Sound Localization in the Owl

Sound localization in the barn owl relies on the early processing of two binaural cues, ITD (interaural time differences) and ILD (interaural level differences), that takes place in two parallel pathways in the auditory brainstem. Previous modeling studies fell into one of two classes, either they used biophysically plausible neural models on simplified binaural stimuli with artificially induced ITDs, or abstract cross-correlation models on realistic acoustical inputs. Here we present a functional spiking neural model of the ITD processing pathway of the barn owl, with a realistic virtual acoustic environment. The acoustical environment was reproduced by filtering natural sounds through measured Head-Related Transfer Functions (HRTFs) in the barn owl (Tyto Alba). Basilar membrane filtering was modeled with a bank of linear gammachirp filters and compression. Monaural neurons in the Nucleus Magnucellularis (NM) receive inputs from auditory nerve fibers and project axons to binaural neurons in the Nucleus Laminaris (NL), with various conduction delays, so that best delays depend on preferred frequency in accordance with measured distributions [1]. Empirical findings show that the best tuning of NL neurons is invariant to level and ILD changes [3], which implies that the spike timing of their monaural inputs should also be invariant to level. This is a challenging problem, since integration to a fixed threshold inevitably results in earlier spike timing when the input level is increased. We address this issue by using a spiking model with dynamic threshold [2,4]. We derive analytical conditions under which one can achieve this level invariance, and show through numerical simulations that the responses of our model to realistic inputs are indeed robust to level and ILD changes. The azimuth is estimated from the activation pattern of NL neurons. We found that the model could accurately estimate the azimuth of a large set of natural sounds with various levels, and significant background noise. Furthermore, we studied the robustness of ITD estimation in our model to reflective environments. We believe this study is a first step towards the development of neural models of sound localization in ecological environments.

Barn owls perform sound localization based on analyses of interaural differences in arrival time and intensity of sound. Two kinds of neural signals representing the interaural time difference (ITD) and the interaural intensity difference (IID) are processed in parallel in anatomically separate pathway. We explain briefly the neural models of pathways of ITD and IID detection which we have already presented [1,2]. We present a neural network model of ICc ls in which the signals representing ITD and IID are first combined with each other. It is shown using our neural models how the neural map, in which ITD and IID are represented along the axes being perpendicular mutually, can be generated in ICc ls by the excitatory inputs from ICc core representing ITD and the inhibitory inputs from bilateral VLVps representing IID. We show that the firing rates of ICc ls neuron are well represented by a suppressive multiplication of ITD and IID inputs. This seems to be the origin of the multiplicative binding found in ICx by Pena and Konishi [3].

Interaural time differences (ITD) and interaural level differences (ILD) both signal horizontal sound source location. To achieve a unified percept of our acoustic environment, these two cues require integration. In the present study, we tested this integration of ITD and ILD with electroencephalography (EEG) by measuring the mismatch negativity (MMN). The MMN can arise in response to spatial changes and is at least partly generated in auditory cortex. In our study, we aimed at testing for an MMN in response to stimuli with counter-balanced ITD/ILD cues. To this end, we employed a roving oddball paradigm with alternating sound sequences in two types of blocks: (a) lateralized stimuli with congruently combined ITD/ILD cues and (b) midline stimuli created by counter-balanced, incongruently combined ITD/ILD cues. We observed a significant MMN peaking at about 112–128 ms after change onset for the congruent ITD/ILD cues, for both lower (0.5 kHz) and higher carrier frequency (4 kHz). More importantly, we also observed significant MMN peaking at about 129 ms for incongruently combined ITD/ILD cues, but this effect was only detectable in the lower frequency range (0.5 kHz). There were no significant differences of the MMN responses for the two types of cue combinations (congruent/incongruent). These results suggest that—at least in the lower frequency ranges (0.5 kHz)—ITD and ILD are processed independently at the level of the MMN in auditory cortex.

