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.     

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.     

Regularly firing neurons in the inferior colliculus have a weak interaural intensity difference sensitivity

The spike discharge regularity may be important in the processing of information in the auditory pathway. It has already been shown that many cells in the central nucleus of the inferior colliculus fire regularly in response to monaural stimulation by the best frequency tones. The aim of this study was to find how the regularity of units was affected by adding ipsilateral tone, and how interaural intensity difference sensitivity is related to regularity. Single unit recordings were performed from 66 units in the inferior colliculus of the anaesthetized guinea pig in response to the best frequency tone. Regularity of firing was measured by calculating the coefficient of variation as a function of time of a unit’s response. There was a positive correlation between coefficient of variation and interaural intensity difference sensitivity, indicating that highly regular units had very weak and irregular units had strong interaural intensity difference sensitivity responses. Three effects of binaural interaction on the sustained regularity were observed: constant coefficient of variation despite change in rate (66% of the units), negative (20%) and positive (13%) rate–CV relationships. A negative rate-coefficient of variation relationship was the dominant pattern of binaural interaction on the onset regularity.     

Sensitivity to spectral interaural intensity difference cues in space-specific neurons of the barn owl

Barn owls use interaural intensity differences to localize sounds in the vertical plane. At a given elevation the magnitude of the interaural intensity difference cue varies with frequency, creating an interaural intensity difference spectrum of cues which is characteristic of that direction. To test whether space-specific cells are sensitive to spectral interaural intensity difference cues, pure-tone interaural intensity difference tuning curves were taken at multiple different frequencies for single neurons in the external nucleus of the inferior colliculus. For a given neuron, the interaural intensity differences eliciting the maximum response (the best interaural intensity differences) changed with the frequency of the stimulus by an average maximal difference of 9.4±6.2 dB. The resulting spectral patterns of these neurally preferred interaural intensity differences exhibited a high degree of similarity to the acoustic interaural intensity difference spectra characteristic of restricted regions in space. Compared to stimuli whose interaural intensity difference spectra matched the preferred spectra, stimuli with inverted spectra elicited a smaller response, showing that space-specific neurons are sensitive to the shape of the spectrum. The underlying mechanism is an inhibition for frequency-specific interaural intensity differences which differ from the preferred spectral pattern. Collectively, these data show that space-specific neurons are sensitive to spectral interaural intensity difference cues and support the idea that behaving barn owls use such cues to precisely localize sounds.Abbreviations ABI average binaural intensity - HRTF head-related transfer function - ICx external nucleus of the inferior colliculus - IID interaural intensity difference - ITD interaural time difference - OT optic tectum - RMS root mean square - VLVp nucleus ventralis lemnisci laterale, pars posterior     

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.     

Tactile-spatial and cross-modal attention effects in the primary somatosensory cortical areas 3b and 1-2 of rhesus monkeys

Neuronal responses in somatosensory cortical areas 3b and 1-2 (S1) were recorded during an attention task involving cue directed selection of one of three simultaneous stimuli: dual sinewave shaped vibrotactile stimuli applied to mirror sites on both hands or a similarly timed auditory tone. The cued stimulus occurred with one of two equally probable patterns: a constant amplitude vibration or the latter with a superimposed brief sinewave amplitude pulse midway during stimulation. Uncued stimuli always contained amplitude pulses. Two monkeys signaled the absence or presence of an amplitude pulse by appropriately moving a foot pedal up or down. Cues initiated trials by marking the location where the monkey had to discriminate the stimulus pattern. Cue location and stimulus pattern varied randomly per trial. Approximately 50% of cells (44/77 in 3b and 39/77 in 1-2) had significantly different firing rates to stimulation cued to the contralateral hand relative to spatially cuing the ipsilateral hand or cross-modally the auditory stimulus. Relatively suppressed firing rates during times prior to the epoch containing amplitude pulses improved signal-to-noise ratios for responses to amplitude pulses. Instances of significant enhanced activity during and after intervals with amplitude pulses were rare and relative to suppressed activity when cues directed attention to the ipsilateral hand or auditory stimulus. The present findings suggest that attention influences even the earliest stage somatosensory cortical processing. Findings were more modest in S1 than those previously seen in S2 (Burton et al., Somatosens Mot Res 14: 237-267, 1997), which supports the concept of multistage attention processes for touch.     

