Influence of the facial ruff on the sound-receiving characteristics of the barn owl’s ears

The barn owl, a nocturnal predator, derives its German name (“Schleiereule”, direct English translation “veil owl”) from the conspicuous ruff that covers the ear openings and gives the head a face-like appearance. The ruff is a specialization for the perception of sound. The densely-ramified reflector feathers forming the border of the ruff direct sound to the ear-openings. We studied the influence of the ruff on the behaviorally relevant sound-localization parameters interaural time difference (ITD) and interaural level difference (ILD). The directionality of the ear was much greater when the ruff was intact than when the reflector feathers were removed. With ruff intact, the distribution of ILDs was oblique and the maximum ITD occurred around 110° of azimuth. When all head feathers were removed, the steepest ILD gradient was much closer to the horizontal axis and ITD was maximal at 90°. Many effects were frequency specific. Thus, the ruff reflects some properties of the human pinna. However, by shifting the point where ITD becomes maximal beyond 90°, the ruff also introduces a break of the front–back symmetry of ITD.     

Sound-localization experiments with barn owls in virtual space: influence of broadband interaural level difference on head-turning behavior

Interaural level differences play an important role for elevational sound localization in barn owls. The changes of this cue with sound location are complex and frequency dependent. We exploited the opportunities offered by the virtual space technique to investigate the behavioral relevance of the overall interaural level difference by fixing this parameter in virtual stimuli to a constant value or introducing additional broadband level differences to normal virtual stimuli. Frequency-specific monaural cues in the stimuli were not manipulated. We observed an influence of the broadband interaural level differences on elevational, but not on azimuthal sound localization. Since results obtained with our manipulations explained only part of the variance in elevational turning angle, we conclude that frequency-specific cues are also important. The behavioral consequences of changes of the overall interaural level difference in a virtual sound depended on the combined interaural time difference contained in the stimulus, indicating an indirect influence of temporal cues on elevational sound localization as well. Thus, elevational sound localization is influenced by a combination of many spatial cues including frequency-dependent and temporal features.     

Multiplicative Auditory Spatial Receptive Fields Created by a Hierarchy of Population Codes

A multiplicative combination of tuning to interaural time difference (ITD) and interaural level difference (ILD) contributes to the generation of spatially selective auditory neurons in the owl''s midbrain. Previous analyses of multiplicative responses in the owl have not taken into consideration the frequency-dependence of ITD and ILD cues that occur under natural listening conditions. Here, we present a model for the responses of ITD- and ILD-sensitive neurons in the barn owl''s inferior colliculus which satisfies constraints raised by experimental data on frequency convergence, multiplicative interaction of ITD and ILD, and response properties of afferent neurons. We propose that multiplication between ITD- and ILD-dependent signals occurs only within frequency channels and that frequency integration occurs using a linear-threshold mechanism. The model reproduces the experimentally observed nonlinear responses to ITD and ILD in the inferior colliculus, with greater accuracy than previous models. We show that linear-threshold frequency integration allows the system to represent multiple sound sources with natural sound localization cues, whereas multiplicative frequency integration does not. Nonlinear responses in the owl''s inferior colliculus can thus be generated using a combination of cellular and network mechanisms, showing that multiple elements of previous theories can be combined in a single system.     

Bi-coordinate sound localization by the barn owl

1. Binaurally time-shifted and intensity-unbalanced noise, delivered through earphones, induced owls to respond with a head-orienting behavior similar to that which occurs to free field auditory stimuli. 2. Owls derived the azimuthal and elevational coordinates of a sound from a combination of interaural time difference (ITD) and interaural intensity difference (IID). 3. IID and ITD each contained information about the azimuth and elevation of the signal. Thus, IID and ITD formed a coordinate system in which the axes were non-orthogonal. 4. ITD was a strong determinant of azimuth, and IID was a strong determinant of elevation, of elicited head turn.     