The sound localization of barn owl with respect to horizontal and vertical direction is made based on analysis of the interaural differences in arrival time and intensity of sound, respectively. The neural information processing of detection of interaural intensity difference (IID) is made on the neural pathway parallel with the pathway of interaural time difference (ITD) detection before both the signals arrive at the shell of central nucleus of the inferior colliculus (ICc shell). We have presented a neural model of ITD detection pathway (Inoue et al, Neurocomputing 2001, vol. 38-40, pp. 675-682). We present a neuronal model of the nucleus ventralis lemnisci lateralis pars posterior (VLVp) in which the signals of sound intensities coming from both the ears are first combined to be compared with each other. We clarify the functional role of mutual inhibitory connections between both VLVps observed experimentally in detection of IID. Outputs of IID sensitive neurons in both VLVps are projected bilaterally to ICc shell and the connections are inhibitory, whereas outputs of ITD sensitive neurons in ICc core projected to ICc shell are excitatory. It is shown using our neuronal models of VLVps, ICc core, and ICc shell that the neural map, in which ITD and IID are represented along the axes perpendicular mutually, can be generated in ICc shell by the excitatory inputs from ICc core and the inhibitory inputs from bilateral VLVps, as observed experimentally. We also show that the firing rate of ICc shell neuron are well represented by a suppressive multiplication of ITD and IID inputs.

The cross-correlation model has long served as the standard computational framework for describing interaural time difference (ITD) processing in the barn owl's auditory system. While successful in explaining initial sinusoidal responses at the site of coincidence detection in the nucleus laminaris, this previous standard model fails to capture the full diversity of ITD tuning observed in the inferior colliculus (IC), where neurons exhibit sharper-than-sinusoidal ITD tuning, nonlinear frequency integration, level-dependent gain control, and interaural level difference (ILD)-dependent modulation of ITD selectivity. Here we present a modified cross-correlation model that addresses these limitations through the addition of parameterized gain control, linear filters with inhibitory surround structure, static nonlinearities, and ILD-dependent modulation of the cross-correlation computation. We show that divisive gain control produces realistic rate-level functions, including non-monotonic responses. Furthermore, inhibitory weights in the linear filter, combined with a threshold or expansive nonlinearity, generate sharper-than-sinusoidal ITD tuning consistent with experimental observations. This model reproduces both linear and nonlinear two-tone frequency integration and demonstrates that independent variation of filter bandwidth and nonlinearity shape accounts for the experimentally observed lack of correlation between side-peak suppression and frequency tuning width across the neuronal population. In addition, ILD-dependent modifications to the model produce shifts in best ITD and reductions in ITD tuning strength, as observed in the lateral shell of the central nucleus of the IC. The model parameters can be efficiently determined using simulation-based inference, enabling generation of realistic neuronal populations. Thus, this flexible, analytically tractable framework provides a foundation for investigating population coding of auditory space in the owl's midbrain.

The role of interaural differences in localization of spatially segregated sound was clarified by performing listening tests on sound localization. Four subjects were asked to distinguish two sources of white noise with various interaural time differences (ITDs) or interaural level differences (ILDs). As a result, the segregated rate reached 80% when the ITD between two white noise sources corresponded to an angular difference of 22 degrees. The segregated rate degraded to 50% when the ITD between two white noise sources corresponded to an angular difference of 7 degrees. In addition, the segregated rate reached 80% when the ILD between two white noise sources corresponded to an angular difference of 30 degrees. The segregated rate degraded to 50% when the ILD between two white noise sources corresponded to an angular difference of about 15 degrees. These results suggest that sound sources could be spatially segregated using even only ITD or ILD.