Meeting report

Neuronal responses in somatosensory cortical areas 3b and 1- 2 (S1) were recorded during an attention task involving cue directed selection of one of three simultaneous stimuli: dual sinewave shaped vibrotactile stimuli applied to mirror sites on both hands or a similarly timed auditory tone. The cued stimulus occurred with one of two equally probable patterns: a constant amplitude vibration or the latter with a superimposed brief sinewave amplitude pulse midway during stimulation. Uncued stimuli always contained amplitude pulses. Two monkeys signaled the absence or presence of an amplitude pulse by appropriately moving a foot pedal up or down. Cues initiated trials by marking the location where the monkey had to discriminate the stimulus pattern. Cue location and stimulus pattern varied randomly per trial. Approximately 50% of cells (44/77 in 3b and 39/77 in 1- 2) had significantly different firing rates to stimulation cued to the contralateral hand relative to spatially cuing the ipsilateral hand or cross-modally the auditory stimulus. Relatively suppressed firing rates during times prior to the epoch containing amplitude pulses improved signal-to-noise ratios for responses to amplitude pulses. Instances of significant enhanced activity during and after intervals with amplitude pulses were rare and relative to suppressed activity when cues directed attention to the ipsilateral hand or auditory stimulus. The present findings suggest that attention influences even the earliest stage somatosensory cortical processing. Findings were more modest in S1 than those previously seen in S2 (Burton et al. , Somatosens Mot Res 14 : 237-267, 1997), which supports the concept of multistage attention processes for touch.     

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.     

Long rise times of sound pulses in grasshopper songs improve the directionality cues received by the CNS from the auditory receptors

Auditory receptors of the locust (Locusta migratoria) were investigated with respect to the directionality cues which are present in their spiking responses, with special emphasis on how directional cues are influenced by the rise time of sound signals. Intensity differences between the ears influence two possible cues in the receptor responses, spike count and response latency. Variation in rise time of sound pulses had little effect on the overall spike count; however, it had a substantial effect on the temporal distribution of the receptor's spiking response, especially on the latencies of first spikes. In particular, with ramplike stimuli the slope of the latency vs. intensity curves was steeper as compared to stimuli with steep onsets (Fig. 3). Stimuli with flat ramplike onsets lead to an increase of the latency differences of discharges between left and right tympanic receptors. This type of ramplike stimulus could thus facilitate directional hearing. This hypothesis was corroborated by a Monte Carlo simulation in which the probability of incorrect directional decisions was determined on the basis of the receptor latencies and spike counts. Slowly rising ramps significantly improved the decisions based on response latency, as compared to stimuli with sudden onsets (Fig. 4). These results are compared to behavioural results obtained with the grasshopper Ch. biguttulus. The stridulation signals of the females of this species consist of ramplike pulses, which could be an adaptation to facilitate directional hearing of phonotactically approaching males.Abbreviations HFR high frequency receptor - ILD interaural level difference - LFR low frequency receptor - SPL sound pressure level - WN white noise     

Echoic Memory: Investigation of Its Temporal Resolution by Auditory Offset Cortical Responses