Adaptation in sound localization processing induced by interaural time difference in amplitude envelope at high frequencies

Background

When a second sound follows a long first sound, its location appears to be perceived away from the first one (the localization/lateralization aftereffect). This aftereffect has often been considered to reflect an efficient neural coding of sound locations in the auditory system. To understand determinants of the localization aftereffect, the current study examined whether it is induced by an interaural temporal difference (ITD) in the amplitude envelope of high frequency transposed tones (over 2 kHz), which is known to function as a sound localization cue.

Methodology/Principal Findings

In Experiment 1, participants were required to adjust the position of a pointer to the perceived location of test stimuli before and after adaptation. Test and adapter stimuli were amplitude modulated (AM) sounds presented at high frequencies and their positional differences were manipulated solely by the envelope ITD. Results showed that the adapter''s ITD systematically affected the perceived position of test sounds to the directions expected from the localization/lateralization aftereffect when the adapter was presented at ±600 µs ITD; a corresponding significant effect was not observed for a 0 µs ITD adapter. In Experiment 2, the observed adapter effect was confirmed using a forced-choice task. It was also found that adaptation to the AM sounds at high frequencies did not significantly change the perceived position of pure-tone test stimuli in the low frequency region (128 and 256 Hz).

Conclusions/Significance

The findings in the current study indicate that ITD in the envelope at high frequencies induces the localization aftereffect. This suggests that ITD in the high frequency region is involved in adaptive plasticity of auditory localization processing.     

Sensitivity to interaural time difference and representation of azimuth in central nucleus of inferior colliculus in the barn owl

Standard electrophysiology and virtual auditory stimuli were used to investigate the influence of interaural time difference on the azimuthal tuning of neurons in the core and the lateral shell of the central nucleus of the inferior colliculus of the barn owl. The responses of the neurons to virtual azimuthal stimuli depended in a periodic way on azimuth. Fixation of the interaural time difference, while leaving all other spatial cues unchanged, caused a loss of periodicity and a broadening of azimuthal tuning. This effect was studied in more detail in neurons of the core. The azimuthal range tested and the frequency selectivity of the neurons were additional parameters influencing the changes induced by fixating the interaural time difference. The addition of an interaural time difference to the virtual stimuli resulted in a shift of the tuning curves that correlated with the interaural time difference added. In this condition, tuning strength did not change. These results suggest that interaural time difference is an important determinant of azimuthal tuning in all neurons of the core and lateral shell of the central nucleus of the inferior colliculus, and is the only determinant in many of the neurons from the core.     

Coding of sound location and frequency in the auditory midbrain of diurnal birds of prey,families accipitridae and falconidae

Summary The coding of sound frequency and location in the avian auditory midbrain nucleus (nMLD) was examined in three diurnal raptors: the brown falcon (Falco berigora), the swamp harrier (Circus aeruginosus) and the brown goshawk (Accipiter fasciatus). Previously this nucleus has been studied with free field stimuli in only one other species, the barn owl (Tyto alba).We found some parallels between the organisation of nMLD in the diurnal raptors and that reported in the barn owl in that the central region of nMLD was tonotopically organised and contained cells that did not encode location, and the lateral region (nMLDl) contained cells which were sensitive to stimulus position. However, unlike the barn owl, which has units with circumscribed receptive fields, cells sensitive to stimulus location had large receptive fields which were restricted in azimuth but not in elevation (hemifield units). Such cells could not provide an acoustic space map in which both azimuthal and elevational dimensions were represented, but there was a tendency for units with contralateral borders to be found superficially, and those with ipsilateral borders to be found deep, in nMLDl. Hemifield units displayed receptive field properties consistent with the directional properties of the tympana in the presence of sound transmission through the interaural canal, if there is a central mechanism which is sensitive to interaural intensity differences.Abbreviations nMLD nucleus mesencephalicus lateralis pars dorsalis - SPL sound pressure level re 20 Pa - nMLDl lateral region of nMLD - ICC central nucleus of the inferior colliculus - ICX external nucleus of the inferior colliculus - IID interaural intensity difference - EI excitatory inhibitory     

