. 3) More neurons showed envelope synchrony to binaural than to monaural stimulation in both anechoic and reverberant environments. 4) The percentage of envelope-coding neurons and their synchrony decreased in reverberation with distance, whereas it remained constant in the anechoic condition. 5) At far distances, for both binaural and monaural stimulation, the neural gain in reverberation could be as high as 30 dB and as much as 10 dB higher than those in the anechoic condition. 6) The majority of neurons were able to code both envelope and azimuth in all of the environments. This study provides a foundation for understanding the neural coding of azimuth and envelope synchrony at different distances in reverberant and anechoic environments. This is necessary to understand how the auditory system processes “where” and “what” information in real environments.

Dual sensitivity of inferior colliculus neurons to ITD in the envelopes of high-frequency sounds: experimental and modeling study

Human listeners are sensitive to interaural time differences (ITDs) in the envelopes of sounds, which can serve as a cue for sound localization. Many high-frequency neurons in the mammalian inferior colliculus (IC) are sensitive to envelope-ITDs of sinusoidally amplitude-modulated (SAM) sounds. Typically, envelope-ITD-sensitive IC neurons exhibit either peak-type sensitivity, discharging maximally at the same delay across frequencies, or trough-type sensitivity, discharging minimally at the same delay across frequencies, consistent with responses observed at the primary site of binaural interaction in the medial and lateral superior olives (MSO and LSO), respectively. However, some high-frequency IC neurons exhibit dual types of envelope-ITD sensitivity in their responses to SAM tones, that is, they exhibit peak-type sensitivity at some modulation frequencies and trough-type sensitivity at other frequencies. Here we show that high-frequency IC neurons in the unanesthetized rabbit can also exhibit dual types of envelope-ITD sensitivity in their responses to SAM noise. Such complex responses to SAM stimuli could be achieved by convergent inputs from MSO and LSO onto single IC neurons. We test this hypothesis by implementing a physiologically explicit, computational model of the binaural pathway. Specifically, we examined envelope-ITD sensitivity of a simple model IC neuron that receives convergent inputs from MSO and LSO model neurons. We show that dual envelope-ITD sensitivity emerges in the IC when convergent MSO and LSO inputs are differentially tuned for modulation frequency.

Spatial tuning to sound-source azimuth in the inferior colliculus of unanesthetized rabbit

Despite decades of research devoted to the study of inferior colliculus (IC) neurons' tuning to sound-source azimuth, there remain many unanswered questions because no previous study has examined azimuth tuning over a full range of 360° azimuths at a wide range of stimulus levels in an unanesthetized preparation. Furthermore, a comparison of azimuth tuning to binaural and contralateral ear stimulation over ranges of full azimuths and widely varying stimulus levels has not previously been reported. To fill this void, we have conducted a study of azimuth tuning in the IC of the unanesthetized rabbit over a 300° range of azimuths at stimulus levels of 10–50 dB above neural threshold to both binaural and contralateral ear stimulation using virtual auditory space stimuli. This study provides systematic evidence for neural coding of azimuth. We found the following: 1) level-tolerant azimuth tuning was observed in the top 35% regarding vector strength and in the top 15% regarding vector angle of IC neurons; 2) preserved azimuth tuning to binaural stimulation at high stimulus levels was created as a consequence of binaural facilitation in the contralateral sound field and binaural suppression in the ipsilateral sound field; 3) the direction of azimuth tuning to binaural stimulation was primarily in the contralateral sound field, and its center shifted laterally toward −90° with increasing stimulus level; 4) at 10 dB, azimuth tuning to binaural and contralateral stimulation was similar, indicating that it was mediated by monaural mechanisms; and 5) at higher stimulus levels, azimuth tuning to contralateral ear stimulation was severely degraded. These findings form a foundation for understanding neural mechanisms of localizing sound-source azimuth.

Sensitivity to Interaural Time Differences in the Dorsal Nucleus of the Lateral Lemniscus of the Unanesthetized Rabbit: Comparison With Other Structures

Interaural time differences, a cue for azimuthal sound location, are first encoded in the superior olivary complex (SOC), and this information is then conveyed to the dorsal nucleus of the lateral lemniscus (DNLL) and inferior colliculus (IC). The DNLL provides a strong inhibitory input to the IC and may serve to transform the coding of interaural time differences (ITDs) in the IC. Consistent with the projections from the SOC, the DNLL and IC had similar distributions of peak- and trough-type neurons, characteristic delays, and best ITDs. The ITD tuning widths of DNLL neurons were intermediate between those of the SOC and IC. Further sharpening is seen in the auditory thalamus, indicating that sharpening mechanisms are not restricted to the midbrain. The proportion of neurons that phase-locked to the tones delivered to each ear progressively decreased from the SOC to the auditory thalamus. The degree of phase-locking for a large majority of DNLL neurons was too weak to support their involvement in processing monaural inputs to generate a sensitivity to ITDs. The response rates of DNLL neurons were on average ∼60% greater than in the IC or SOC, indicating that the inhibitory input provided to the IC by the DNLL is robust.