Previous studies showed that the amplitude and latency of the auditory offset cortical response depended on the history of the sound, which implicated the involvement of echoic memory in shaping a response. When a brief sound was repeated, the latency of the offset response depended precisely on the frequency of the repeat, indicating that the brain recognized the timing of the offset by using information on the repeat frequency stored in memory. In the present study, we investigated the temporal resolution of sensory storage by measuring auditory offset responses with magnetoencephalography (MEG). The offset of a train of clicks for 1 s elicited a clear magnetic response at approximately 60 ms (Off-P50m). The latency of Off-P50m depended on the inter-stimulus interval (ISI) of the click train, which was the longest at 40 ms (25 Hz) and became shorter with shorter ISIs (2.5∼20 ms). The correlation coefficient r² for the peak latency and ISI was as high as 0.99, which suggested that sensory storage for the stimulation frequency accurately determined the Off-P50m latency. Statistical analysis revealed that the latency of all pairs, except for that between 200 and 400 Hz, was significantly different, indicating the very high temporal resolution of sensory storage at approximately 5 ms.     

Pressure sensation by an anterior pagoda neuron population distributed in multiple ganglia in the leech, Whitmania pigra

Sensory processing of pressure signals in the central nervous system of the leech, Whitmania pigra, was studied through the interaction between pressure sensory neurons and anterior pagoda neurons. The responses of anterior pagoda neurons to one pulse or a train of pulses in pressure sensory neurons were characterized by the latency and amplitude of excitatory postsynaptic potentials. Here we show that each pressure sensory neuron is able to activate all the anterior pagoda neurons throughout the leech central nervous system. The response patterns of all anterior pagoda neurons were appropriate to the pressure location: in the longitudinal direction the anterior pagoda neuron further away from the pressure sensory neuron had a smaller response with longer latency; inside each ganglion, the anterior pagoda neuron on the contralateral side had a larger response with shorter latency than that on the ipsilateral side. All anterior pagoda neurons excited by pressure sensory neurons comprised a parallel system in which each anterior pagoda neuron was independent from the others. The location information of pressure stimuli was represented through the response of all 40 anterior pagoda neurons covering the whole leech body with a specific pattern of latency and amplitude.     

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.     

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     

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.     

A Dominance Hierarchy of Auditory Spatial Cues in Barn Owls

Background

Barn owls integrate spatial information across frequency channels to localize sounds in space.

Methodology/Principal Findings

We presented barn owls with synchronous sounds that contained different bands of frequencies (3–5 kHz and 7–9 kHz) from different locations in space. When the owls were confronted with the conflicting localization cues from two synchronous sounds of equal level, their orienting responses were dominated by one of the sounds: they oriented toward the location of the low frequency sound when the sources were separated in azimuth; in contrast, they oriented toward the location of the high frequency sound when the sources were separated in elevation. We identified neural correlates of this behavioral effect in the optic tectum (OT, superior colliculus in mammals), which contains a map of auditory space and is involved in generating orienting movements to sounds. We found that low frequency cues dominate the representation of sound azimuth in the OT space map, whereas high frequency cues dominate the representation of sound elevation.

Conclusions/Significance

We argue that the dominance hierarchy of localization cues reflects several factors: 1) the relative amplitude of the sound providing the cue, 2) the resolution with which the auditory system measures the value of a cue, and 3) the spatial ambiguity in interpreting the cue. These same factors may contribute to the relative weighting of sound localization cues in other species, including humans.     

GABA能抑制调制大棕蝠下丘听神经元时间编码模式

大棕幅（Eptesicus fuscus）下丘神经元对重复率为10pps(pulse per second）、30pps的串声刺激均产生跟随反应,但对90pps串声刺激的跟随反应则不尽相同,微电泳bicuculline阻断GABA能抑制作用后,所记录的58个神经元中,有13个（22％）放电率及串声刺激反应模式无;45个（78％）神经元放电率有不同程度的增加。对10pps、30pps串声刺激仍能产生跟随反应,但对90pps串声刺激的跟随反应模式有多种变化。其中：17个（29％）神经元为放电率增加的跟随反应;9个（15％）神经元放电率增加,对前100ms的串刺激产生反应且放电密集,而对随后200ms的串刺激只产生少量的放电;15个（26％）神经元放电率增加,在前几十毫秒范围内有较多的放电反应,后续的反应很弱;4个（7％）神经元只对第一个声刺激产生反应,且放电率增加,随后放电急剧减少。结果提示中脑下丘神经元对听觉信息的时间编码可能具有更复杂的机理。     