Optimal nonlinear cue integration for sound localization

Integration of multiple sensory cues can improve performance in detection and estimation tasks. There is an open theoretical question of the conditions under which linear or nonlinear cue combination is Bayes-optimal. We demonstrate that a neural population decoded by a population vector requires nonlinear cue combination to approximate Bayesian inference. Specifically, if cues are conditionally independent, multiplicative cue combination is optimal for the population vector. The model was tested on neural and behavioral responses in the barn owl’s sound localization system where space-specific neurons owe their selectivity to multiplicative tuning to sound localization cues interaural phase (IPD) and level (ILD) differences. We found that IPD and ILD cues are approximately conditionally independent. As a result, the multiplicative combination selectivity to IPD and ILD of midbrain space-specific neurons permits a population vector to perform Bayesian cue combination. We further show that this model describes the owl’s localization behavior in azimuth and elevation. This work provides theoretical justification and experimental evidence supporting the optimality of nonlinear cue combination.     

Properties of low-frequency head-related transfer functions in the barn owl (Tyto alba)

The barn owl (Tyto alba) possesses several specializations regarding auditory processing. The most conspicuous features are the directionally sensitive facial ruff and the asymmetrically arranged ears. The frequency-specific influence of these features on sound has consequences for sound localization that might differ between low and high frequencies. Whereas the high-frequency range (>3 kHz) is well investigated, less is known about the characteristics of head-related transfer functions for frequencies below 3 kHz. In the present study, we compared 1/3 octaveband-filtered transfer functions of barn owls with center frequencies ranging from 0.5 to 9 kHz. The range of interaural time differences was 600 μs at frequencies above 4 kHz, decreased to 505 μs at 3 kHz and increased again to about 615 μs at lower frequencies. The ranges for very low (0.5–1 kHz) and high frequencies (5–9 kHz) were not statistically different. Interaural level differences and monaural gains increased monotonically with increasing frequency. No systematic influence of the body temperature on the measured localization cues was observed. These data have implications for the mechanism underlying sound localization and we suggest that the barn owl’s ears work as pressure receivers both in the high- and low-frequency ranges.     

Maps of interaural time difference in the chicken’s brainstem nucleus laminaris

Animals, including humans, use interaural time differences (ITDs) that arise from different sound path lengths to the two ears as a cue of horizontal sound source location. The nature of the neural code for ITD is still controversial. Current models differentiate between two population codes: either a map-like rate-place code of ITD along an array of neurons, consistent with a large body of data in the barn owl, or a population rate code, consistent with data from small mammals. Recently, it was proposed that these different codes reflect optimal coding strategies that depend on head size and sound frequency. The chicken makes an excellent test case of this proposal because its physical prerequisites are similar to small mammals, yet it shares a more recent common ancestry with the owl. We show here that, like in the barn owl, the brainstem nucleus laminaris in mature chickens displayed the major features of a place code of ITD. ITD was topographically represented in the maximal responses of neurons along each isofrequency band, covering approximately the contralateral acoustic hemisphere. Furthermore, the represented ITD range appeared to change with frequency, consistent with a pressure gradient receiver mechanism in the avian middle ear. At very low frequencies, below 400 Hz, maximal neural responses were symmetrically distributed around zero ITD and it remained unclear whether there was a topographic representation. These findings do not agree with the above predictions for optimal coding and thus revive the discussion as to what determines the neural coding strategies for ITDs.     

Effects of binaural decorrelation on neural and behavioral processing of interaural level differences in the barn owl (Tyto alba)

The effect of binaural decorrelation on the processing of interaural level difference cues in the barn owl (Tyto alba) was examined behaviorally and electrophysiologically. The electrophysiology experiment measured the effect of variations in binaural correlation on the first stage of interaural level difference encoding in the central nervous system. The responses of single neurons in the posterior part of the ventral nucleus of the lateral lemniscus were recorded to stimulation with binaurally correlated and binaurally uncorrelated noise. No significant differences in interaural level difference sensitivity were found between conditions. Neurons in the posterior part of the ventral nucleus of the lateral lemniscus encode the interaural level difference of binaurally correlated and binaurally uncorrelated noise with equal accuracy and precision. This nucleus therefore supplies higher auditory centers with an undegraded interaural level difference signal for sound stimuli that lack a coherent interaural time difference. The behavioral experiment measured auditory saccades in response to interaural level differences presented in binaurally correlated and binaurally uncorrelated noise. The precision and accuracy of sound localization based on interaural level difference was reduced but not eliminated for binaurally uncorrelated signals. The observation that barn owls continue to vary auditory saccades with the interaural level difference of binaurally uncorrelated stimuli suggests that neurons that drive head saccades can be activated by incomplete auditory spatial information.     

