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.     

The function of the medial superior olive in small mammals: temporal receptive fields in auditory analysis

Traditionally, the medial superior olive, a mammalian auditory brainstem structure, is considered to encode interaural time differences, the main cue for localizing low-frequency sounds. Detection of binaural excitatory and inhibitory inputs are considered as an underlying mechanism. Most small mammals, however, hear high frequencies well beyond 50 kHz and have small interaural distances. Therefore, they can not use interaural time differences for sound localization and yet possess a medial superior olive. Physiological studies in bats revealed that medial superior olive cells show similar interaural time difference coding as in larger mammals tuned to low-frequency hearing. Their interaural time difference sensitivity, however, is far too coarse to serve in sound localization. Thus, interaural time difference sensitivity in medial superior olive of small mammals is an epiphenomenon. We propose that the original function of the medial superior olive is a binaural cooperation causing facilitation due to binaural excitation. Lagging inhibitory inputs, however, suppress reverberations and echoes from the acoustic background. Thereby, generation of antagonistically organized temporal fields is the basic and original function of the mammalian medial superior olive. Only later in evolution with the advent of larger mammals did interaural distances, and hence interaural time differences, became large enough to be used as cues for sound localization of low-frequency stimuli. Accepted: 28 February 2000     

Structural Changes and Lack of HCN1 Channels in the Binaural Auditory Brainstem of the Naked Mole-Rat (Heterocephalus glaber)

Naked mole-rats (Heterocephalus glaber) live in large eu-social, underground colonies in narrow burrows and are exposed to a large repertoire of communication signals but negligible binaural sound localization cues, such as interaural time and intensity differences. We therefore asked whether monaural and binaural auditory brainstem nuclei in the naked mole-rat are differentially adjusted to this acoustic environment. Using antibody stainings against excitatory and inhibitory presynaptic structures, namely the vesicular glutamate transporter VGluT1 and the glycine transporter GlyT2 we identified all major auditory brainstem nuclei except the superior paraolivary nucleus in these animals. Naked mole-rats possess a well structured medial superior olive, with a similar synaptic arrangement to interaural-time-difference encoding animals. The neighboring lateral superior olive, which analyzes interaural intensity differences, is large and elongated, whereas the medial nucleus of the trapezoid body, which provides the contralateral inhibitory input to these binaural nuclei, is reduced in size. In contrast, the cochlear nucleus, the nuclei of the lateral lemniscus and the inferior colliculus are not considerably different when compared to other rodent species. Most interestingly, binaural auditory brainstem nuclei lack the membrane-bound hyperpolarization-activated channel HCN1, a voltage-gated ion channel that greatly contributes to the fast integration times in binaural nuclei of the superior olivary complex in other species. This suggests substantially lengthened membrane time constants and thus prolonged temporal integration of inputs in binaural auditory brainstem neurons and might be linked to the severely degenerated sound localization abilities in these animals.     

The Modulation by Intensity of the Processing of Interaural Timing Cues for Localizing Sounds

Features of sounds such as time and intensity are important binaural cues for localizing their sources. Interaural time differences (ITDs) and interaural level differences are extracted and processed in parallel by separate pathways in the brainstem auditory nuclei. ITD cues are small, particularly in small-headed animals, and processing of these cues is optimized by both morphological and physiological specializations. Moreover, recent observations in mammals and in some birds indicate that interaural time and level cues are not processed independently but cooperatively to improve the detection of interaural differences. This review will specifically summarize what is known about how inhibitory circuits improve the measurements of ITD in a sound-level-dependent manner.     

Asymmetric Excitatory Synaptic Dynamics Underlie Interaural Time Difference Processing in the Auditory System

Low-frequency sound localization depends on the neural computation of interaural time differences (ITD) and relies on neurons in the auditory brain stem that integrate synaptic inputs delivered by the ipsi- and contralateral auditory pathways that start at the two ears. The first auditory neurons that respond selectively to ITD are found in the medial superior olivary nucleus (MSO). We identified a new mechanism for ITD coding using a brain slice preparation that preserves the binaural inputs to the MSO. There was an internal latency difference for the two excitatory pathways that would, if left uncompensated, position the ITD response function too far outside the physiological range to be useful for estimating ITD. We demonstrate, and support using a biophysically based computational model, that a bilateral asymmetry in excitatory post-synaptic potential (EPSP) slopes provides a robust compensatory delay mechanism due to differential activation of low threshold potassium conductance on these inputs and permits MSO neurons to encode physiological ITDs. We suggest, more generally, that the dependence of spike probability on rate of depolarization, as in these auditory neurons, provides a mechanism for temporal order discrimination between EPSPs.     

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.     