1. Interaural level differences (ILDs), created by the head and pinna, have long been known to be the dominant acoustic cue for azimuthal localization of high-frequency tones. However, psychophysical experiments have demonstrated that human subjects can also lateralize complex high-frequency sounds on the basis of interaural time differences (ITDs) of the signal envelope. The lateral superior olive (LSO) is one of two pairs of binaural nuclei where the primary extraction of binaural cues for sound source location occurs. "IE" cells in LSO are inhibited by stimuli to the contralateral and excited by stimuli to the ipsilateral ear, and their response rate is therefore dependent on ILD. Anatomic specializations in the afferent pathways to the LSO suggest that this circuit also has a function in the detection of timing cues. We hypothesized that, besides ILD sensitivity, the IE property also conveys a sensitivity to ITDs of amplitude-modulated (AM) tones and could provide the physiological substrate for the psychophysical effect mentioned above. 2. In extracellular recordings from binaural LSO cells in barbiturate-anesthetized cats, response rate was a periodic function of ITDs of AM stimuli, i.e., all cells displayed ITD sensitivity. Binaural responses were smaller than responses to stimulation of the ipsilateral ear alone and were minimal when the envelopes in both ears were in-phase or nearly so. There was good correspondence between responses to ITDs and to dynamic interaural phase differences (IPDs), created by a difference in the envelope frequency to the two ears. Qualitatively, the responses were consistent with the outcome of an IE operation on temporally structured inputs. 3. To compare the relative importance of ILD and ITD, responses to combinations of the two cues were obtained. Despite robust ITD sensitivity in all binaural LSO cells encountered, the changes in response rate that would occur in response to naturally occurring ITDs were small in comparison with the changes expected for naturally occurring ILDs. The main limitation on ITD sensitivity was a steep decline in average discharge rate as the modulation frequency exceeded several hundred Hertz. 4. ITD sensitivity was also present to broadband stimuli, again with minimal rates occurring near 0 ITD. The sensitivity depended in a predictable fashion on the passband of filtered noise and was absent to binaurally uncorrelated noise bands. In response to clicks, ILDs interacted with ITD in a complicated fashion involving amplitude and latency effects. 5. Three low-characteristic frequency (CF) LSO cells were encountered that were IE and showed ITD sensitivity to the fine structure of low-frequency stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

SUMMARYHearing information is very important when visual information is limited. Sound source localization has been noted as particularly important in hearing information processing. Barn owls have excellent auditory processing. We propose a hardware model based on the auditory sense mechanism of barn owls. In this paper, we consider a model of the external nucleus of the inferior colliculus (ICx), which locates the source of a sound by the interaural time difference (ITD) for localization in the horizontal direction, and the interaural level difference (ILD) for localization in the vertical direction. The results show that the detection position of an ITD model and the detection position of an ILD model can converge. In addition, the output position of the ICx model changes with the position of the sound source.

Experiments were conducted with a single, bilateral cochlear implant user to examine interaural level and time-delay cues that putatively underlie the design and efficacy of bilateral implant systems. The subject's two implants were of different types but custom equipment allowed presentation of controlled bilateral stimuli, particularly those with specified interaural time difference (ITD) and interaural level difference (ILD) cues. A lateralization task was used to measure the effect of these cues on the perceived location of the sensations elicited. For trains of fixed-amplitude, biphasic current pulses at 100 pps, the subject demonstrated sensitivity to an ITD of 300 micros, providing evidence of access to binaural information. The choice of bilateral electrode pair greatly influenced ITD sensitivity, suggesting that electrode pairings are likely to be an important consideration in the effort to provide binaural advantages. The selection of bilateral electrode pairs showing sensitivity to ITD was partially aided by comparisons of the pitch elicited by individual electrodes in each ear (when stimulated alone with fixed-amplitude current pulses at 813 pps): specifically, interaural electrodes with similar pitches were more likely (but not certain) to show ITD sensitivity. Significant changes in lateral position occurred with specific electrode pairs. With five bilateral electrode pairs of 14 tested, ITDs of 300 and 600 micros moved an auditory image significantly from right to left. With these same pairs, ILD changes of approximately 11% of the dynamic range (in microApp) moved an auditory image from the far left to the far right-significantly farther than the nine pairs not showing significant ITD sensitivity. However, even these nine pairs did show response changes as a function of the interaural (or confounding monaural) level cue. Overall, insofar as the access to bilateral cues demonstrated herein generalizes to other subjects, it provides hope that the normal binaural advantages for speech recognition and sound localization can be made available to bilateral implant users.

Prediction of binaural click lateralization by brainstem auditory evoked potentials