Coding interaural time differences at low best frequencies in the barn owl.

In birds and mammals, precisely timed spikes encode the timing of acoustic stimuli, and interaural acoustic disparities propagate to binaural processing centers. The Jeffress model proposes that these projections act as delay lines to innervate an array of coincidence detectors, every element of which has a different relative delay between its ipsilateral and contralateral excitatory inputs. Thus, interaural time difference (ITD) is encoded into the position of the coincidence detector whose delay lines best cancel out the acoustic ITD. Neurons of the avian nucleus laminaris and mammalian MSO phase-lock to both monaural and binaural stimuli but respond maximally when phase-locked spikes from each side arrive simultaneously, i.e. when the difference in the conduction delays compensates for the ITD. McAlpine et al. [Nat. Neurosci. 4 (2001) 396] identified an apparent difference between avian and mammalian ITD coding. In the barn owl, the maximum firing rate appears to encode ITD. This may not be the case for the guinea pig, where the steepest region of the function relating discharge rate to interaural time delay (ITD) is close to midline for all neurons, irrespective of best frequency (BF). These data suggest that low BF ITD sensitivity in the guinea pig is mediated by detection of a change in slope of the ITD function, and not by maximum rate. We review coding of low best frequency ITDs in barn owls and mammals and discuss whether there may be differences in the code used to signal ITD in mammals and birds.     

The synthesis and use of the owl’s auditory space map

The barn owl (Tyto alba) is capable of capturing prey by passive hearing alone, guided by a topographic map of auditory space in the external nucleus of its inferior colliculus. The neurons of this auditory space map have discrete spatial receptive fields that result from the computation of interaural differences in the level (ILD) and time-of-arrival (ITD) of sounds. Below we review the synthesis of the spatial receptive fields from the frequency-specific ITDs and ILDs to which the neurons are tuned, concentrating on recent studies exploiting virtual auditory space techniques to analyze the contribution of ILD. We then compared the owls spatial discrimination, assessed behaviorally, with that of its space map neurons. Spatial discrimination was assessed using a novel paradigm involving the pupillary dilation response (PDR), and neuronal acuity was assessed by measuring the changes in firing rate resulting from changes in source location, scaled to the variance. This signal-detection-based approach revealed that the change in the position of the neural image on this map best explains the spatial discrimination measured using the PDR. We compare this result to recent studies in mammalian systems.     

Mutation in the Kv3.3 Voltage-Gated Potassium Channel Causing Spinocerebellar Ataxia 13 Disrupts Sound-Localization Mechanisms

Normal sound localization requires precise comparisons of sound timing and pressure levels between the two ears. The primary localization cues are interaural time differences, ITD, and interaural level differences, ILD. Voltage-gated potassium channels, including Kv3.3, are highly expressed in the auditory brainstem and are thought to underlie the exquisite temporal precision and rapid spike rates that characterize brainstem binaural pathways. An autosomal dominant mutation in the gene encoding Kv3.3 has been demonstrated in a large Filipino kindred manifesting as spinocerebellar ataxia type 13 (SCA13). This kindred provides a rare opportunity to test in vivo the importance of a specific channel subunit for human hearing. Here, we demonstrate psychophysically that individuals with the mutant allele exhibit profound deficits in both ITD and ILD sensitivity, despite showing no obvious impairment in pure-tone sensitivity with either ear. Surprisingly, several individuals exhibited the auditory deficits even though they were pre-symptomatic for SCA13. We would expect that impairments of binaural processing as great as those observed in this family would result in prominent deficits in localization of sound sources and in loss of the "spatial release from masking" that aids in understanding speech in the presence of competing sounds.     