Improvements of Sound Localization Abilities by the Facial Ruff of the Barn Owl (Tyto alba) as Demonstrated by Virtual Ruff Removal

Background

When sound arrives at the eardrum it has already been filtered by the body, head, and outer ear. This process is mathematically described by the head-related transfer functions (HRTFs), which are characteristic for the spatial position of a sound source and for the individual ear. HRTFs in the barn owl (Tyto alba) are also shaped by the facial ruff, a specialization that alters interaural time differences (ITD), interaural intensity differences (ILD), and the frequency spectrum of the incoming sound to improve sound localization. Here we created novel stimuli to simulate the removal of the barn owl''s ruff in a virtual acoustic environment, thus creating a situation similar to passive listening in other animals, and used these stimuli in behavioral tests.

Methodology/Principal Findings

HRTFs were recorded from an owl before and after removal of the ruff feathers. Normal and ruff-removed conditions were created by filtering broadband noise with the HRTFs. Under normal virtual conditions, no differences in azimuthal head-turning behavior between individualized and non-individualized HRTFs were observed. The owls were able to respond differently to stimuli from the back than to stimuli from the front having the same ITD. By contrast, such a discrimination was not possible after the virtual removal of the ruff. Elevational head-turn angles were (slightly) smaller with non-individualized than with individualized HRTFs. The removal of the ruff resulted in a large decrease in elevational head-turning amplitudes.

Conclusions/Significance

The facial ruff a) improves azimuthal sound localization by increasing the ITD range and b) improves elevational sound localization in the frontal field by introducing a shift of iso–ILD lines out of the midsagittal plane, which causes ILDs to increase with increasing stimulus elevation. The changes at the behavioral level could be related to the changes in the binaural physical parameters that occurred after the virtual removal of the ruff. These data provide new insights into the function of external hearing structures and open up the possibility to apply the results on autonomous agents, creation of virtual auditory environments for humans, or in hearing aids.     

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.     

Sound localization: Jeffress and beyond

Many animals use the interaural time differences (ITDs) to locate the source of low frequency sounds. The place coding theory proposed by Jeffress has long been a dominant model to account for the neural mechanisms of ITD detection. Recent research, however, suggests a wider range of strategies for ITD coding in the binaural auditory brainstem. We discuss how ITD is coded in avian, mammalian, and reptilian nervous systems, and review underlying synaptic and cellular properties that enable precise temporal computation. The latest advances in recording and analysis techniques provide powerful tools for both overcoming and utilizing the large field potentials in these nuclei.     

Binaural disparity cues available to the barn owl for sound localization

1. Bilateral recording of cochlear potentials was used to measure the variations in interaural time differences (ITDs) and interaural intensity differences (IIDs) as a free-field auditory stimulus was moved to different positions around a barn owl's head. 2. ITD varied smoothly with stimulus azimuth across a broad frequency range. 3. ITD varied minimally with stimulus elevation, except at extreme angles from the horizontal. 4. IID varied with both stimulus elevation and stimulus azimuth. Lower frequencies were more sensitive to variations in azimuth, whereas higher frequencies were more sensitive to variations in elevation. 5. The loci of spatial coordinates that form iso-IID contours and iso-ITD contours form a non-orthogonal grid that relates binaural disparity cues to sound location.     

Robustness of neuronal tuning to binaural sound localization cues against age-related loss of inhibitory synaptic inputs

Sound localization relies on minute differences in the timing and intensity of sound arriving at both ears. Neurons of the lateral superior olive (LSO) in the brainstem process these interaural disparities by precisely detecting excitatory and inhibitory synaptic inputs. Aging generally induces selective loss of inhibitory synaptic transmission along the entire auditory pathways, including the reduction of inhibitory afferents to LSO. Electrophysiological recordings in animals, however, reported only minor functional changes in aged LSO. The perplexing discrepancy between anatomical and physiological observations suggests a role for activity-dependent plasticity that would help neurons retain their binaural tuning function despite loss of inhibitory inputs. To explore this hypothesis, we use a computational model of LSO to investigate mechanisms underlying the observed functional robustness against age-related loss of inhibitory inputs. The LSO model is an integrate-and-fire type enhanced with a small amount of low-voltage activated potassium conductance and driven with (in)homogeneous Poissonian inputs. Without synaptic input loss, model spike rates varied smoothly with interaural time and level differences, replicating empirical tuning properties of LSO. By reducing the number of inhibitory afferents to mimic age-related loss of inhibition, overall spike rates increased, which negatively impacted binaural tuning performance, measured as modulation depth and neuronal discriminability. To simulate a recovery process compensating for the loss of inhibitory fibers, the strength of remaining inhibitory inputs was increased. By this modification, effects of inhibition loss on binaural tuning were considerably weakened, leading to an improvement of functional performance. These neuron-level observations were further confirmed by population modeling, in which binaural tuning properties of multiple LSO neurons were varied according to empirical measurements. These results demonstrate the plausibility that homeostatic plasticity could effectively counteract known age-dependent loss of inhibitory fibers in LSO and suggest that behavioral degradation of sound localization might originate from changes occurring more centrally.     