Discrimination of sensory stimuli is fundamentally constrained by the information encoded in neuronal responses. In the barn owl, interaural time difference (ITD) serves as a primary cue for azimuthal sound localization and is represented topographically in the midbrain auditory space map in the external nucleus of the inferior colliculus (ICx). While prior studies have demonstrated a correspondence between spatial tuning and behavioral acuity, it remains unclear how changes in sensory reliability influence this relationship. Here, we examined how behavioral and neuronal ITD discrimination thresholds vary with binaural correlation (BC), which manipulates ITD cue reliability. Using the pupil dilation response as a behavioral metric in head-fixed owls of either sex, we found that ITD just-noticeable differences increased exponentially as BC decreased. In contrast, the widths of ICx ITD tuning curves increased more modestly, indicating that tuning resolution alone does not account for behavioral discrimination performance. By computing the Fisher information from ICx neuronal responses, we showed that the average neuronal discriminability predicts behavioral thresholds across BC values. A habituation-based model incorporating BC-dependent changes in tuning width, firing rate, and response variability successfully accounted for both direction and ITD discrimination. These findings support a model in which perceptual acuity is governed by the combined influence of neuronal tuning and variability and provide a unified framework for understanding how midbrain auditory representations underlie adaptive spatial hearing.

The acoustical cues for sound location are generated by spatial- and frequency-dependent filtering of propagating sound waves by the head and external ears. Although rats have been a common model system for anatomy, physiology, and psychophysics of localization, there have been few studies of the acoustical cues available to rats. Here, directional transfer functions (DTFs), the directional components of the head-related transfer functions, were measured in six adult rats. The cues to location were computed from the DTFs. In the frontal hemisphere, spectral notches were present for frequencies from approximately 16 to 30 kHz; in general, the frequency corresponding to the notch increased with increases in source elevation and in azimuth toward the ipsilateral ear. The maximum high-frequency envelope-based interaural time differences (ITDs) were 130 mus, whereas low-frequency (<3.5 kHz) fine-structure ITDs were 160 mus; both types of ITDs were larger than predicted from spherical head models. Interaural level differences (ILDs) strongly depended on location and frequency. Maximum ILDs were <10 dB for frequencies <8 kHz and were as large as 20-40 dB for frequencies >20 kHz. Removal of the pinna eliminated the spectral notches, reduced the acoustic gain and ILDs, altered the acoustical axis, and reduced the ITDs.

With the exception of low‐frequency characteristic frequency (CF) units, the ipsilaterally evoked discharge of the majority of S‐segment cells can be inhibited with simultaneous stimulation of the contralateral ear. The contralateral inhibitory CF is usually identical to the ipsilateral excitatory CF. The width of the contralateral inhibitory tuning curve is similar to the width of the ipsilateral excitatory tuning curve. Partial inhibition of the ipsilaterally evoked discharge increases the interspike intervals and increases the variability of the discharge. Inhibition, like excitation, is tonically acting. The contralateral inhibitory input with equally intense tones (measured in terms of decibels above threshold) is either about as effective as the excitatory input or less effective, rarely more effective. The primary factor determining the spike output from S‐segment cells is not the absolute intensity level of the stimulus but rather the relative intensity difference of the stimulus at the two ears. [Work supported in part by National Institutes of Health, U. S. Department of Health, Education, and Welfare.]

This paper presents a new method of sound source localization based on zero-crossings generated from binaural filter-bank outputs. To detect the sound source direction, in the conventional methods the inter-aural time differences (ITDs) and the inter-aural intensity differences (IIDs) are estimated using the cross-correlations of neuronal firing rates. However, these methods require high computational complexity involved in the computation of cross-correlations and they suffer from inaccuracies in estimating the ITDs and IIDs, especially in a noisy multisource environment. In this context, we propose a method using zero-crossing and peak-amplitudes (ZCPAs) of binaural filter-bank outputs for accurate and efficient estimation of ITDs and IIDs. The proposed method is able to provide accurate estimation of the sound source direction and robustness to noise while offering significantly less computational complexity compared to cross-correlation based methods.

A novel deep learning (DL) method is proposed for binaural sound source localization with low SNR. Firstly, the binaural sound signals are decomposed into several channels by using Gammatone filter. Secondly, the 4 feature parameters of Head-related Transfer Function, interaural time difference (ITD), interaural coherence (IC), interaural level difference (ILD), and interaural phase difference (IPD) are extracted. Thirdly, ITD and IC go through a Deep Belief Network (DBN) to determine the quadrant of the sound source and reduce the positioning range. Then, ITD, IC, ILD, and IPD go through a Deep Neural Network (DNN) to obtain the azimuthal angle within 90 degrees. Experimental results show that the proposed algorithm can solve the front-back confusion, and obtain a superior performance with lower complexity and higher precision under low SNR conditions.