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.     

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     

The role of pressure difference reception in the directional hearing of budgerigars (Melopsittacus undulatus)

In many birds, the middle ears are connected through an air-filled interaural pathway. Sound transmission through this pathway may improve directional hearing. However, attempts to demonstrate such a mechanism have produced conflicting results. One reason is that some species of birds develop a lower static air pressure in the middle ears when anaesthetized, which reduces eardrum vibrations. In anaesthetized budgerigars with vented interaural air spaces and presumed normal eardrum vibrations, we find that sound propagating through the interaural pathway considerably improves cues to the directional hearing. The directional cues in the received sound combined with amplitude gain and time delay of sound propagating through the interaural pathway quantitatively account for the observed dependence of eardrum vibration on direction of sound incidence. Interaural sound propagation is responsible for most of the frontal gradient of eardrum vibration (i.e. when a sound source is moved from a small contralateral angle to the same ipsilateral angle). Our study confirms that at low frequencies the interaural sound propagation may cause vibrations of the eardrum to differ much in time, thus providing a possible cue for directional hearing. The acoustically effective size of the head of our birds (diameter 28 mm) is much larger than expected from the dimensions of the skull, so apparently the feathers on the head have a considerable acoustical effect.Dedicated to Professor Franz Huber on the occasion of his 80th birthday.     

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     

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     

AEPs at the onset and offset of repetitive sound modulation,due to mismatch with the contents of an auditory sensory store

Long latency auditory evoked potentials (AEPs), chiefly consisting of a negative peak at about 150 msec and a positivity at 250 msec, were recorded at the beginning and end of periods during which the interaural time difference of binaural noise was switched between 0.0 and 0.8 msec at a fast rate (ISI = 50 or 25 msec) or the frequency of continuous binaural clicks was switched between 167 and 200 Hz every 80, 50 or 25 msec. In the latter case the offset responses occurred later than onset by a mean of 89, 47 and 27 msec respectively, suggesting they were probably generated at the moment the next switch was expected but failed to occur.The offset responses must be non-specific with respect to the interaural delay or the frequency of clicks, since neurones which respond to particular delays or frequencies and are made refractory by a rapid rate of stimulation should not suddenly become less so at the last in a series of identical stimuli, or be activated by the absence of a further event. It is proposed that the potentials are due to a higher order of neurone which automatically responds to the occurrence of a “mismatch” between the immediate sound and an image of that which was previously present, encoded in a short-term sensory store. In addition to frequency content and interaural delay, the image must contain information about the temporal modulation pattern of the sound over the previous few seconds.     

Tuning bat LSO neurons to interaural intensity differences through spike-timing dependent plasticity

Bats, like other mammals, are known to use interaural intensity differences (IID) to determine azimuthal position. In the lateral superior olive (LSO) neurons have firing behaviors which vary systematically with IID. Those neurons receive excitatory inputs from the ipsilateral ear and inhibitory inputs from the contralateral one. The IID sensitivity of a LSO neuron is thought to be due to delay differences between the signals coming from both ears, differences due to different synaptic delays and to intensity-dependent delays. In this paper we model the auditory pathway until the LSO. We propose a learning scheme where inputs to LSO neurons start out numerous with different relative delays. Spike timing-dependent plasticity (STDP) is then used to prune those connections. We compare the pruned neuron responses with physiological data and analyse the relationship between IID’s of teacher stimuli and IID sensitivities of trained LSO neurons.     

Sensory cues for sound localization in the cricket<Emphasis Type="Italic"> Teleogryllus oceanicus</Emphasis>: interaural difference in response strength versus interaural latency difference

Two potential sensory cues for sound location are interaural difference in response strength (firing rate and/or spike count) and in response latency of auditory receptor neurons. Previous experiments showed that these two cues are affected differently by intense prior stimulation; the difference in response strength declines and may even reverse in sign, but the difference in latency is unaffected. Here, I use an intense, constant tone to disrupt localization cues generated by a subsequent train of sound pulses. Recordings from the auditory nerve confirm that tone stimulation reduces, and sometimes reverses, the interaural difference in response strength to subsequent sound pulses, but that it enhances the interaural latency difference. If sound location is determined mainly from latency comparison, then behavioral responses to a pulse train following tone stimulation should be normal, but if the main cue for sound location is interaural difference in response strength, then post-tone behavioral responses should sometimes be misdirected. Initial phonotactic responses to the post-tone pulse train were frequently directed away from, rather than towards, the sound source, indicating that the dominant sensory cue for sound location is interaural difference in response strength.     