Neural mechanisms of sound localization in owls

Barn owls localize sound by using the interaural time difference of the horizontal plane and the interaural intensity difference for the vertical plane. The owl's auditory system possesses the two binaural cues in separate pathways in the brainstem. Owls use a process similar to cross-correlation to derive interaural time differences. Convergence of different frequency bands in the inferior colliculus solves the problems of phase-ambiguity which is inherent in cross-correlating periodic signals. The two pathways converge in the external nucleus of the inferior colliculus to give rise to neurons that are selective for combinations of the two cues. These neurons form a map of auditory space. The map projects to the optic tectum to form a bimodal map which, in turn, projects to a motor map for head turning. The visual system calibrates the auditory space map during ontogeny in which acoustic variables change. In addition to this tectal pathway, the forebrain can also control the sound-localizing behaviour.     

Study of sound localization by owls and its relevance to humans

Human psychoacoustical studies have been the main sources of information from which the brain mechanisms of sound localization are inferred. The value of animal models would be limited, if humans and the animals did not share the same perceptual experience and the neural mechanisms for it. Barn owls and humans use the same method of computing interaural time differences for localization in the horizontal plane. The behavioral performance of owls and its neural bases are consistent with some of the theories developed for human sound localization. Neural theories of sound localization largely owe their origin to the study of sound localization by humans, even though little is known about the physiological properties of the human auditory system. One of these ideas is binaural cross-correlation which assumes that the human brain performs a process similar to mathematical cross-correlation to measure the interaural time difference for localization in the horizontal plane. The most complete set of neural evidence for this theory comes from the study of sound localization and its brain mechanisms in barn owls, although partial support is also available from studies on laboratory mammals. Animal models of human sensory perception make two implicit assumptions; animals and humans experience the same percept and the same neural mechanism underlies the creation of the percept. These assumptions are hard to prove for obvious reason. This article reviews several lines of evidence that similar neural mechanisms must underlie the perception of sound locations in humans and owls.     

Perception of Binaural Cues Develops in Children Who Are Deaf through Bilateral Cochlear Implantation

There are significant challenges to restoring binaural hearing to children who have been deaf from an early age. The uncoordinated and poor temporal information available from cochlear implants distorts perception of interaural timing differences normally important for sound localization and listening in noise. Moreover, binaural development can be compromised by bilateral and unilateral auditory deprivation. Here, we studied perception of both interaural level and timing differences in 79 children/adolescents using bilateral cochlear implants and 16 peers with normal hearing. They were asked on which side of their head they heard unilaterally or bilaterally presented click- or electrical pulse- trains. Interaural level cues were identified by most participants including adolescents with long periods of unilateral cochlear implant use and little bilateral implant experience. Interaural timing cues were not detected by new bilateral adolescent users, consistent with previous evidence. Evidence of binaural timing detection was, for the first time, found in children who had much longer implant experience but it was marked by poorer than normal sensitivity and abnormally strong dependence on current level differences between implants. In addition, children with prior unilateral implant use showed a higher proportion of responses to their first implanted sides than children implanted simultaneously. These data indicate that there are functional repercussions of developing binaural hearing through bilateral cochlear implants, particularly when provided sequentially; nonetheless, children have an opportunity to use these devices to hear better in noise and gain spatial hearing.     

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.     

Minimal Conductance-Based Model of Auditory Coincidence Detector Neurons

Sound localization is a fundamental sensory function of a wide variety of animals. The interaural time difference (ITD), an important cue for sound localization, is computed in the auditory brainstem. In our previous modeling study, we introduced a two-compartment Hodgkin-Huxley type model to investigate how cellular and synaptic specializations may contribute to precise ITD computation of the barn owl''s auditory coincidence detector neuron. Although our model successfully reproduced fundamental physiological properties observed in vivo, it was unsuitable for mathematical analyses and large scale simulations because of a number of nonlinear variables. In the present study, we reduce our former model into three types of conductance-based integrate-and-fire (IF) models. We test their electrophysiological properties using data from published in vivo and in vitro studies. Their robustness to parameter changes and computational efficiencies are also examined. Our numerical results suggest that the single-compartment active IF model is superior to other reduced models in terms of physiological reproducibility and computational performance. This model will allow future theoretical studies that use more rigorous mathematical analysis and network simulations.     

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.     

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.     

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.     

Sound localization behavior of the green treefrog (Hyla cinerea) and the barking treefrog (H. gratiosa)

Summary Female treefrogs (Hyla cinerea andH. gratiosa) can accurately localize a sound source (playback of male mating calls) if both ears are intact. When the sensitivity of one eardrum is attenuated, by coating it with a thin layer of silicone grease, females no longer can locate the sound source. This study demonstrates that female anurans rely on interaural cues for localization of a calling male. The neural basis for an anuran's sound localization ability presumably involves binaural convergence on single cells in the central auditory nervous system.This work was supported by research grants from the National Science Foundation and the U.S. Public Health Service. The assistance of Anne J.M. Moffat in measuring the directional characteristics of the loudspeaker is gratefully appreciated.