Discharge Patterns of Neurons in the Ventral Nucleus of the Lateral Lemniscus of the Unanesthetized Rabbit

The ventral nucleus of the lateral lemniscus (VNLL) is a major auditory nucleus that sends a large projection to the inferior colliculus. Despite its prominence, the responses of neurons in the VNLL have not been extensively studied. Previous studies in nonecholocating species have used anesthesia, which is known to affect discharge patterns. In addition, there is disagreement about the proportion of neurons that are sensitive to binaural stimulation. This report examines the responses of neurons in the VNLL of the unanesthetized rabbit to monaural and binaural stimuli. Most neurons responded to contralateral tone bursts at their best frequency and had either sustained or phasic discharge patterns. A few neurons were only inhibited. Most sustained neurons were classified as short-latency sustained (SL-sustained), but a few were of long latency. Some SL-sustained neurons exhibited multiple peaks in their discharge pattern, i.e., they had a “chopper” discharge pattern, whereas other SL-sustained neurons did not exhibit this pattern. In ordinary chopper neurons, the multiple peaks corresponded to the evenly spaced action potentials of a regular discharge. In unusual chopper neurons, the action potential associated with a particular peak could fail to occur during any one presentation of the stimulus. Unusual chopper neurons had a relatively irregular discharge. Phasic neurons were of two types: onset and transient. Onset neurons typically responded with a single action potential at the onset of the tone, whereas transient neurons produced a burst of action potentials. Transient neurons were relatively rare. About half the neurons also were influenced by ipsilateral stimulation. Most binaurally influenced neurons were either sensitive to interaural temporal disparities (ITDs) or excited by contralateral stimulation and inhibited by ipsilateral stimulation. Neurons sensitive to ITDs were mostly of the onset type and were embedded in the fiber tract medial to the main part of the nucleus. Neurons inhibited by ipsilateral stimulation could be of the sustained or onset type. The sustained neurons were located on the periphery of the main nucleus as well as in the fiber tract. Most of the monaural neurons were in the main, high-density part of VNLL. The present results demonstrate that the VNLL contains neurons with a heterogeneous set of responses, and that many of the neurons are binaural.

Neural responses to simple simulated echoes in the auditory brain stem of the unanesthetized rabbit

1. In most natural environments, sound waves from a single source will reach a listener through both direct and reflected paths. Sound traveling the direct path arrives first, and determines the perceived location of the source despite the presence of reflections from many different locations. This phenomenon is called the "law of the first wavefront" or "precedence effect." The time at which the reflection is first perceived as a separately localizable sound defines the end of the precedence window and is called "echo threshold." The precedence effect represents an important property of the auditory system, the neural basis for which has only recently begun to be examined. Here we report the responses of single neurons in the inferior colliculus (IC) and superior olivary complex (SOC) of the unanesthetized rabbit to a sound and its simulated reflection. 2. Stimuli were pairs of monaural or binaural clicks delivered through earphones. The leading click, or conditioner, simulated a direct sound, and the lagging click, or probe, simulated a reflection. Interaural time differences (ITDs) were introduced in the binaural conditioners and probes to adjust their simulated locations. The probe was always set at the neuron's best ITD, whereas the conditioner was set at the neuron's best ITD or its worst ITD. To measure the time course of the effects of the conditioner on the probe, we examined the response to the probe as a function of the conditioner-probe interval (CPI). 3. When IC neurons were tested with conditioners and probes set at the neuron's best ITD, the response to the probe as a function of CPI had one of two forms: early-low or early-high. In early-low neurons the response to the probe was initially suppressed but recovered monotonically at longer CPIs. Early-high neurons showed a nonmonotonic recovery pattern. In these neurons the maximal suppression did not occur at the shortest CPIs, but rather after a period of less suppression. Beyond this point, recovery was similar to that of early-low neurons. The presence of early-high neurons meant that the overall population was never entirely suppressed, even at short CPIs. Taken as a whole. CPIs for 50% recovery of the response to the probe among neurons ranged from 1 to 64 ms with a median of approximately 6 ms. 4. The above results are consistent with the time course of the precedence effect for the following reasons. 1) The lack of complete suppression at any CPI is compatible with behavioral results that show the presence of a probe can be detected even at short CPIs when it is not separately localizable. 2) At a CPI corresponding to echo threshold for human listeners (approximately 4 ms CPI) there was a considerable response to the probe, consistent with it being heard as a separately localizable sound at this CPI. 3) Full recovery for all neurons required a period much longer than that associated with the precedence effect. This is consistent with the relatively long time required for conditioners and probes to be heard with equal loudness. 5. Conditioners with either the best ITD or worst ITD were used to determine the effect of ITD on the response to the probe. The relative amounts of suppression caused by the two ITDs varied among neurons. Some neurons were suppressed about equally by both types of conditioners, others were suppressed more by a conditioner with the best ITD, and still others by a conditioner with the worst ITD. Because the best ITD and worst ITD presumably activate different pathways, these results suggest that different neurons receive a different balance of inhibition from different sources. 6. The recovery functions of neurons not sensitive to ITDs were similar to those of ITD-sensitive, neurons. This suggests that the time course of suppression may be common among different IC populations. 7. We also studied neurons in the SOC. Although many showed binaural interactions, none were sensitive to ITDs. Thus the response of this population may not be