Forecast ability of the auditory system during perception of gradually or abruptly moving short sound images

The ability to localize endpoints of sound image trajectories was studied in comparison with stationary sound image positions. Sound images moved either gradually or abruptly to the left or right from the head midline. Different types of sound image movement were simulated by manipulating the interaural time delay. Subjects were asked to estimate the position of the virtual sound source, using the graphic tablet. It was revealed that the perceived endpoints of the moving sound image trajectories, like stationary stimulus positions, depended on the interaural time delay. The perceived endpoints of the moving sound images simulated by stimuli with the final interaural time delay lower than 200 micros were displaced further from the head midline as compared to stationary stimuli of the same interaural time delays. This forward displacement of the perceived position of the moving target can be considered as "representational momentum" and can be explained by mental extrapolation of the dynamic information, which is necessary for successive sensorimotor coordination. For interaural time delays above 400 micros, final positions of gradually and abruptly moving sound sources were closer to the head midline than corresponding stationary sound image position. When comparing the results of both duration conditions, it was shown that in case of longer stimuli the endpoints of gradually moving sound images were lateralized further from the head midline for interaural time delays above 400 micros.     

Binaural masking and sensitivity to interaural delay in the inferior colliculus.

The binaural masking level difference (BMLD) is a psychophysical effect whereby signals masked by a noise at one ear become unmasked by sounds reaching the other. BMLD effects are largest at low frequencies where they depend on signal phase, suggesting that part of the physiological mechanism responsible for the BMLD resides in cells that are sensitive to interaural time disparities. We have investigated a physiological basis for unmasking in the responses of delay-sensitive cells in the central nucleus of the inferior colliculus in anaesthetized guinea pigs. The masking effects of a binaurally presented noise, as a function of the masker delay, were quantified by measuring the number of discharges synchronized to the signal, and by measuring the masked threshold. The noise level for masking was lowest at the best delay for the noise. The mean magnitude of the unmasking across our neural population was similar to the human psychophysical BMLD under the same signal and masker conditions.     

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 Neural Code for Auditory Space Depends on Sound Frequency and Head Size in an Optimal Manner

A major cue to the location of a sound source is the interaural time difference (ITD)–the difference in sound arrival time at the two ears. The neural representation of this auditory cue is unresolved. The classic model of ITD coding, dominant for a half-century, posits that the distribution of best ITDs (the ITD evoking a neuron’s maximal response) is unimodal and largely within the range of ITDs permitted by head-size. This is often interpreted as a place code for source location. An alternative model, based on neurophysiology in small mammals, posits a bimodal distribution of best ITDs with exquisite sensitivity to ITDs generated by means of relative firing rates between the distributions. Recently, an optimal-coding model was proposed, unifying the disparate features of these two models under the framework of efficient coding by neural populations. The optimal-coding model predicts that distributions of best ITDs depend on head size and sound frequency: for high frequencies and large heads it resembles the classic model, for low frequencies and small head sizes it resembles the bimodal model. The optimal-coding model makes key, yet unobserved, predictions: for many species, including humans, both forms of neural representation are employed, depending on sound frequency. Furthermore, novel representations are predicted for intermediate frequencies. Here, we examine these predictions in neurophysiological data from five mammalian species: macaque, guinea pig, cat, gerbil and kangaroo rat. We present the first evidence supporting these untested predictions, and demonstrate that different representations appear to be employed at different sound frequencies in the same species.     