On the ability of neurons in the barn owl's inferior colliculus to sense brief appearances of interaural time difference

Summary This paper investigates the ability of neurons in the barn owl's (Tyto alba) inferior colliculus to sense brief appearances of interaural time difference (ITD), the main cue for azimuthal sound localization in this species. In the experiments, ITD-tuning was measured during presentation of a mask-probe-mask sequence. The probe consisted of a noise having a constant ITD, while the mask consisted of binaurally uncorrelated noise. Collicular neurons discriminated between the probe and masking noise by showing rapid changes from untuned to tuned and back to untuned responses.The curve describing the relation between probe duration and the degree of ITD-tuning resembled a leaky-integration process with a time constant of about 2 ms. Many neurons were ITD-tuned when probe duration was below 1 ms. These extremely short effective probe durations are interpreted as evidence for neuronal convergence within the pathway computing ITD. The minimal probe duration necessary for ITD-tuning was independent of the bandwidth of the neurons' frequency tuning and also of the best frequency of a neuron. Many narrowly tuned neurons having different best frequencies converge to form a broad-band neuron. To yield the short effective probe durations the convergence must occur in strong temporal synchronism.Abbreviations ICc central nucleus of the inferior colliculus; - ICx external nucleus of the inferior colliculus; - ITD interaural time difference - LP Likelihood parameter     

Binaural processing in the synthesis of auditory spatial receptive fields

The owls auditory system computes interaural time (ITD) and interaural level (ILD) differences to create a two-dimensional map of auditory space. Space-specific neurons are selective for combinations of ITD and ILD, which define, respectively, the horizontal and vertical dimensions of their receptive fields. ITD curves for postsynaptic potentials indicate that ICx neurons integrate the results of binaural cross correlation in different frequency bands. However, the difference between the main and side peaks is slight. ICx neurons further enhance this difference in the process of converting membrane potentials to impulse rates. Comparison of subthreshold postsynaptic potentials (PSPs) and spike output for the same neurons showed that receptive fields measured in PSPs were much larger than those measured in spikes in both ITD and ILD dimensions. A multiplication of separate postsynaptic potentials tuned to ITD and ILD can account for the combination sensitivity of these neurons to ITD–ILD pairs.     

Noninvasive fMRI Investigation of Interaural Level Difference Processing in the Rat Auditory Subcortex

Objective

Interaural level difference (ILD) is the difference in sound pressure level (SPL) between the two ears and is one of the key physical cues used by the auditory system in sound localization. Our current understanding of ILD encoding has come primarily from invasive studies of individual structures, which have implicated subcortical structures such as the cochlear nucleus (CN), superior olivary complex (SOC), lateral lemniscus (LL), and inferior colliculus (IC). Noninvasive brain imaging enables studying ILD processing in multiple structures simultaneously.

Methods

In this study, blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is used for the first time to measure changes in the hemodynamic responses in the adult Sprague-Dawley rat subcortex during binaural stimulation with different ILDs.

Results and Significance

Consistent responses are observed in the CN, SOC, LL, and IC in both hemispheres. Voxel-by-voxel analysis of the change of the response amplitude with ILD indicates statistically significant ILD dependence in dorsal LL, IC, and a region containing parts of the SOC and LL. For all three regions, the larger amplitude response is located in the hemisphere contralateral from the higher SPL stimulus. These findings are supported by region of interest analysis. fMRI shows that ILD dependence occurs in both hemispheres and multiple subcortical levels of the auditory system. This study is the first step towards future studies examining subcortical binaural processing and sound localization in animal models of hearing.     