The directionality of the ear of the pigeon (Columba livia)

Summary The directionality of cochlear microphonic potentials in the azimuthal plane was investigated in the pigeon (Columba livia), using acoustic free-field stimulation (pure tones of 0.25–6 kHz).At high frequencies in the pigeon's hearing range (4–6 kHz), changing azimuth resulted in a maximum change of the cochlear microphonic amplitude by about 20 dB (SPL). The directionality decreased clearly with decreasing frequency.Acoustic blocking of the contralateral ear canal could reduce the directional sensitivity of the ipsilateral ear by maximally 8 dB. This indicates a significant sound transmission through the bird's interaural pathways. However, the magnitude of these effects compared to those obtained by sound diffraction (maximum > 15 dB) suggests that pressure gradients at the tympanic membrane are only of subordinate importance for the generation of directional cues.The comparison of interaural intensity differences with previous behavioral results confirms the hypothesis that interaural intensity difference is the primary directional cue of azimuthal sound localization in the high-frequency range (2–6 kHz).Abbreviations CM cochlear microphonic potential - IID interaural intensity difference - IID-MRA minimum resolvable angle calculated from interaural intensity difference - MRA minimum resolvable angle - OTD interaural ongoing time difference - RMS root mean square - SPL sound pressure level     

Innovative biomechanics for directional hearing in small flies

In humans and animals alike, the localization of sound constitutes a fundamental processing task of the auditory system. Directional hearing relies on acoustic cues such as the interaural amplitude and time differences and also, sometimes, the signal spectral composition. In small animals, such as insects, the auditory receptors are forcibly set close together, a design constraint imposing very short interaural distances. Due to the physics of sound propagation, the close proximity of the sound receivers results in vanishingly small amplitude and time cues. Yet, because of their directionality, small auditory systems embed original and innovative solutions that can be of inspirational value to some acute problems of technological miniaturization. Such ears are found in a parasitoid fly that acoustically locates its singing cricket host. Anatomically rather unconventional, the fly's auditory system is endowed with a directional sensitivity that is based on the mechanical coupling between its two hemilateral tympanal membranes. The functional principle permitting this directionality may be of particular relevance for technological applications necessitating sensors that are low cost, low weight, and low energy. Based on silicon-etching technology, early prototypes of sub-millimeter acoustic sensors provide evidence for directional mechanical responses. Further developments hold the promise of applications in hearing aid technology, vibration sensors, and miniature video-acoustic surveillance systems.     

Constraints on the coding of sound frequency imposed by the avian interaural canal

Summary Extracellular recordings were made from the midbrain auditory area to determine the limits of auditory frequency sensitivity in a variety of birds. The audiograms of some species show a consistent missing frequency range of 1/3 to 1/2 an octave, to which no neurons are tuned. All species, except owls, have a low upper frequency limit in comparison with mammals of similar headwidth. A consideration of both the upper frequency limits and the missing frequency ranges led to the conclusion that frequencies which do not generate localization cues are not represented in the midbrain. The upper frequency limit appears to match the upper limit of generation of significant interaural and monaural intensity cues to localization. The variation of these cues with frequency was examined through a simple model of the birds' sound receiving system which incorporated the interaural canal and considered the tympanic membranes as pressure difference receivers. Apart from coraciiform species, which have low upper frequency limits matching the frequency of the primary missing frequency band of other species, and owls, which have high upper frequency limits, the upper frequency limits of the birds studied are inversely related to head-width.The argument for missing frequency ranges being related to nonlocalizable frequencies is simpler, for it has been found previously, using cochlear microphonic recording, that within a bird's audiogram there are frequency regions with poor directionality cues. These regions appear to correspond to the missing frequency ranges.Abbreviation nMLD nucleus mesencephalicus lateralis dorsalis