Discrimination of the dynamic properties of sound source spatial location in humans: Electrophysiology and psychophysics

The spatial resolution of the human auditory system was studied under conditions, where the location of the sound source was changed according to different temporal patterns of interaural time delay. Two experimental procedures were run in the same group of subjects: a psychophysical procedure (the transformed staircase method) and an electrophysiological one (which requires recording of mismatch negativity, the auditory evoked response component). It was established that (1) the value of the mismatch negativity reflected the degree of spatial deviation of the sound source; (2) the mismatch negativity was elicited even at minimum (20μs) interaural time delays under both temporal patterns (abrupt azimuth change and gradual sound movement at different velocities); (3) an abrupt change of the sound source azimuth resulted in a greater mismatch negativity than gradual sound movement did if the interaural time delay exceeded 40 μs; (4) the discrimination threshold values of the interaural delay obtained in the psychophysical procedure were greater than the minimum interaural delays that elicited mismatch negativity, with the exception of the expert listeners, who exhibited no significant difference.     

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.     

Intramodal and interaural specificity of the human slow auditory evoked potential

Parameters of slow auditory evoked potentials (SAEPs) recorded during monotonic monaural stimulation and a programmed change in the frequency of successive tonal stimuli were compared. In one variant of polytonic stimulation, besides the frequency, the side of stimulation also was changed (alternation). During polytonic stimulation the amplitude of the SAEPs was greater than during monotonic. Maximal amplitudes were found during alternating polytonic stimulation. A decrease in the variability of amplitude of the SAEPs and an increase in their peak latencies were observed during polytonic stimulation. It is concluded that SAEPs are characterized by intramodal and interaural specificity. The tonotopic and bilaterally symmetrical organizations of the system of SAEP generation can be demonstrated more satisfactorily at low sound intensities. Data indicating that neuron populations of the system of SAEP generation, perceiving tonal stimuli which differ very little from each other "overlap" to a greater degree than populations perceiving more different sounds, are given, The data on intramodal and interaural specificity of the SAEP are discussed from the standpoint of its extralemniscal origin.State Postgraduate Medical Institute, Tbilisi. Translated from Neirofiziologiya, Vol. 9, No. 5, pp. 460–468, September–October, 1977.     

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.     

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.     

Black‐capped chickadees Poecile atricapillus sing at higher pitches with elevated anthropogenic noise,but not with decreasing canopy cover

Several songbird species sing at higher frequencies (i.e. higher pitch) when anthropogenic noise levels are elevated. Such frequency shifting is thought to be an adaptation to prevent masking of bird song by anthropogenic noise. However, no study of this phenomenon has examined how vegetative differences between noisy and quiet sites influence frequency shifting. Variation in vegetative structure is important because the acoustic adaptation hypothesis predicts that birds in more open areas should also sing at higher frequencies. Thus, vegetative structure may partially explain the observation of higher frequency songs in areas with high levels of anthropogenic noise. To distinguish between frequency shifting due to noise or vegetative structure we recorded the songs of black‐capped chickadees Poecile atricapillus vocalizing in high and low noise sites with open and closed canopy forests. Consistent with the noise‐dependent frequency hypothesis, black‐capped chickadees sang at higher frequencies in high noise sites than in low noise sites. In contrast, birds did not sing at higher frequencies in sites with more open canopies. These results suggest that frequency shifting in chickadees is more strongly related to ambient noise levels than to vegetative structure. A second frequency measure, inter‐note ratio, was reduced at higher levels of canopy cover. We speculate that this may be due to a non‐random distribution of dominant males. In sum, our results support the hypothesis that some birds sing at higher frequencies to avoid overlap with anthropogenic noise, but suggest that vegetative structure may play a role in the modification of other song traits.     

Reassessing mechanisms of low-frequency sound localisation

Interaural time differences (ITDs) are the dominant cues for human localisation of low-frequency sounds. Although a mechanism for ITD processing proposed in 1948 seems applicable to birds, and is consistent with many aspects of the responses found in mammals, recent data suggest that key tenets of the model might need to be reconsidered. The model requires, at every frequency, a distribution of cells with firing rate peaks across all ITD values within the animal's physiological range. The ITD tuning relies on internal delays in the form of a neural delay line. The evidence for such a delay line structure in mammals is not as convincing as it is in birds and, in some small animals the full range of physiological ITDs are not fully represented by peak firing of neurones at every frequency channel. Alternative means of achieving internal delays such as inhibitory inputs or the delays associated with cochlear filtering are being considered.     

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