Delay Line Models of Sound Localization in the Barn Owl

SYNOPSIS. The detection of interaural time differences underliesazimuthal sound localization in the barn owl. Sensitivity tothese time differences arises in the brainstem nucleus laminaris.Auditory information reaches the nucleus laminaris via bilateralprojections from the cochlear nucleus magnocellularis. The magnocellularinputs to the nucleus laminaris act as delay lines to createmaps of interaural time differences. These delay lines are tappedby postsynaptic coincidence detectors that encode interauraltime differences. The entire circuit, from the auditory nerveto the nucleus magnocellularis to the nucleus laminaris, isspecialized for the encoding and preservation of temporal information.A mathematical model of this circuit (Grun et al., 1990) providesuseful predictions.     

Precognitive and cognitive elements in sound localization

Sound localization behavior is of great importance for an animal's survival. To localize a sound, animals have to detect a sound source and assign a location to it. In this review we discuss recent results on the underlying mechanisms and on modulatory influences in the barn owl, an auditory specialist with very well developed capabilities to localize sound. Information processing in the barn owl auditory pathway underlying the computations of detection and localization is well understood. This analysis of the sensory information primarily determines the following orienting behavior towards the sound source. However, orienting behavior may be modulated by cognitive (top-down) influences such as attention. We show how advanced stimulation techniques can be used to determine the importance of different cues for sound localization in quasi-realistic stimulation situations, how attentional influences can improve the response to behaviorally relevant stimuli, and how attention can modulate related neural responses. Taken together, these data indicate how sound localization might function in the usually complex natural environment.     

Directional hearing in the barn owl (Tyto alba)

Summary The acoustical properties of the external ear of the barn owl (Tyto alba) were studied by measuring sound pressure in the ear canal and outer ear cavity. Under normal conditions, pressure amplification by the external ear reaches about 20 dB between 3–9 kHz but decreases sharply above 10 kHz. The acoustic gain curve of the outer ear cavity alone is close to that of a finite-length exponential horn between 1.2–13 kHz with maximum gain reaching 20 dB between 5–9 kHz. Pressure gain by the facial ruff produces a maximum of 12 dB between 5–8 kHz and decreases rapidly above 9 kHz.The directional sensitivity of the external ear was obtained from pressure measurements in the ear canal. Directivity of the major lobe is explained, to a first approximation, by the sound diffraction properties of a circular aperture. Aperture size is based on the average radius (30 mm) of the open face of the ruff. Above 5 kHz, the external ear becomes highly directional and there is a 26° disparity in elevation between the acoustic axis of the left and right ear. In azimuth, directivity patterns are relocated closer to the midline as frequency increases and the acoustic axis moves at a rate of 20°/octave between 2–13 kHz. Movement of the axis can be explained, to a first approximation, by the acoustical diffraction properties of an obliquely truncated horn, due to the asymmetrical shape of the outer ear cavity.The directional sensitivity of the barn owl ear was studied by recording cochlear microphonic (CM) potentials from the round window membrane. Between 3–9 kHz, CM directivity patterns are clearly different to the directivity patterns of the external ear; CM directionality is abruptly lost above 10 kHz. Above 5 kHz, CM directivity patterns are characterized by an elongated major lobe containing the CM axis, forming a tilted band of high amplitude but low directionality (CM axial plane), closely bordered by minima or nulls. The highest directionality is found in theCM directional plane, approximately perpendicular to the CM axial plane. The left and right ear axial planes are symmetrical about the interaural midline (tilted 12° to the right of the midline of the head) and inclined by an average of 60° to the left and right respectively. In azimuth, the CM axis moves towards the midline at a rate of 37°/octave as frequency increases from 2–9 kHz, crossing into contralateral space near 7 kHz. In the CM directional plane, the directivity of the major lobe suggests that a pressure gradient may occur at the TM. The region of frontal space mapped by movement of the CM axis in azimuth closely matches the angle of sound incidence which would be expected to produce the maximum driving pressure at the TM. It is suggested that acoustical interference at the TM results from sound transmission through the interaural canal and therefore the ear is inherently directional. It is proposed that ear directionality in the barn owl may be explained by the combined effect of sound diffraction by the outer ear cavity and a pressure gradient at the TM.Abbreviations CM cochlear microphonic - RMS root mean square - SPL sound pressure level - TM tympanic membrane